FEMS Microbiology Reviews 24 (2000) 225^249

www.fems-microbiology.org

The roots of microbiology and the in£uence of Ferdinand Cohn on

microbiology of the 19th century
Gerhart Drews *
Institute of Biology 2, Microbiology, Schaenzlestr. 1, D-79104 Freiburg, Germany

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

Received 9 June 1999; received in revised form 5 January 2000; accepted 6 January 2000

Abstract

The beginning of modern microbiology can be traced back to the 1870s, and it was based on the development of new concepts that
originated during the two preceding centuries on the role of microorganisms, new experimental methods, and discoveries in chemistry,
physics, and evolutionary cell biology. The crucial progress was the isolation and growth on solid media of clone cultures arising from single
cells and the demonstration that these pure cultures have specific, inheritable characteristics and metabolic capacities. The doctrine of the
spontaneous generation of microorganisms, which stimulated research for a century, lost its role as an important concept. Microorganisms
were discovered to be causative agents of infectious diseases and of specific metabolic processes. Microscopy techniques advanced studies on
microorganisms. The discovery of sexuality and development in microorganisms and Darwin's theory of evolution contributed to the
founding of microbiology as a science. Ferdinand Cohn (1828^1898), a pioneer in the developmental biology of lower plants, considerably
promoted the taxonomy and physiology of bacteria, discovered the heat-resistant endospores of bacilli, and was active in applied
microbiology. ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.

Keywords : Concepts in microbiology ; Infectious disease ; Spontaneous generation ; Inheritable feature; Taxonomy of bacteria ; Physiological diversity ;
Bacillus endospore ; Ferdinand Cohn

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
2. The roots of modern science originated in the 17th and 18th centuries . . . . . . . . . . . . . . . 226
3. The progress of biology in the 19th century . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
3.1. The progress in chemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
3.2. Anatomy, microscopy, developmental cell biology, and sexuality . . . . . . . . . . . . . . . . 227
3.3. The development of the evolutionary view in biology . . . . . . . . . . . . . . . . . . . . . . . . . 228
4. The discovery of microorganisms and their ¢rst classi¢cation . . . . . . . . . . . . . . . . . . . . . . 229
4.1. The bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
4.2. The fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
4.3. The protozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231
5. The concepts of taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231
5.1. The species problem in bacteriology and new concepts for classi¢cation . . . . . . . . . . . 231
6. Spontaneous generation vs. evolution of microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . 235
7. The concepts of biological diversity of bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238
7.1. The organismic and chemical theories of fermentation . . . . . . . . . . . . . . . . . . . . . . . . 238
7.2. Autotrophy, chemolithotrophy, and phototrophy . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
7.3. Putrefaction and pathogenicity of bacteria, and immunology . . . . . . . . . . . . . . . . . . . 240
8. The achievements of Ferdinand Cohn . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246

* Tel. : +49 (761) 2032607; Fax: +49 (761) 2032779; E-mail : drews@pop3.uni-freiburg.de

0168-6445 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 6 4 4 5 ( 0 0 ) 0 0 0 2 6 - 7

FEMSRE 678 29-5-00

226 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
1. Introduction
Progress in science has never been a continuous process.
Discoveries, revolutionary ideas, and new concepts were
very often neglected, misunderstood, or attacked if they
did not follow the mainstream of the time. Although bac-
teria were discovered by observation under the microscope
in the 17th century, they were believed to generate sponta-
neously and to be transformed into other morphological
and physiological types (pleomorphism). It was not clear
whether bacteria and other infusoria were the cause or the
products of biological or chemical processes. Discussions
on controversial concepts initiated experimental work to
prove or disprove theories. Rational empiricism slowly
overcame speculative reasoning.
2. The roots of modern science originated in the 17th and
18th centuries
In the 17th century, people began to trust the testimony
of nature more than the testimony of human ideas. A
scientist proceeds from the evidence of his own observa-
tion, but also from the basis of human written authority.
Modern empiricism was borne on the concept that proper
knowledge ought to be derived from a direct sensory ex-
perience of reality in nature. The inductive method for
scienti¢c work in which the conclusion is based on obser-
vations and measurements was proposed by Francis Ba-
con (1561^1626). The classical method of deduction,
which solved scienti¢c problems by sharp reasoning, was
still in use then, but empirical research was favored. Renë
Descartes (1596^1650) propagated that conclusions were
only valid if they could be mathematically proven (in Prin-
ciples of Philosophy, published in 1644). It was still a long
road to the modern ideas that there is no absolute truth in
biology and that a working hypothesis disproved by ex-
perimental evidence has to be replaced by a new hypoth-
esis.
Galileo Galilei's Discourse Concerning Two New Scien-
ces (1620), Robert Boyle's Excellence and Grounds of the
Mechanical Hypothesis (1666), and Isaac Newton's (1643^
1727) Mathematical Principles of Natural Philosophy
(1687) introduced a mechanistic view of nature. Physical
forces were put forth as the cause of biological processes.
There was no dissonance between reductive causal explan-
ation, the omnipresence of God and his part in the vital
principle, and mathematical abstraction. In addition to the
material world, the spiritual world was stressed by Baruch
Spinoza (1632^1677).
Gottfried Wilhelm Leibniz (1646^1716), who reacted
positively to the discovery of the world of microorganisms,
tried to harmonize religious belief with the aspects of the
new science. The animalcules were designated as a very
low order of monads. The philosophers of that time found
in the revelations of the microscope a way to combine the
FEMSRE 678 29-5-00
natural and supernatural worlds and to place the knowl-
edge of nature within theological space [1]. The mechanis-
tic-materialistic view was supported and extended by
Georges Louis Leclerc Comte de Bu¡on (1707^1788),
who published a universal history of nature with descrip-
tions from minerals up to humans (Histoire Naturelle,
Gënëral et Particulie©re, 1749^1804, 54 volumes, completed
by Etienne de Lacëpe©de after Bu¡on's death). Bu¡on
stressed the importance of fossils as witnesses of earlier
periods of life on earth, but he denied the descent of extant
organisms from those of earlier periods because bastards
are sterile and evidence of intermediates between present
and extinct forms was lacking. He believed the Newtonian
concept that organic molecules from the decomposition of
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
organisms generate or can be incorporated into a new
organism [2]. In his work both the inductive method and
the deductive method were used. By the end of the 17th
century, even those naturalists and philosophers in£uenced
by the mechanical perception of nature doubted Descartes'
e¡ort to derive the generation of animals from a mecha-
nistic nature [3].
Scientists who preferred the inductive method were con-
fronted with problems such as how precarious instrumen-
tally mediated experience could be and how much work
was required to declare observations as reliable. Another
problem accompanying the more modern use of individual
sensory experience was the evaluation of traditionally es-
tablished knowledge [1,3^5].
Although the inductive method was used more and
more in research, philosophers and many scientists, in£u-
enced by philosophical ideas, believed until far into the
19th century that they could solve biological problems
by reasoning and explain physiological functions by un-
clearly de¢ned abstract terms like `vital forces'. Immanuel
Kant (1724^1804) believed that in our thoughts we pass
from a mechanistic view of the parts to a teleological view
of the whole, and we cannot separate these classes of view;
there is a hidden basic principle of nature which unites the
mechanistic and teleological views. Georg Christoph Lich-
tenberg (1742^1799), a mathematician and physicist in
Go«ttingen, should be mentioned because he personi¢ed
the experimenter who was critical and skeptical of his
own results and rejected any speculative philosophy. He
represented an example of the English empiricism in the
age of enlightenment.
3. The progress of biology in the 19th century
In the 19th century, many biologists made an imperfect
fusion of the Kantian scheme with materialism, as for
example by the `Naturphilosophen' such as Lorenz Oken
(1779^1851), who contributed considerably to embryol-
ogy, but who tried to construct a biology that could re£ect
the action of the human mind in the animal kingdom and
who considered `natural sciences as the science of the eter-
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
nal transubstantiation of God in the world' (1848); Gott-
fried D. Nees von Esenbeck (1776^1858); and Carl Gustav
Carus (1789^1869), who made careful comparative studies
in di¡erent ¢elds, but tried to explain biological phenom-
ena by teleological principles. These men proposed `ideal
forms' and linked them with the conception of the purpose
that is inherent in living things. The ideas of Naturphilo-
sophie, which dominated in the ¢rst half of the 19th cen-
tury, especially in Germany, were replaced by the unifying
idea of natural sciences in order to discover the laws of
nature and to rule humanity. One exponent of this think-
ing was the German pathologist and anthropologist Ru-
dolf Virchow (1821^1902) [5,6].
3.1. The progress in chemistry
In addition to the mechanistic view of biological pro-
cesses, the beginning of chemical analysis was important
for the progress in biological research. Antoine Laurent
Lavoisier (1743^1794) disproved the phlogiston theory of
Georg Ernst Stahl (1660^1734) by determining the weights
of products from chemical reactions. Oxygen, dinitrogen,
and carbon dioxide were discovered as components of air.
Joseph Gay-Lussac (1778^1850) isolated the metals of the
alkaline-earth group and formulated the law of combining
volumes of gases. In 1811, Amadeo Avogadro described
the distinction between molecules and atoms and proposed
the concept that equal volumes of di¡erent gases contain
the same number of particles under the same physical
conditions. The modern system of chemical symbols and
formulas was developed and many new elements were dis-
covered by Jo«ns Berzelius (1779^1848). He also coined the
term `catalysis' for a process in which a compound a¡ects
the velocity of a chemical reaction, but remains unchanged
and does not contribute to the substrate or products of the
reaction. Friedrich Wo«hler (1800^1882) and Justus von
Liebig (1803^1873) strongly in£uenced biology through
their analysis and synthesis of organic compounds and
by disproving the role of a vital power in the synthesis
of organic compounds. They refuted, however, the role
of microorganisms in fermentation and putrefaction and
proposed, instead of `the metamorphosis' by an organic
product of decomposition, the `ferment'.
Although bioenergetics and thermodynamics were not
included in textbooks until late in the 19th century and
thermodynamic calculations were not considered for met-
abolic processes, the unde¢ned and obscure term `vital
force' was replaced by the understanding that activities
of living things require the performance of work, whether
chemical, mechanical, osmotic, or electric [7]. The theory
of heat and conservation and the correlation of energy was
proposed by Julius Robert Mayer in 1845 and the law of
the conservation of energy and the calculation of heat
units were proposed by Hermann L. Helmholtz in 1846
and James Prescott Joule in 1843. Scientists slowly became
aware that energy is supplied by metabolism, respiration,
FEMSRE 678 29-5-00
227
fermentation, and photosynthesis, but the problem of en-
ergy coupling, i.e. the linkage between energy-yielding and
energy-consuming processes, was not resolved before the
1940s and 1960s.
3.2. Anatomy, microscopy, developmental cell biology, and
sexuality
In the 16th to 18th centuries, the great diversity of
plants and animals was recognized and the anatomy of
humans, animals, and plants was described in numerous
comprehensive articles.
The ¢rst microscopes consisting of one or two optical
lenses were build by Johannes and Zacharias Janssen
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
about 1590. The propagation of light and its re£ection
and refraction by an optical lens has been known since
the work of Christian Huygens (1629^1695). He con-
structed simple microscopes and telescopes. The magni¢-
cation of these microscopes was low, and the pictures of
objects were a¡ected by the chromatic and spherical aber-
ration of their lenses because the light rays of various
wavelengths do not focus in the same plane. It is remark-
able that Marcello Malpighi (1628^1694), Nehemiah Grew
(1628^1711), Antonie van Leeuwenhoek (1632^1723), and
Robert Hooke (1635^1703) observed and described bacte-
ria, protozoa, fungi, spermatozoa, erythrocytes, and tis-
sues of plants and animals in ¢ne detail using these prim-
itive instruments. Leonhard Euler (1707^1783) postulated
and several scientists such as G.B. Amici and A. Chevalier
constructed the ¢rst achromatic lenses by combining lenses
of di¡erent refraction indices. The objectives and oculars
of the commercially produced microscopes were, until late
in the 19th century, of variable quality because they were
produced by empirical methods of trial and error. A pro-
gressive step was taken when the physicist Ernst Abbe
(1840^1905) developed a theory of the image formation
in the light microscope and constructed, in cooperation
with the mechanic Carl Zeiss (1816^1905) and the pro-
ducer of optical glass Friedrich Otto Schott (1851^1935),
oil-immersion lenses with a high numerical aperture and
the Abbe condenser for optimal illumination of the speci-
men ¢eld. The problem of spherical aberration, which
caused blurred ¢gures in the periphery of the microscope
¢eld of view, was solved by a combination of di¡erent
lenses. These new improved microscopes were made pop-
ular in the cell biology and microbiology institutes about
1877^1878 by Ferdinand Cohn and Robert Koch, who
tested these objectives and Abbe's condenser [8,9]. Since
then, microscopes ¢tted with oil-immersion lenses that
bring about a maximal resolution of 0.2 Wm have been
available. The documentation of bacteria was decisively
improved by Robert Koch (1843^1910). He developed
the method of staining smears in cooperation with C.
Weigert [10] and the method of ¢xation of bacteria on
cover slips, and introduced microphotography [11,12] us-
ing a heliostat for illumination [11^14]. The di¤cult prob-
228 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
lems in the preparation of microphotographs were vividly
described by Heymann [13].
The cells as building stones of tissues and organisms
were described by C.F. Wol¡. The great period of cell
biology began in the 1840s with the availability of an
improved microscope, the knowledge of comparative his-
tology increased, and new thoughts on the role of cells
grew [15]. Johannes E. Purkinje (1787^1869) was the ¢rst
to use the term protoplasm [16] and proposed the idea of
the similarity of animal and plant cells. Hugo von Mohl
(1805^1872) and Matthias J. Schleiden (1804^1881) were
recognized as the founders of the cell theory; they consid-
ered the cell as an independent living entity of all organ-
isms [17^19]. Initially the protoplasm was considered as a
very simple mucous material. In the 1880s, the nucleus was
shown to be an indispensable constituent of animal and
plant cells, and mitotic cell division was described by E.
Strasburger, Francis Balfour, L. Auerbach, and W. Flem-
ming.
Microorganisms were believed to be very variable (pleo-
morphic) and to generate spontaneously. In the period of
£ourishing cell biology around 1840, many scientists began
to study the developmental history of lower algae, fungi,
and protozoa, and later of bacteria. Ferdinand Cohn
(1828^1898) investigated the unicellular algae Protococcus
pluvialis Ku«tzing and Stephanosphaera pluvialis and eluci-
dated the di¡erent stages of development and the di¡er-
ence between vegetative and generative multiplication of
swarm cells (macrogonidia and isogametes) [20^24]. About
the same time, but independently, the sexuality of algae
was discovered in 1854 by Gustave Thuret in Fucus, of
Vaucheria in 1855 by Nathanael Pringsheim (1824^1894),
and of Sphaeroplea annulina and Oedogonium in 1855/1856
by Cohn [22,24]. The fecundation of the egg cell in the
oogonium by the spermatozoids or the fusion of isoga-
metes in cryptogamae, algae, and fungi was carefully
studied by Cohn, Heinrich Anton de Bary, Thuret, Prings-
heim, and others [19]. It was concluded that sexuality is a
peculiarity not only of higher but also of lower organisms.
The discovery by Cohn [25,26] of the complex develop-
mental cycle, functional di¡erentiation, and sexual repro-
duction of Volvox globator and many other microorgan-
isms was not only interesting from the point of cell
biology, but also important for modern taxonomy and
physiology. The concept that shape and function of each
higher organism is based on a special plan was developed
by the comparative anatomy studies in the 17th and 18th
centuries. The progress in chemistry and comparative cell
biology extended this concept to cells as the building
stones of all organisms which are structurally and func-
tionally di¡erentiated during the development of the or-
ganism.
3.3. The development of the evolutionary view in biology
Several scientists of the 17th and 18th centuries became
FEMSRE 678 29-5-00
aware that extant life forms were organized di¡erently
than those of earlier periods of the Earth's history. It
was also realized that most organisms live in restricted
areas, in natural habitats. The question of the origin of
species was realized and the descent of species from com-
mon ancestors was discussed, but the static view of nature
and the belief that all organisms could be traced back to
creation or di¡erent forms of spontaneous generation,
such as abiogenesis or heterogenesis, dominated
[3,27,28]. Species were believed to be invariable.
Jean Baptiste Antoine de Monet Chevalier de Lamarck
(1744^1828) was one of the ¢rst to explain the multiplicity
of forms of organization and their gradation from primi-
tive to highly developed species by a process of evolution
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
[28,29]. Impressed by the comprehensive comparative
studies of fossils and living organisms, he postulated that
the fossil species are ancestors of the living species. La-
marck proposed that the environmental conditions
changed over long periods and that low to high complex-
ity evolved by an inherent potential and by adaptation to
the changed environmental conditions. He believed that
the acquired properties were transmitted to the next gen-
eration. Although he did not explain the mechanism, his
theory of evolutionary change replaced the static view of
nature.
Georges Lëopold Cuvier (1769^1832) contributed to the
theory of evolution with comprehensive comparative stud-
ies on the anatomy of vertebrates and invertebrates and
with paleontological studies, but continued to believe the
constancy of species. He and the geologist Charles Lyell
believed that extinction of species was caused by changes
in environmental conditions during geological periods and
that new species originated discontinuously by creation,
spontaneous generation, or sudden changes.
Charles Robert Darwin (1809^1882) founded his theory
of the evolution on the basis of his own studies and the
numerous published observations of comparative anatomy
of living and fossil organisms [30]. He concluded that all
organisms have a common origin. Darwin assumed a con-
tinuous formation of a large and inexhaustible supply of
genetic, i.e. inheritable, variations. In subpopulations of
species, living in a separate habitat, natural selection
caused diversity even within a species. Individuals and
populations formed that changed their features slowly
from that of the original species. New species originate
from varieties. Natural selection was, in the view of Dar-
win and Alfred Russel Wallace (1823^1913), not an acci-
dental process, but was caused by di¡erential success in
reproduction and competition within the population of the
organisms and was determined by the interactions with the
speci¢c physical, chemical, and biological conditions of its
habitat. New varieties optimally adapted to their sur-
roundings survived and dominated in their habitat; less
adapted varieties disappeared [28,30,31]. The principles
of natural selection, evolution, and origin of species were
not accepted immediately by the scienti¢c community of
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
the 19th century, and the concept of spontaneous gener-
ation by abiogenesis was revived to explain the formation
of the ¢rst organisms on Earth [6,27].
4. The discovery of microorganisms and their ¢rst
classi¢cation
4.1. The bacteria
The supposition that various diseases are caused by mi-
croorganisms was expressed several times in the early lit-
erature [29]. In 36 BC, Marcus Terentius Varro wrote that
animals (animalia quaedam minuta) that cannot be fol-
lowed by the eye were transferred through the air to other
persons and caused serious diseases. It is clear from his
publication that he described malaria, which is caused by
the sporozoon Plasmodium and is spread by the mosquito
Anopheles [32]. Girolamo Fracastoro (1478^1553) studied
the `French disease' syphilis and wrote in 1546 that the
`contagion is an infection that passes from one thing to
another' by direct contact between two persons, by con-
taminated material, or over long distances. He also de-
scribed the pathology of a contagious disease, presumably
spotted fever caused by Rickettsiae [29,33]. Athanasius
Kircher (1602^1680) studied infectious diseases caused by
a contagium animatum. In contrast to the medical doctors
of his time, who believed that diseases are caused by pu-
trefaction of the body humor or miasma, he observed
`vermes' in the blood or lymph nodes of people su¡ering
from bubonic plague caused by Yersinia pestis. Presum-
ably he did not see the bacteria, but rather particles in
the tissues.
The ¢rst clear evidence for the existence of bacteria was
given by Leeuwenhoek. He was an optician by hobby and
constructed, as did many contemporaries, numerous mi-
croscopes. The important step forward came from his very
careful and imaginative style of observation. In more than
200 letters to the Royal Society in London, which were
published in the Transactions of the Royal Society, and in
letters to Robert Hooke, he described di¡erent forms of
bacteria, yeasts, and protozoa [1,4,34^36]. He also per-
formed some simple experiments, e.g. he studied the in£u-
ence of acetic acid on the mobility of bacteria, which he
called animalcules, beesjes, or cleijne schepsels. The de-
tailed description of bacteria from tooth plaque, water
samples, and hay infusion is remarkable considering the
low magni¢cation and resolution of his simple instru-
ments. The bacteria he saw were documented by drawings.
The size of the bacteria was determined by comparison
with grains of sand or erythrocytes. The movement of
bacteria was described in detail. The new knowledge on
the animalcules or vermes quickly circulated and initiated
many microscopy studies in order to ¢nd infusoria in or-
ganic material or tissues from sick people [36]. The devel-
opment of the idea of the contagium animatum up to the
FEMSRE 678 29-5-00
229
causal analysis of infectious diseases will be dealt with in
Section 7.3.
Carl von Linnë classi¢ed the microscopic organisms in
the genus `chaos' (1773^1776). Otto Friedrich Mu«ller
(1730^1784) criticized the scientists of this epoch for con-
templating the infusoria without any critical characteriza-
tion and classi¢cation. In his book Animalcula infusoria
£uviatilia et marina, he classi¢ed the infusoria by morpho-
logical and biological criteria, such as movement, habitat,
and formation of aggregates. From the 18 genera he pro-
posed, only several characteristic types, especially Flagel-
lata and Ciliata, can be identi¢ed. Bacteria, but also Pro-
tozoa, appear under the taxa Monas and Vibrio. He
described 10 species of Monas and 31 species of Vibrio.
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
The description of the infusoria was documented by ¢g-
ures [37]. The knowledge of the larger forms of infusoria,
the protozoa and unicellular algae, was improved in the
following decades, but the studies on bacteria concen-
trated on the question of their origin (see Section 6).
Christian Gottfried Ehrenberg used an improved micro-
scope, ¢tted with achromatic combinations of lenses, to
study the `Infusionsthierchen als vollkommene Organis-
men' (infusoria-animalcules as complete organisms) [38].
The largest part of this book was devoted to the protozoa.
The most simple organisms he observed were classi¢ed as
Monadina and Vibrionia. The tail-less, lip-less, eye-less,
most simple monadina were subdivided into sphere mo-
nads and rod monads. The genera Monas, Bacterium, Vi-
brio, Spirillum, Spirochaeta, and Spirodiscus were de-
scribed, but the species were less well characterized.
Fëlix Dujardin subdivided the bacteria, combined in the
family Vibrioniens, into the genera Bacterium, Vibrio, and
Spirillum [39]. Four species of Bacterium ^ B. termo, B.
catenula, B. punctum, and B. triloculare ^ were described.
The species Vibrio lineola, V. rugula, V. serpens, and V.
bacillus were distinguished from Spirillum undula, S. vol-
utans, and S. plicatile by their shape and movement. The
organisms described by both authors cannot easily be
identi¢ed by present taxonomic characteristics. The work
of Maximilian Perty [40] did not improve the taxonomy.
He confused the characterization by mixing up develop-
mental stages with species. He subdivided the so-called
animal-plants or Phytozoidia, into Filigera, Sporozoidia,
and Lampozoidia, and further subdivided the latter into
Vibrionida, Spirillina, and Bacterina. Allied to the Spiril-
lina, the species Spirochaeta plicatilis, Spirillum volutans,
Spirillum undula, and Spirillum rufum were mentioned.
The Bacterina were subdivided into Vibrio, Bacterium,
Metallacter and Sporonema.
4.2. The fungi
The large fruiting bodies of basidiomycetes and ascomy-
cetes, conspicuous to the unaided eye, may have been
known to man since primitive times. Humans have used
fungi, often unknowingly, for fermentation in wine, beer,
230 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
and bread making. Fungi were also used as food, drugs, or
poison.
In the 16th and 17th centuries, the shape, appearance,
and usefulness for man of numerous fungi were described,
for example, by Charles de L'Ecluse (Clusius ; 1526^1609)
[41]. Gaspard Bauhin (1560^1624) was the ¢rst to discern
genera and species in his detailed and illustrated descrip-
tion of plants. In his book, 2700 species of plants and 100
species of fungi were described. The fungi were separated
into esculentii, noxii, and perniciosi [42]. Joseph Pitton de
Tournefort (1656^1708) presented a hierarchical ordered
system with detailed descriptions of genera [43]. Fungi
were separated into six groups: (1) centrally stalked with
cap; (2) centrally stalked without cap; (3) laterally
stalked ; (4) globose without stalk, including myxomy-
cetes; (5) subterranean forms; and (6) corraloid forms.
Developmental stages, e.g. teleutospores of rust or myce-
lium of fungi, as described by Robert Hooke, were not
included.
How fungi propagated was not known, and they were
believed to originate from decaying substances. The revo-
lutionary idea that all plants produce seeds was proposed
by Porta in 1590. He described spores, which he called
seeds, isolated from numerous fungi. M. Malpighi pic-
tured in his book of the anatomy of plants [44] sporo-
phores, sterigmata, and spores, and speculated whether
spores were units of propagation. Pier Antonio Micheli
(1679^1737), although he never received an academic de-
gree, made great progress in the description of cryptoga-
mae. He introduced the names of many generic names,
such as Mucor, Aspergillus, and Polyporus, and his de-
scriptions of species are so detailed that they can be iden-
ti¢ed today. With a primitive microscope, he observed
seeds (spores) and sporophores in many groups of fungi,
and he cultured certain molds on pieces of fruit. He fol-
lowed the germination of spores and the growth and de-
velopment of fungi up to the fruiting bodies, and con-
cluded that each fungus formed its own seeds and is
reproduced only by its own kind [45]. Carl von Linnë
(1707^1778) included the described fungi as a class of their
own in his book on species plantarum [46], where he es-
tablished the binomial system of nomenclature. He did
not, however, contribute to a better understanding of fun-
gi.
In the second part of the 18th century, many detailed
descriptions of fungi were published and illustrated with
excellent drawings [47]. Phenomena of infected plants had
been known since the classical period. Phytopathology,
based on empirical research, was initiated by Mathieu Till-
et (1714^1791). He studied loose smuts and hard smut of
wheat and showed that they are infectious diseases. He
observed that seeds (spores) from smutted kernels produce
smutty wheat [48]. In 1767, Giovanni Targioni-Tozzetti, a
disciple of Micheli, described the infection of plants by
germinating rust spores. He observed the penetration of
the epidermis through the stomata by germ tubes and the
FEMSRE 678 29-5-00
development of the fungus inside the wheat plant [49]. In
the same year, Felice Fontana published the results of his
microscopy studies on the rust of grain. Bënëdict Prëvost
(1755^1819), who was not familiar with these important
observations, published in 1807 his detailed and careful
studies on the germination of bunt or smut spores and
the infection and development of the fungus in wheat
plants. He observed that copper sulfate inhibits the germi-
nation of spores, and he demonstrated by ¢eld experi-
ments that the disease can be controlled by soaking the
wheat seeds in a solution of copper sulfate [50]. Although
this method was not widely accepted at that time, it was a
precursor of the Bordeaux mixture, introduced by Pierre
Millardet in 1885, which became in combination with the
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
lime-sulfur solution the world's outstanding preventive
fungicide, used at ¢rst to ¢ght downy mildew on vine
leaves caused by Plasmopara viticola [51].
A new period of research in mycology began with Hein-
rich Anton de Bary (1831^1888). He and many of his
students and coworkers, such as O. Brefeld, E. Fischer,
A. Meyer, P. Millardet, and M. Woronin, published im-
portant papers in the ¢eld of sexual and asexual reproduc-
tion, development, and parasitism of fungi [52^55,60]. In
1893, Pierre Dangeard observed nuclear fusion in the tele-
utospores of a rust fungus, and in 1894 in Peziza. He
interpreted this process correctly as a fecundation. This
progress in developmental biology was the basis of a mod-
ern taxonomy of fungi. Ferdinand Cohn studied the devel-
opment of the zygomycete Pilobolus crystallinus and of the
entomophthoracea Empusa muscae [56,57].
Johann Scho«nlein in 1839 and David Gruby in 1841
described Trichophyton and Candida albicans as infectious
fungal parasites of man and founded the ¢eld of medical
mycology [29].
The ¢rst systematics of fungi was published by Christian
Persoon [58]. He understood that mushrooms are only
fruiting bodies and are not the whole plant. He recognized
two types of fruiting bodies: those in which the hymenium
is uncovered during maturation of the spores and those in
which the hymenium is enclosed, e.g. the pu¡ball (bovist).
He established a herbarium containing the type species.
The fungi known at that time were divided into 71 genera.
Other systematic treatments of fungi were published by
Elias Magnus Fries [59], and in 1837^1854 by August
Corda [29]. These early systematic studies were based ex-
clusively on morphological data. De Bary emphasized the
importance of the developmental history and of the sex-
uality for classi¢cation of fungi [53].
Nutritional physiology and the development of exact
methods to analyze growth and nutrition of fungi were
founded by Jules Raulin, who elucidated the mineral re-
quirements of Aspergillus niger [61]. The growth of fungi
on a mineral medium completed with an organic carbon
source was introduced by Louis Pasteur, but Raulin was
the ¢rst to determine quantitatively the growth of fungi
and the consumption of the nutrients. He recognized that
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
besides the macroelements and one organic carbon source,
trace elements were essential for the growth of Aspergillus,
but their exact analysis required improved methods for
puri¢cation, which were not available at that time.
4.3. The protozoa
The protozoa, called `infusoria', have been described in
many monographs since the 17th century. Christian Gott-
fried Ehrenberg (1795^1876) was well known for his de-
tailed and comprehensive description of more than 500
species [38]. He observed that the small animals take up
particles of carmin or indigo into vesicle-like structures,
which he called stomach. He proposed the concept that
protozoa have complex internal structures similar to those
of higher organisms. Felix Dujardin (1801^1862), who
stressed the importance of the work of Ehrenberg, rejected
this hypothesis as most of his contemporaries did. Dujar-
din improved the systematics of protozoa and observed
that sodium phosphate, ammonium oxalate, sodium bicar-
bonate, and ammonium nitrate were used by the infusoria
as nutrients [39].
5. The concepts of taxonomy
The comparative anatomy studies in the 17th and 18th
centuries brought together a comprehensive knowledge of
the shape, structure, and organization of organisms. The
great diversity in the world of living beings, the purely
practical need to bring order into the richness of life,
and the desire to investigate the perfect harmony of nature
and its diversity were motives to study systematics. In
the era of Linnaeus, systematics had enormous prestige
and dominated all other contemporary research. Linnaeus
and his contemporaries believed that genera and higher
taxa are creations of God and that therefore his sys-
tematics represented a natural system. This systematics
was based on essential properties and originated from
creationist thinking in the absence of an evolutionary
theory (essentialism). The principle of logical downward
division is based on the similarity of organisms and £owed
from the higher to the lower taxa using the method
of dichotomy. It was a purely descriptive work, but it
was a rich source of information. Linnë not only intro-
duced binary nomenclature, he also completed the species
description by adding remarks on the habitats of the
species.
The quite di¡erent systems which originated in the 17th
and 18th centuries were in£uenced by the choice of the
characteristics used for the ¢rst division [28]. Even within
a system, the type of characteristic was changed, e.g. from
fructi¢cation to vegetative growth, or from morphological
to physiological features. It was discussed whether one
should use only a single key characteristic or multiple
characteristics; whether one could use characteristics other
FEMSRE 678 29-5-00
231
than morphological characteristics for classi¢cation, e.g.
physiological and ecological features; and whether the
characters should be weighted. The re¢ned and extended
knowledge of organisms living in di¡erent parts of the
world and the revolution in philosophical thinking made
the downward classi¢cation of essentialism unsuitable for
classi¢cation. Practical considerations led to the adapta-
tion of an upward classi¢cation of empirical grouping us-
ing numerous characteristics. This method started with the
characterization of species, followed by sorting of species
into groups of similar ones, and combining these groups
into a hierarchy of higher taxa [28]. In 1772, Adanson
introduced the use of multiple characteristics for classi¢-
cation. He recognized that di¡erent characteristics have
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
di¡erent taxonomic signi¢cance.
Taxonomy was revolutionized in the 19th century by
Charles Darwin, the founder of evolutionary taxonomy.
Darwin explained why groups of species are related to
each other. In the thirteenth chapter of The Origin of
Species [30], he developed the theory of classi¢cation.
His theory of common descent provided reasons for the
degrees of similarity among organisms and an explanation
for the hierarchy and for the homogeneity of taxa in a
natural classi¢cation. Darwin also discussed methods
and di¤culties of classi¢cation. He stressed that true clas-
si¢cation is genealogical and, therefore, the taxonomical
value of all characters has to be weighted. Similarities due
to descent have to be separated from similarities due to
convergence. However, the Darwinian revolution had only
a minor impact on the methodology of classi¢cation. Up-
ward classi¢cation had already been introduced before
Darwin [28].
The classi¢cation of microorganisms, especially of high-
er taxa, was improved in the 19th century by the discovery
of sexuality and of the development of fungi, lower algae,
and protozoa. In earlier times, very often di¡erent stages
in the life cycle or zoospores were described as di¡erent
species or interpreted as polymorphy. The discovery of the
ascus and the basidium and their role as meiosporangia
was decisive for the grouping of ascomycetes and basidio-
mycetes.
5.1. The species problem in bacteriology and new concepts
for classi¢cation
Bacteria have been known since the early observations
of Leeuwenhoek, and many studies were published after
that time which describe `small animals' or `infusoria' as
contagion (Jakob Henle (1809^1885), contagium vivum
[62]) or as `ferment' of butyric acid fermentation [63,64].
Unfortunately, no scientist carefully isolated the particular
microorganisms and studied them in their environment.
The bacterial forms observed with the microscope were
described as a new species without consideration of the
forerunner. The work of Ehrenberg and Dujardin was
an exception, but they did not characterize the species
232 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

su¤ciently. The problem of the origin of bacteria and of
independent, distinct species was still not solved by 1850.
Ferdinand Cohn (1828^1898) stressed that in the ¢eld of
bacteriological systematics, one has to start at point zero
[65,66]. His taxonomic studies were based on an excellent
knowledge of the unicellular algae, lower fungi, protozoa,
and bacteria. He noticed that the cellular organization and
other structural details of bacteria could not be resolved,
even when the bacteria were observed with the strongest
oil-immersion objective of the microscope (the methods of
phase-contrast microscopy and staining of bacteria were
still not discovered) [65,66]. Only a few characteristics
were available for classi¢cation, and it was not known
whether they are stable and species-speci¢c stages of de-
ment, chemical features, and descent could only be an-
swered in the future when new chemical methods became
available [65,66,76]. From the beginning of his studies,
Cohn was convinced that the kingdom of bacteria con-
sisted of species with inherent characters. He defended
this concept against Theodor Billroth (1829^1894) and
many other contemporaries who believed that all spherical
bacterial forms and all rod-shaped bacterial forms each
belong to only one species of plants and have `only one
form of life' (`eine einzige Lebensform') which can adapt
to di¡erent conditions of the environment and change
their form accordingly (pleomorphy): Micro-, Meso-,
Megacoccus and Micro-, Meso-, and Megabacteria. Bill-
roth combined all genera proposed by Cohn in the poly-

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

velopment, or variations caused by environmental condi-
tions. Sexual reproduction of bacteria was unknown.
The isolation of single cell clones and the pure culture
technique were slowly developed from the cultivation on
solid media and enrichment cultures. The growth of col-
ored bacteria on starch-containing food was described by
Herrmann Ho¡mann ([36], p. 110). Joseph Schroeter, a
coworker of Cohn, transferred colonies of pigmented bac-
teria, grown on slices of cooked potato, to another piece
of solid food to separate the colored from the colorless
bacteria [67]. Clone cultures of fungi were obtained in the
laboratories of de Bary and Brefeld by sowing single
spores on solid media ([54], pp. 2 and 5; [60,68]). Scientists
became rapidly acquainted with the culture of bacteria on
solid media and the technique was used in the laboratories
of Cohn and Koch starting in about 1875 [36]. The sepa-
ration of single cells by streaking bacteria on solidi¢ed
gelatin was introduced by Koch in 1877 [12] and the use
of plates with gelatin was introduced by Koch [12,14,69]
and Esmarch [70,71]. Frankland [72] and Petri [73] devel-
oped a small, practical culture chamber, the Petri dish, to
keep the cultures free of contamination through the air.
The introduction of agar as a solidifying agent greatly
improved the isolation and culture of bacteria because
agar is inert for most bacteria and is still solid at 37³C,
the temperature at which most pathogenic bacteria were
cultivated [74,75].
Cohn noticed that species and genera of bacteria have
meanings di¡erent than those of higher organisms, be-
cause generative propagation was not known. The classi-
¢cation of bacteria had to start from the characterization
of `form-genera' and `form-species'. The question whether
these species are related to each other in their develop-
morphic species Coccobacteria septica, except for Spiril-
lum and Spirochaete, which he did not consider [77,78].
Joseph Lister defended the idea that bacteria are generated
from conidia of fungi and that they change their morphol-
ogy during culture on di¡erent media [76,79]. From the
description of his experiments, it seems clear that he trans-
ferred a mixture of di¡erent organisms to new media and
that speci¢c microorganisms were selected during growth.
During this time, several pathologists described microor-
ganisms in di¡erent diseased tissues, but they did not iso-
late and characterize the bacteria [36]. Although they
speculated that these organisms cause the illness, no ex-
periments were undertaken to identify the organisms and
to study their e¡ect on the human body.
During a period of about 20 years Cohn and coworkers
studied numerous distinctive characteristics of bacteria,
such as cytological details, movement, growth under var-
ious conditions in mineral media substituted with one car-
bon source or on complex media, appearance of pigments,
and the formation and germination of endospores (Fig. 1).
The structure of £agella and the swarming phenomenon
were detected, and the function of £agella was correctly
interpreted [66,67,76,80]. On the basis of these investiga-
tions and his being impressed by Darwin's theory of ori-
gin, evolution, and selection of species, Cohn developed a
new concept of bacterial classi¢cation. Bacteria were de-
¢ned as mostly pigment-free cells of characteristic shape
that multiply by cross division and live as single cells,
¢lamentous cell chains, or cell aggregates. They contain
a plasma membrane and sometimes refractile granules.
They form a distinct kingdom of microorganisms that
are discernible by heritable characteristics that allow the
classi¢cation into distinct species with typical character-

C
Fig. 1. Di¡erent bacteria, drawn by Cohn. A: (Table V in [66]). 8) Cladothrix dichotoma, described on p. 185 in [66], similar to Scytonema, false
branching; 9) Bacillus anthracis, from blood of a cow which died from anthrax; 10) mobile bacteria with endospores from rennet ; 11) bacilli with endo-
spores from butyric acid fermentation; 12) Micrococcus and spores from rennet ; 13) Micrococcus bombycis from silkworm, sick from £accid disease.
B: (Table VI in [66]). 9, 10) Lamprocystis (Clathrocystis) roseopersicina ; 11) Chromatium (Monas) warmingii ; 12) Chromatium (Monas) okenii; 13) Chro-
matium vinosum (Monas vinosa); 14) Rhabdomonas rosea containing sulfur globules, pink colored; 15) Ophidomonas (Spirillum) sanguinea, large, red col-
ored with light-scattering granules (Thiospirillum jenense?); 16) Spirochaete Obermeieri, Borrelia recurrentis with red blood cells; 17) Bacillus ruber
Frank (p. 181 in [66]), red colored, growing on cooked rice; 18) Myxococcus (Micrococcus) fulvus, red colored colonies.

FEMSRE 678 29-5-00

 Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
233
G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

FEMSRE 678 29-5-00

234 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

istics, which are transmitted to the following generation

when bacteria multiply. Cohn proposed that within the
species, varieties originate, which transmit their new fea-
tures to the next generation. He was convinced that bac-
teria belong to the plant kingdom and that they are related
to algae [66,76,80^82]. From his studies on development,
he concluded that bacteria are closely related to the Phy-
cochromaceae (Rabenhorst 1865), which were also known
as Myxophyceae (Wallroth 1833), Schizophyceae, or Cya-
nophyceae (Sachs 1874); today they are named cyanobac-
teria ([83], p. 1711). Schizophyceae and Schizomyceae
(bacteria) were combined in the group of Schizophyta (¢s-
sion plants) [76,80,84,85]. The close relationship between
bacteria and Schizophyceae was exempli¢ed by compari-

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

son of the chlorophyll- and phycocyan-containing Oscilla-
toria with the colorless Beggiatoa (Fig. 2). These two gen-
era have the same shape and cellular organization and the
same type of movement, which is a combination of gliding
forwards and backwards, a rotation around the longitudi-
nal axis, and a vivid bending of the trichomes. The Chroo-
coccaceae were compared with Micrococcus and Bacte-
rium, Merismopedia with Sarcina, and Spirulina with
Spirillum. A relationship between groups of bacteria, phy-
cochromaceen, £orideen (red algae), and lichen was de-
duced mainly on the basis of the pigments chlorophyll,
phycocyan, and phycoerythrin and the type of cell divi-
sion, movement, and reproduction [84,85]. Cohn supposed
that the Phycochromaceae were early inhabitants of the
earth because of their ability to grow in extreme habitats,
their simple way of reproduction, and their fossil record.
The fungi were considered as a group of microorganisms
not related to the bacteria and phycochromaceen [76,86].
Cohn classi¢ed the bacteria into: (I) Sphaerobacteria
Fig. 2. Beggiatoa species, from Cohn, F. (1866) Hedwigia 5, 161^166.
(sphere-shaped) with the genus Micrococcus, (II) Micro-
bacteria (rod-like) with the genus Bacterium, (III) Desmo-
bacteria (¢lamentous bacteria) with the genera Bacillus ternitz, and others still believed that bacteria originated
and Vibrio, and (IV) Spirobacteria (screw-like bacteria) from decaying plant and animal tissues ([36], p. 130) or
with the genera Spirillum and Spirochaeta [76,80,81]. Mi- spontaneously [27,76]. E. Hallier supported the germ
crococcus was divided into three groups of species based theory of infectious diseases, but he believed that the mi-
on the characteristics chromogen (pigmented), zymogen crococci he isolated from pathogenic material were trans-
(fermenting), and contagion (pathogen). Bacterium termo formed into fungi [87]. The fungus theory of Hallier was
was speci¢ed as the cause of putrefaction. Contagion and strongly refuted by de Bary because of Hallier's faulty
putrefaction were discerned as speci¢c features. In the de- experiments [88]. Hallier considered the succession of dif-
scription of the screw-like bacteria, Cohn followed the ferent organisms that he observed in his culture apparatus
names proposed by Ehrenberg : Spirochaeta plicatilis, Spi- as stages of the same organism, which he regarded as
rillum volutans, S. tenue, and S. undula. The bacteria were genetically connected [87]. Billroth, Lister, Na«geli [89],
cultivated on synthetic media with various carbon sources and other contemporaries defended the opinion that the
or on complex media. The inheritance of features, e.g. morphological and physiological di¡erences between the
pigmentation, was supported by their stability in following species are caused by nutrition and other growth condi-
generations. The pigments were di¡erentiated by solubility tions [35,36]. T.A. Edwin Klebs (1834^1913), a patholo-
or insolubility in water and their color and were analyzed gist, agreed with the hypothesis that bacteria can be clas-
by simple chromatographic, spectroscopic, and chemical si¢ed into di¡erent species, and he defended the germ
methods. The genus Sarcina [66,76] was determined by theory of infectious diseases ; in addition to micrococci
the occurrence of division in three perpendicular planes. and bacilli, he proposed microsporines and monadines
The principles of Cohn's bacterial taxonomy were not [90,91]. Ray Lankester observed enrichments of purple
generally accepted. H. Karsten, A. Wiegand, Estor, Win- bacteria in decaying organic material and named the pig-

FEMSRE 678 29-5-00

 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
ment bacteriopurpurin and the bacterium Bacterium rubes-
cens [92]. He thought that all the bacteria that contained
bacteriopurpurin but which had di¡erent shapes were
phases of one and the same organism (pleomorphism)
[93]. Cohn, Ehrenberg, Engelmann, Warming, N. Winog-
radsky, and Zopf described many species of purple bacte-
ria (the name was coined by Engelmann) mainly on the
basis of their morphology, pigmentation, physiology, and
cell inclusions (Fig. 1) [38,76,80,81].
An important achievement of Cohn was the species con-
cept, founded on the hypothesis that distinct species-spe-
ci¢c populations have several inheritable characteristics in
common, which di¡erentiate them from other species. The
concept was solidi¢ed as soon as pure cultures of bacteria
were isolated which had stable markers such as pathoge-
nicity, e.g. Bacillus anthracis [94], or nitri¢cation, e.g. Ni-
trosomonas [95^97]. The principle of upward classi¢cation
based on invariable, multiple characteristics remained the
method of choice for decades. The progress in methods to
study bacteria and the increasing knowledge of the phys-
iological and biochemical features of bacteria led not only
to the identi¢cation of new species, but also to grouping of
the species into higher taxa. The concept of bacteria as an
independent group of microorganisms with di¡erent inher-
itable characteristics and their relationship to the Schizo-
phyceae (Cyanobacteria) was con¢rmed and extended by
R. Stanier and C.B. van Niel [98], who proposed the term
prokaryotic cell organization, which di¡ered from the
organization of eukaryotic cells. This fruitful concept
was quickly accepted by the scienti¢c community and later
extended by the discovery of archaebacteria as an inde-
pendent group of prokaryotes distinct from eubacteria and
cyanobacteria [99,100].
The concept of a bacterial species, however, is still open
to discussion. Since prokaryotes do not have the same
form of sexuality as higher organisms, of which species
are de¢ned as groups of interbreeding natural populations
that are reproductively isolated, a bacterial species has
been regarded as ``a collection of strains that share
many features in common and di¡er considerably from
other strains'' [101]. This de¢nition is unsatisfactory be-
cause it remains in the opinion of the taxonomist to de¢ne
a new species. It is known that bacteria can exchange
genetic material even over large phylogenetic distances,
but the extent to which homologous recombination be-
tween host and foreign DNA takes place di¡ers strongly.
In modern bacterial taxonomy, morphological character-
istics, which dominated the classi¢cation in the past cen-
tury, are of minor importance. The weight of the genomic
characterization has increased over that of the chemical
composition of cell constituents, e.g. the components of
the cell wall and metabolic products and pathways. It is
recommended that strains which share at least approxi-
mately 70% nucleotide sequence identity and a di¡erence
of less than 5³C in the melting point of DNA/DNA du-
plexes belong to the same species [102]. This level of sim-
FEMSRE 678 29-5-00
235
ilarity leaves room for genomic and phenotypic di¡erences
due to the di¡erent life history of the strains, but simulta-
neously allows the combination of these strains in a spe-
cies, which has for practical purposes enough common
features. There are several reasons for not changing the
present classi¢cation of prokaryotes on the basis of a rig-
orous use of this species de¢nition: (i) not enough data on
strain diversity and interspecies relationships are available,
(ii) di¡erent criteria have been applied to identify species,
(iii) very closely related strains are for diagnostic purposes
still separate species, e.g. in the group of enteric bacteria,
and (iv) evolutionary systematics, as proposed by C. Dar-
win, is the only way to come to a `true natural system' of
bacteria.
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
An increasingly robust map of evolutionary diversi¢ca-
tion has been compiled, and the progress in the construc-
tion of phylogenetic trees on the basis of true DNA/DNA
homologies is impressive. The recognition of Archaea as a
distinct kingdom of organisms has in£uenced thoughts on
the evolutionary relationships among living organisms.
This phylogenetic classi¢cation will be the ¢nal objective
of systematics, although at present there is no general
agreement about the domain concepts of C.R. Woese
(Bacteria, Archaea, Eukarya), the ¢ve-kingdom classi¢ca-
tion of L. Margulis (Prokaryotes [Monera], Eukaryotes
[Plants, Animals, Fungi, Protists]), or the division of pro-
karyotes in Monodermata, having a single `cell membrane'
(Gram-positive) and Didermata, having two `cell mem-
branes' (Gram-negative) [103]. The important role of pro-
karyotes in the evolution of life seems to be evident, but
the origin of the di¡erent groups of eukaryotic and pro-
karyotic organisms and their evolutionary relationship re-
mains open to further studies. The same is true for the
species concept for bacteria. A phylogenetic classi¢cation
is the ¢nal goal, but an arti¢cial classi¢cation is still in use,
even though we know that markers such as phototrophy,
autotrophy, pathogenicity, and methanogenesis are not
characteristic for a phylogenetic group [102,103].
6. Spontaneous generation vs. evolution of microorganisms
The hypothesis of spontaneous generation of living
beings from the elements or from putrefaction, decaying
organic matter, and humidity was an old belief described
by Aristotle and other philosophers and poets of antiquity
that occupied the attention of many scientists over the
centuries and adhered to a wide spectrum of philosophical
views until modern times [1,3,4,27,29,35,104]. All propo-
nents of spontaneous generation believed that living enti-
ties can arise suddenly by chance from inorganic matter
(abiogenesis) or from organic matter, which was itself de-
rived from organisms (heterogenesis), independently of
any parents. Vitalists deny any possibility of abiogenesis
by chance, while others, following the universality of
strictly deterministic natural laws in the mechanistic phi-
236 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
losophy of R. Descartes, believed in the abiogenetic way
of spontaneous generation. The doctrine of spontaneous
generation has long been considered as an inhibitor of
scienti¢c progress. It will be shown here by a few examples
that the controversial discussion on this theory became
¢nally a driving force of scienti¢c progress because it ini-
tiated numerous experiments and resulted in new concepts
and experiments [27].
The extensive studies on the anatomy of higher and
lower plants and animals in the 17th century revealed
that animals and plants developed from eggs and semen.
Francesco Redi (1626^1697) discovered that putrefying
matter is not the material from which animals generate,
but a substrate on which animals deposit their eggs. He
observed that £ies lay their eggs on £esh and that maggots
generate from eggs, and £ies from maggots. Leeuwenhoek
was convinced that no living things came from putrefac-
tion, but that they derived from those created in the be-
ginning [4]. He studied the development of insects and
vermes from eggs. From his results the following questions
arose: (1) is air needed to support life?, (2) do all animals
come from eggs?, and (3) can seeds and eggs survive for
inde¢nitely long periods? [1,4].
Leeuwenhoek rejected the idea of spontaneous genera-
tion also for the microscopic organisms and believed that
the animalcules were distributed by air in the form of
seeds or germs, but he did not prove this hypothesis [4].
The distribution of germs by air was a controversial issue
in the 19th century. Louis Joblot (1645^1723) also denied
the doctrine of spontaneous generation, and this standing
was considered to be contrary to all reason and religion.
He experimented with heated infusions to see whether they
could produce animalcules. He boiled fresh hay and dis-
tributed the infusion into two vessels, one of which was
closed and the other was left open. After a considerable
time he observed animalcules only in the open vessel [105].
Like Leeuwenhoek, he believed that the eggs of animal-
cules were carried by air into the uncovered vessel. John
Turberville Needham (1713^1781) performed similar ex-
periments, but he used closed and open vessels in which
he heated meat extract. In both vessels a dense population
of organisms was observed after several days of incuba-
tion. Needham repeatedly observed that after heating dif-
ferent kind of infusions and careful closing to avoid con-
tamination from air, innumerable ¢laments swelled from
an internal force and became perfect zoophytes or micro-
scopic animalcules [106]. He and also Bu¡on concluded
that in each living material is a vegetative force ^ a uni-
versal semen that can initiate new life in any organic sub-
stance. Bu¡on developed the idea that vitality is an inde-
structible property of living things [107].
Abbë Lazzaro Spallanzani (1729^1799) observed in in-
fusions a sequence of di¡erent animalcules. In numerous
experiments, he showed that heating prevents the appear-
ance of animalcules in infusions if the £asks are sealed
hermetically and the air in the bottle did not contain ani-
FEMSRE 678 29-5-00
malcules. He found that the heating period required to
render an infusion sterile is variable, and he concluded
that Needham's infusions were contaminated by air
[108]. Needham commented that in Spallanzani's experi-
ments, the prolonged heating destroyed the vegetative
force and modi¢ed the air. In response to Needham's ob-
jections, Spallanzani repeated his experiments and con-
cluded that animalcules developed in £asks that were
corked, but not in hermetically sealed £asks that were
heated for 0.5^2 h. He also did experiments with £asks
having capillary necks to avoid diminishing the `elasticity
of the air', as accused by Needham. Two types of animal-
cules were described : those of superior order, which were
easily destroyed in 30 s at 100³C, and the other exceed-
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
ingly minute organisms that sometimes survived boiling
for 30 min. He also showed that boiling water is much
more e¡ective in sterilization than hot air and that boiling
media for long periods did not prevent growth of animal-
cula [108,109].
The opposition to Spallanzani and like-minded people
rested on the adherence to the traditional 18th century
mechanistic concept of spontaneous generation. Oppo-
nents of spontaneous generation were faced with the prob-
lem of the generalization of an experimental result: the
statements that all organisms arise from parents or that
no organism arises spontaneously from matter can be dis-
proved for one organism, but neither can be proven with
absolute certainty. Moreover, Spallanzani had several lim-
itations; most importantly, his microscope was insu¤cient
to see bacterium-sized objects. He attacked the doctrine of
spontaneous generation from an a priori belief in the hy-
pothesis that all living things arise from parents. Thus, the
experiments of Spallanzani and the critical thoughts of
Leeuwenhoek did not convince the adherents to the doc-
trine of spontaneous generation of animalcules, and the
doctrine remained a widely held belief and was supported
by many biologists, such as O.F. Mu«ller, Treviranus, La-
marck, Ku«tzing, and Dujardin far into the 19th century
[27,35,36]. Although cell biologists and histologists pro-
vided more and more examples of organisms that arise
from parents and argued by analogy that all living things
were produced in the same way, the doctrine survived in a
transformed view. Lamarck believed that spontaneous
generation is necessary in order to understand the discon-
tinuities in fossil records and the evolution from the lower
forms on the escalator of life to the more complex higher
organisms [104].
The spreading of microorganisms through the air was
very often thought to be a source of contamination. F.
Schulze [110] gassed heat-sterilized infusions with air
sucked through concentrated sulfuric acid. No growth of
organisms was observed until the vessel with the infusion
was exposed to open air. Felix-Archime©de Pouchet and
Hughes Bennet, however, observed growth in the appara-
tus described by Schulze. J. Tyndall (1820^1893) noticed
that the air has to pass slowly through the sulfuric acid;
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
otherwise, the gas bubbles could transfer microorganisms.
Theodor Schwann (1810^1882) designed an apparatus
consisting of a £ask that contained an infusion sterilized
by boiling. Air was conducted through a heated glass tube
before reaching the infusion. Such £asks kept for 6 weeks
did not show any growth of microorganisms, but after
opening the £ask, the infusion became putrid. Schwann
concluded that the germs or seeds of infusoria in the air
were destroyed by heat. In the same apparatus, the £asks
were ¢lled with boiled sugar solution and yeast. In £asks
with unheated air, the sugar was degraded, alcohol was
formed, and the yeast cells grew ([35], pp. 86^87). A new
principle of air sterilization was introduced by H.
Schro«der and T. von Dusch [111]. They ¢ltered air
through cotton-wool before passing it through the infu-
sion. The ¢lter trapped the germs, and no growth was
observed in the heated infusion. Although these and other
scientists showed experimentally that no animalcules de-
veloped in boiled infusions and therefore no spontaneous
generation occurs if the air is free of germs, the number of
opponents did not decrease.
One of the opponents was F.A. Pouchet (1800^1872),
who began his experiments with the aim of proving spon-
taneous generation. He believed that life was generated by
a vital force coming from pre-existing living matter (het-
erogenesis [27,112]). According to his theory, the main
factors of heterogenesis are organic matter, water, access
of air, and a suitable temperature. He repeated the experi-
ments of Schwann and Schulze, but obtained contrasting
results. At this time, Louis Pasteur (1822^1895) extracted
germs from the cotton-wool after ¢ltration of air and ob-
served them under the microscope, thereby demonstrating
that germs are distributed through air [63]. The presence
and distribution of microorganisms in the air was also
studied in Cohn's laboratory. In a simple set-up, air was
sucked through a previously sterilized medium. The aer-
ated medium was incubated at di¡erent temperatures, and
the growing fungi and bacteria were studied microscopi-
cally [113]. Mi£et showed that the number and type of
microorganisms growing in the aerated media were depen-
dent on the source of air (laboratory, garden, or open
¢eld). Similar experiments were performed by Pasteur
and coworkers, who showed that air in the mountain re-
gion of the Alps at 2000 m altitude contained far fewer
germs than air in locales in Paris [63,104,114]. Pasteur also
concluded that alkaline infusions required a higher tem-
perature or prolonged periods of boiling to destroy the
germs than acidic infusions [104,114,115]. In order to
avoid contamination, but to allow access of air to the
infusion, he used £asks with a neck that had been heated
and pulled out into a capillary and bent several times: the
boiled infusion in these £asks remained sterile. The spon-
taneous-generation proponent Pouchet did not give up. He
conducted an extensive series of experiments similar to
Pasteur's, but again came up with contrasting results. Fi-
nally, a commission of the Academy of Sciences, which
FEMSRE 678 29-5-00
237
was prejudiced, decided the discussion in favor of Pasteur.
It was not seriously considered that Pasteur worked with
yeast extract or other de¢ned media, while Pouchet used
hay infusions. Pasteur refuted the doctrine of spontaneous
generation not only because of the results of his steriliza-
tion experiments, but also because of preconceived ideas
that speci¢c fermentations, such as butyric, alcoholic or
lactic acid fermentation, are caused by speci¢c microor-
ganisms even when no oxygen is present and because of
his anti-materialistic belief in a Creator God [63,64,104,
114^117].
The heterogenists and others continued to carry out
di¡erent types of experiments to prove or disprove spon-
taneous generation [1,27,29,35,104]. Charlton Bastian
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
(1837^1915) was not convinced that germs were trans-
ferred through the atmosphere, and he opposed the theory
that diseases are caused by parasites. His experiments
showed that some germs may be much more thermoresis-
tant than had been previously supposed. The practice of
heating liquids to 115^120³C for sterilization was intro-
duced by Pasteur and Chamberland. Chamberland devel-
oped the autoclave and in 1884, a ¢lter made of porous
porcelain to remove all microbes from water [27,35].
John Tyndall (1820^1893), a great experimenter and in-
genious thinker, was an opponent of spontaneous gener-
ation. He developed a method to make particles in air
visible using light scattering and compared the infectious-
ness of the particle density in air with the growth density
in the culture vessels in his apparatus. He observed that
the `power of air' to develop life in sterile media paralleled
its capacity to scatter light. Air from which all particles
were sedimented was shown to be sterile [118]. He con-
cluded that air is a carrier of germs. Tyndall observed, as
W. Roberts [119], F. Cohn [76,82], and Eidam [120] did,
that neutralized hay infusion withstands long-term boiling.
He concluded that bacteria have phases of development ^
one phase is relatively thermolabile and is destroyed by
heating at 100³C in 5 min, whereas the other phase, which
was regarded as the germ of the bacterium, is thermore-
sistant to boiling temperatures [121]. F. Cohn discovered
in the same year that the heat-resistant phase in the devel-
opment of the hay bacillus is the endospore (Fig. 1). He
described the whole life cycle of Bacillus subtilis and the
formation and germination of endospores by detailed mi-
croscopy studies [82]. On the basis of his results, Tyndall
elaborated the important method of fractional steriliza-
tion, known today as tyndallization [121]. By this method,
vegetative and heat-sensitive stages of bacteria are killed
by boiling of the suspension. After a certain period, which
is necessary for the heat-resistant germ to pass into a heat-
sensitive state, the infusion was boiled a second time. Tyn-
dall determined the time for the interval and the number
of repetitions necessary for complete sterilization. The re-
sults of Cohn and Tyndall explained many of the contro-
versial results of the advocates and opponents of the doc-
trine of spontaneous generation, especially the observation
238 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
that hay infusion, which very often contains heat-resistant
spores, resists boiling.
If infusoria are not generated spontaneously from or-
ganic matter, how are they originated and propagated ?
After publication of Darwin's The Origin of Species in
1859 and the increasing evidence of earlier periods of life
on earth, the concept that organisms share a common
origin and subsequently diverged through time was slowly
adopted by scientists. However, Darwinism revived the
discussion on spontaneous generation, although it was re-
stricted to the question of the beginning of life and the
origin of microorganisms. In France, Darwinian evolution
was regarded as a doctrine allied with the forces that
threatened church and state [104]. Ray Lankester in Eng-
land believed that abiogenesis was a necessary and integral
part of the universal evolution theory [27]. The discussion
on how the archetype of organisms originated on Earth is
still open.
Ernst Haeckel, one of the early propagandists of Dar-
win's theory, constructed various phylogenetic trees of or-
ganisms [31]. Phylogeny, a term coined by Haeckel, is the
attempt to reconstruct the evolutionary history of life.
Haeckel divided the organisms into three main groups:
animals, plants, and protists. Since the knowledge about
bacteria at this time was very meager, Haeckel included
them in the collective term infusoria. Cohn, who likewise
was convinced of the theory of evolution, speculated that
the ¢rst living germs arrived from other planets and that
all organisms evolved from these primitive organisms ^
new heritable varieties originated and were separated in
speci¢c habitats by natural selection. He proposed that
the phycochromaceen were early inhabitants of the Earth
because of their ability to adapt to extreme habitats, their
simple way of reproduction, and the fossil records [76,79^
81,84,85].
Over much of the next century, biologists' interest in
phylogeny was minimal, but it was rekindled with the
accumulation of new phylogenetic data from the ¢eld of
molecular biology. The development of DNA and RNA
sequence technology and of mathematical methods to
compare conserved sequences in rRNA and proteins rev-
olutionized evolutionary and phylogenetic biology, espe-
cially of bacteria, which developed from an area receiving
little attention to one playing a central role in the phylo-
genetic tree ¢rst proposed by Carl Woese and coworkers
[99,100]. The concept of the prokaryotes and the eukary-
otes as two groups of organisms, each of which comprises
a large evolutionary diversi¢cation [99], was largely con-
¢rmed and later extended to a tripartite classi¢cation of
Bacteria, Archaea, and Eukarya [99,100]. The concept of
Cohn [76,84,86] that cyanophyceae (now cyanobacteria)
are related to bacteria was supported by the concept of
the prokaryotic cell [98]. Cyanobacteria were recognized as
one of the nearly 20 main lines of descent in the domain of
Bacteria [101]. The phylum cyanobacteria and the chloro-
plasts, which were proposed to derive from endosymbiotic
FEMSRE 678 29-5-00
cyanobacteria, have a complex phylogenetic structure
[122]. The three groups of organisms ^ eubacteria, arch-
aebacteria, and eukaryotes ^ are now generally accepted as
major phylogenetic branches of the tree of life. Woese and
Fox [99] proposed the progenote as a primitive hypothet-
ical ancestor of prokaryotes and eukaryotes. However, the
unraveling of the true evolutionary relationships of the
three kingdoms remains a matter of speculation and fur-
ther studies [123^126].
Archaebacteria have, besides their own typical features,
markers which are characteristic of eukaryotes or eubac-
teria [103,126,127]. It has been discussed whether they are
polyphyletic and relatives of Gram-positive bacteria [103].
Some physiological attributes, e.g. molecules of the photo-
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
synthetic apparatus, are distributed throughout taxa that
are phylogenetically not closely related. However, the pho-
tosynthetic apparatus seems to have evolved only once
[128^130]; the genetic information for their components
possibly spread by lateral transfer to di¡erent phylogenetic
groups. Anoxygenic photosynthesis ¢rst developed about
3.5 Gyr ago; oxygenic photosynthesis dominated about
2 Gyr ago [128,129]. For recent literature on the evolution
of microorganisms, see [103,126,131^135].
7. The concepts of biological diversity of bacteria
The end products of metabolic processes, such as alco-
hol or lactic acid, have been known since ancient times,
but they were not traced back to the activities of microbes.
In the 19th century, the understanding increased that not
unde¢ned vital forces, but organisms can metabolize or-
ganic and inorganic substrates. This insight was based
mainly on the progress in chemical analysis and the ob-
servation under the microscope of microorganisms in fer-
menting, putrefying, and infectious organic material, and
was also supported by an increase in rational experimental
analysis in biology.
7.1. The organismic and chemical theories of fermentation
For a long time, chemists dominated who proposed that
fermentation is caused by a spontaneous internal transfor-
mation of organic material ([29], p. 23) or by a `ferment'
(`Ga«hrungssto¡') [136,137]. Lavoisier quantitatively
studied alcoholic fermentation. He concluded that the sug-
ar was split into an oxidized portion (carbon dioxide) and
a reduced portion (alcohol) [138]. Gay-Lussac observed
that oxygen is necessary to start fermentation, but not
for its continuation [139]. The hypothesis that fermenta-
tion, putrefaction, and contagiousness are the result of
some spontaneous chemical change in the organic matter
or tissues (microzymas) and that microorganisms are just a
product but not the causative agent of disease and fermen-
tation [35] was proposed by Liebig [136,137] and Bëchamp
[140].
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
Yeast was considered by Berzelius as a catalyst, like
platinum, which was not transformed during fermentation.
Liebig postulated that the `ferment' is produced from
`Kleber' (gluten) by oxidation with the oxygen from water
[136,137]. G.V.M. Fabbroni [141] suggested that the de-
composition of sugar during fermentation is caused, in
absence of oxygen, by a vegetative-albumenoid substance.
Caniard de la Tour (1777^1859), Theodor A.H.
Schwann (1810^1882) and Traugott Ku«tzing (1807^1893)
were the ¢rst to propose independently of each other that
alcoholic fermentation is a biological process and that
yeast is a reproducing, living thing (sugar fungus, Saccha-
romyces) [142^144]. Schwann and Ku«tzing described yeast
in detail. Liebig and Wo«hler anonymously published a
persi£age of the theory of fermentation caused by living
cells [Annalen der Pharmazie 24 (1839) 100]. In a serious
article, Liebig [137] described fermentation, putrefaction,
and decomposition as processes attributed to the instabil-
ity of certain substances, which are able to communicate
their instability to other substances in succession. He
called these unstable, nitrogen-containing substances `fer-
ment', which he believed arose as a modi¢cation of a
vegetable saccharine solution exposed to air; the fermen-
tation continued in the absence of air. The chemist Mitch-
erlich concluded from his own observation that yeast is
essential for fermentation, but acts by contact, following
the catalytic theory of Berzelius [145].
Louis Pasteur (1822^1885) took a great step forward in
research on fermentation by studying not only the sub-
strate and the products of growth and fermentation, but
also the organisms in the fermentation broth. He investi-
gated the formation of lactic, butyric, acetic, and tartaric
acids and of alcohol [64,114^117] and observed anaerobic
life by butyric acid fermentation [64]. In the book Etudes
sur la Bie©re [116], Pasteur summarized and extended his
work on fermentation and life without oxygen. The mod-
ern view that yeast might ferment sugar through the pro-
duction of a soluble ferment or enzyme was proposed as
early as 1858 by Moritz Traube [146]. Finally in 1897,
Eduard Buchner (1860^1907) isolated `zymase' from yeast
juice which catalyzed the formation of alcohol from sugar
[147]. He opened the door to the fruitful studies of the
biochemistry of enzymes, cofactors, and enzymatic pro-
cesses in the 20th century.
This short overview on the history of fermentation
shows that the concepts of catalysis and species-speci¢c
metabolic capacities of microorganisms, experimentally
proved by new analytical and microbiological methods,
paved the way for modern research of this ¢eld. The multi-
tude of theories, their controversial discussion, and new
experimental approaches accelerated the progress.
7.2. Autotrophy, chemolithotrophy, and phototrophy
Autotrophy, i.e. growth of organisms with carbon diox-
ide as the only carbon source, was discovered in green
FEMSRE 678 29-5-00
239
plants by Jan Ingenhousz (1730^1799) and Nicolas Thëo-
dore de Saussure (1767^1845) [148^150]. The term auto-
trophy was introduced by Wilhelm Pfe¡er [7]. Ingenhousz
showed that plants in the presence of light absorb carbon
dioxide and liberate oxygen and that the CO2 is used for
nutrition [148,149]. Saussure determined quantitatively the
increase of the plant dry weight and the decrease of CO2
during the day in correlation with the light intensity, and
he observed that during the night, oxygen is consumed
and CO2 is released [150]. Liebig, Boussinggault, and
Sachs studied the nutritional physiology of plants grown
in a pure mineral solution [19,151]. The term photosyn-
thesis for the light-induced assimilation of CO2 was coined
late in the 19th century. Research on oxygenic (oxygen-
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
producing) photosynthesis increased very slowly, yielding
some important results in the middle of the last century
(e.g. chloroplasts as the site of photosynthesis, and starch
as the product [151]), and culminated in the 1960s with the
discovery of the CO2 -¢xation cycle, the water-splitting sys-
tem in photosystem II, and the generation of the proton-
motive force by light-driven electron transport [152]. After
the discovery of photosynthetic CO2 ¢xation, it was be-
lieved that oxygen is generated by the splitting of CO2 ; the
origin of oxygen from water was not discovered before
1941 [153].
Autotrophy and photosynthesis were discovered much
later in bacteria than in plants and algae. For many dec-
ades, CO2 ¢xation was assumed to be restricted to plants
[76]. Pigmented, bacteriochlorophyll (bacteriopurpurin)-
containing bacteria have been described since the 1830s
by Cohn, Ehrenberg, Esmarch, Perty, Warming, Winog-
radsky, Zopf and others [38,76,81,92,154^157]. Wilhelm
Engelmann (1843^1909) investigated the in£uence of
the quantity and quality of light on the movement (photo-
kinesis) and phototaxis of these bacteria [155^157]. He
was the ¢rst to conclude from growth experiments with
these bacteria under anoxic conditions in the light that
the `purple schizomycetes' assimilate CO2 like the green
plants and that they are able to transform the absorbed
light energy into chemical energy [157]. Twenty years
passed before the anoxygenic type of bacterial photosyn-
thesis was con¢rmed by Molisch [154]. Engelmann was not
sure because he had contradictory results and was possibly
convinced that oxygen liberation is connected with CO2
assimilation.
In 1877, T. Schloesing and A. Mu«ntz observed the bac-
terial oxidation of ammonia to nitrite and nitrate. R. War-
ington found that this is a two-step process. Nikolaevitch
Winogradsky (1856^1953) isolated the nitrifying bacteria
and discovered that the oxidation of ammonia to nitrite by
Nitrosomonas and the oxidation of nitrite to nitrate by
Nitrobacter yielded free chemical energy, a process which
has been named chemolithotrophy [95^97]. He also ob-
served that these bacteria can grow with CO2 as the
only carbon source. Thus, these bacteria are chemoli-
thoautotrophs.
240 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
Cohn described the presence of hydrogen sul¢de in stag-
nant water bodies and the formation and degradation of
sulfur droplets in Beggiatoa (Fig. 2). Erroneously he con-
cluded that Beggiatoa is responsible for the synthesis of
H2 S [66]. The oxidation of hydrogen sul¢de to sulfur and
sulfuric acid under microaerophilic conditions in Beggia-
toa was demonstrated by Winogradsky [158]. The reduc-
tion of sulfate to sul¢de by Bacterium desulfuricans was
¢rst described by M. Beijerinck [159].
In 1885, H. Hellriegel (1831^1895) and H. Wilfarth dis-
covered the ¢xation of dinitrogen in root nodules of legu-
minous plants, and they showed that the combined nitro-
gen compounds formed in the nodules were supplied to
the plants. The causative bacteria were isolated and de-
scribed by Beijerinck [160]. The reduction of N2 to ammo-
nia by the free-living, aerobic bacterium Azotobacter
chroococcum was shown by Beijerinck and van Delden
[161,162], and dinitrogen ¢xation by the anaerobic bacte-
rium Clostridium pasteurianum was discovered by Winog-
radsky [163]. Dinitrogen ¢xation by phototrophic bacteria
was detected in cyanobacteria by G.E. Fogg in 1942 and
in purple bacteria by H. Gest in 1950. These important
results and the progress in the analysis of fermentation
and oxidation/reduction processes led to modern concepts
of metabolism in the 20th century, e.g. the unifying theory
of microbial metabolism proposed by Albert J. Kluyver
[164,165].
7.3. Putrefaction and pathogenicity of bacteria, and
immunology
Putrefaction was always observed as a process of decay
of organic material, a source of unpleasant odor, and a
possible cause of disease in man and animals. The exact
nature of the putrid process was, however, for a long time
a matter of speculation because no experimental approach
was available [1,14,35,36,166]. In the second part of the
19th century, growth experiments using selected and de-
¢ned media with cultures of microorganisms enriched in
one species revealed that microorganisms have speci¢c,
inheritable features for the production of pigments or fer-
mentation products or for the oxidation of inorganic com-
pounds. Putrefaction was traced back to the activity of
bacteria able to decompose nitrogen-containing organic
material. The standpoint of Liebig, that putrefaction is a
rearrangement of molecules, was refuted [76,116]. Four
possibilities for the mechanism of putrefaction were dis-
cussed by Cohn [76]: (i) bacteria assimilate proteins and
transform them into their own cell material ; (ii) bacteria
produce and excrete a ferment-like compound which sol-
ubilizes and decomposes protein (like barley grains, which
produce diastase, which splits starch into sugar); and (iii
and iv) bacteria oxidize or reduce protein enzymatically
with oxidizing or reducing ferments. It was concluded
that pigmented bacteria or other bacteria split protein
molecules after uptake directly or by excreted ferments
FEMSRE 678 29-5-00
into ammonia and other compounds and assimilate am-
monia as nitrogen source [76].
7.3.1. Bacteria as contagion
The process of putridity was more and more associated
with the idea of sepsis as a cause of septicemia, pyemia,
and putrid infection. B. Gaspard administered putrid ma-
terial to experimental animals and observed the develop-
ment of symptoms. The nature of pyemia and septicemia,
however, remained a mystery [35]. The pathological e¡ects
of putrid infections on the cellular level were described by
Virchow [167]. He and other scientists studied the e¡ect of
dose on the symptoms of septic shock, intoxication, ab-
scesses, and cytopathic modi¢cations of tissues [36,166^
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
168]. Koch [14,69] investigated the histology of infected
tissues, and he examined with a microscope ¢tted with
an oil-immersion lens system and an Abbe condenser the
germs in slide preparations stained with aniline colors. He
stressed that each type of infection resulted in a character-
istic histological picture caused by the microorganisms
speci¢c for the illness; the bacterial causative agent had
to be isolated from the tissue [14]. Several scientists, such
as E.v. Bergmann (1868), Hiller (1879), and Blumberg
(1885), were opponents of the germ theory of putrefaction
and proposed that putrefaction is caused by toxic com-
pounds [35,36]. The observation of vibriones (Treponema
pallidum) in syphilitic pus and Trichomonas vaginalis in the
vagina by Donnë, the detection of the anthrax bacillus by
C.J. Davaine [169], the description of a mold, called Bo-
trytis bassiana (Beauveria) as a causative agent of a silk-
worm disease by A.M. Bassi [170], and other observations
motivated Jacob Henle (1840) to reactivate the germ
theory of disease and to study infectious diseases [62].
This was at about the same time that Pasteur's studies
revealed speci¢c microorganisms as the causative agents
of di¡erent fermentations.
The numerous cholera epidemics, the observations of
Davaine on anthrax, of Traube (1864) and E.K. Klebs
(1869) on urethritis and nephritis, of Rind£eisch (1869)
on a¡ections in the heart muscle, the demonstration of
Borrelia recurrentis only during an attack of fever in the
blood of patients su¡ering from relapsing fever by
O. Obermeier [171], and other observations on infected
tissues [172] stimulated E. Hallier (1831^1904) to isolate
and cultivate germs from infected tissues in his culture
glass [173,174]. Unfortunately he interpreted the germs,
isolated from humans and animals infected by cholera,
typhus, gonorrhea, diphtheria, and pox virus, as forms
of fungi (polymorphism). This incorrect interpretation
was rejected by the mycologists de Bary and Brefeld and
bacteriologists such as Cohn, Rind£eisch, and Burdon-
Sanderson [35,36]. In spite of the inconsistent results of
the numerous observations, the view that bacteria and
other microorganisms may be the causative agents of the
diseases received increasing consent ([36], pp. 86^103).
The crucial experiments showing that one distinctive
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
species causes a speci¢c infectious disease were performed
by Robert Koch (1843^1910). The decision to select an-
thrax for the ¢rst series of experiments was fortunate be-
cause the infected tissues contain numerous bacilli (Bacil-
lus anthracis). Koch isolated the bacteria from an animal
that died of anthrax and set up cultures in a moist cham-
ber, where the growth, division, and sporulation of the
bacilli were observed with the microscope and documented
by microphotography, which was developed by Koch [12].
In the decisive experiment, it was shown that B. anthracis,
isolated from the diseased animal, and not Bacillus subtilis,
caused anthrax in mice. Koch wrote to Cohn, who was at
this time an internationally recognized authority in bac-
teriology, that he would like to demonstrate his results in
Cohn's laboratory. The demonstration of his decisive re-
sults in Cohn's laboratory in Breslau in the presence of
Julius Cohnheim and Carl Weigert, both pathologists in
Breslau, was an important step in the progress of infec-
tious biology and the ¢rst proof that distinct bacterial
species can cause a disease with typical symptoms. The
results were published [94] after Cohn's article on the spor-
ulation of B. subtilis [82] in the journal Beitra«ge zur Biol-
ogie der P£anzen, founded by Cohn. The experimental
proof of infectious disease, later described as Koch's pos-
tulates, was the beginning of modern medical microbiol-
ogy [13,35,36]. The postulates comprise the isolation of the
microorganism from the infected tissues, the growth of the
microorganism in pure culture using the plate and slide
technique [69,175], the improved methods of observation
using microscopy, staining and documentation of the bac-
teria [10,12,175], the achievement of the typical symptoms
of the disease by inoculation of the isolated bacteria into a
sensitive host [176^178], and the isolation of the same
microorganism from the newly infected host. The ¢rst
success was followed by the discovery of Mycobacterium
tuberculosis as the causative agent of tuberculosis
[177,178]; of Corynebacterium diphtheriae, which causes
the toxigenic disease diphtheria [179]; and of Vibrio cho-
lerae, which causes cholera [180]. A. Ogston, using Koch's
technique to isolate and determine the number of micro-
cocci in pus, cultivated cocci in glass cells with Cohn's or
Pasteur's £uid under oxic or anoxic conditions and con-
cluded that Streptococcus (Rosenbach) and Staphylococcus
cause in£ammation and suppuration [181,182]. Rosenbach
[172] subdivided the genus Staphylococcus into species. In
summary, the development of several new techniques and
the concept that speci¢c infectious diseases are caused by
distinct species of bacteria having inheritable virulence
factors were the prerequisite for placing research on the
etiology of infectious diseases on a valid scienti¢c ground.
7.3.2. Control of infectious diseases
While Koch and his coworkers and disciples were con-
centrating on the isolation and characterization of para-
sitic and saprophytic bacteria, the French school under the
guidance of Pasteur was directed toward the prevention of
FEMSRE 678 29-5-00
241
infectious diseases. By repeated passages of pathogenic
germs on arti¢cial media at high temperatures (42³C), in
non-host animals, or in speci¢c tissues, they obtained bac-
teria with attenuated virulence. These attenuated cultures
were used to inoculate animals or humans. The vaccinated
individuals were shown to be resistant to the virulent
strains of fowl cholera, anthrax, swine erysipelas, or rabies
[183^186].
7.3.3. Disinfection
The observation that carbolic acid inhibits growth of
microorganisms and the formation of pus in wounds
[187] and the numerous observations that microorganisms
cause fermentation, putrefaction, and infections stimulated
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
Joseph Lister (1827^1912) to develop the antiseptic system
[188,189]. He worked out procedures for treating wounds
with phenolic compounds that were generally accepted
and introduced into the medical practice after a long peri-
od of uncertainty. Koch and others tested many other
disinfectants [190,191].
7.3.4. Immunology
From studies on the interactions of warm-blooded
bodies with inoculated parasites and the successful ¢ght
against infectious diseases, research in the large ¢eld of
immunology was initiated and the theories of humoral
and cellular immunity were developed [29,35]. E. Metch-
niko¡ (1845^1916) studied phagocytosis [192], and E. von
Behring (1854^1917) and S. Kitasato (1852^1931) detected
the antitoxins against infections of Clostridium tetani and
Corynebacterium diphtheriae [193]. Paul Ehrlich (1854^
1915) published important articles on toxins and antitox-
ins and their standardization and on the speci¢city of anti-
bodies against antigens [194,195]. The extreme complexity
of the immune system was revealed at the end of the 19th
century.
8. The achievements of Ferdinand Cohn
Ferdinand Cohn was born on January 24, 1828 in Bres-
lau, now Wroclaw, into a Jewish family. His life-long
interest in history and the classical languages Latin and
Greek was born during his education at the Maria Mag-
dalena Gymnasium (Fig. 3). After the ¢nal examination at
this Gymnasium he began his studies of natural sciences
with the main subject botany in Breslau in 1844 (Fig. 4).
Cohn continued his studies from 1846 to 1849 in Berlin
because his application for admission to the doctoral ex-
amination at the university in Breslau was refused because
of his Jewish faith. He received his doctoral degree in
Berlin on November 13, 1847 at the age of 19. In 1849,
Cohn returned to Breslau full of ideas for studying devel-
opmental cell biology, especially of lower plants and mi-
croorganisms by means of microscopy methods. He com-
pleted his Habilitation (second dissertation) in October
242 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

Fig. 3. Maria-Magdalenen Gymnasium in Breslau at 1867, the high school of Ferdinand Cohn, destroyed during World War II, now replaced by a
hotel opposite the Maria-Magdalenen church. From: Unbekanntes Portra«t einer Stadt, catalogue of an exhibition, by Iwona Binkowska and Marzena
Smolak, translated by Jerzy Pasieka, Muzeum historyczne we Wroclawiu, Ratusz wroclawski 1997.

1850, became a lecturer (auMerplanma«Miger Professor) on
April 2, 1857, and an associate professor on July 30, 1859.
He married Pauline Reichenbach in 1866, and was ap-
pointed full professor on April 17, 1872 (Fig. 5). In
1866, he founded the Institute of Plant Physiology and
established a research group (Fig. 6). A new building for
plant physiology, a herbarium, and a museum of botany
were constructed in the botanical garden of the university
and were opened in 1888 (Figs. 7 and 8). Cohn died on
June 25, 1898 (Fig. 9). The details of his career have been
described recently [79,196].
Cohn contributed to a broad ¢eld of topics in biology.
His reserve in self-representation and his modesty may be
the reason why his name is at the present time much less
known than that of Koch and Pasteur. Cohn's major ¢eld
during his studies in Breslau and Berlin was botany. In
Berlin he received a decisive intellectual stimulus for his
subsequent research. His studies on plant cells and on the

Fig. 4. The main building of the university of Breslau (north side), alma mater Viadrina, founded by Leopold III, picture taken about 1867, published
in, see Fig. 3.

FEMSRE 678 29-5-00

 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249 243

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

Fig. 5. Letter of appointment of Ferdinand Cohn as full professor. Text translated: Your Honorable is informed by order of the Mr. Minister of Intel-
lectual A¡airs, most devoted, that in instance of the philosophical faculty your Majesty, the emperor and king has signi¢ed his pleasure, to appoint you
as full professor in the philosophical faculty of this university. With my best congratulations, I send herewith the at April 17 by his majesty accom-
plished appointment, and request you, for the purpose of an imprint, to give the carrier 15 Sgr. You will receive a further order for the suitable in-
crease of your salary. To the royal professor of the university, Mr. Dr. Ferdinand Cohn, right honourable. Transcript of the order is herewith commu-
nicated to the philosophical faculty by order of the Mr. Minister of Intellectual A¡airs with regard to the proposal of the 13th March. The royal
curator of the university Con¢dential councillor and president.

FEMSRE 678 29-5-00

244 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

mental stages of approximately 90 plants should be ob-

served and documented by volunteers throughout the year
at di¡erent places in Silesia. Cohn reported and coordi-
nated the registered changes in the vegetation for many
years [202]. Cohn published important contributions on
the movement of plants induced by external stimuli (light,
chemical, and mechanical) [203^208].
Cohn's comprehensive knowledge in many ¢elds of bi-
ology was combined with a deep interest in history and
art. Cohn felt obliged to mediate knowledge of natural
sciences to a wide audience. He was convinced that edu-
cation in natural sciences was as important as training in
cultural sciences and that scienti¢c thoughts are important
not only for scientists, but also for the general public to

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

open their minds. He stressed and practised this idea dur-
ing his entire life. All those who listened to him were im-
pressed by his gifted, clear, rhetorical, and brilliant speech.
His popular description of a broad spectrum of botanical
knowledge was combined in the collected lectures on
plants, which was published in 1882, and in a second,
revised edition in 1897 [209]. The article on `Plants in
the ¢ne arts' [210] presents a retrospect on the description
of plants in art and science during several epochs. In 1856
he gave a lecture in Berlin on the history of gardens.

Fig. 6. The only room with windows of the Institute of Plant Physiol-
ogy, founded in 1866 by Cohn in an old building of the university. On
the right side in the foreground the sea water aquarium, a kind of en-
richment culture, from which many bacteria and protozoa have been
isolated and described; in the background F. Cohn with his coworkers.
From [214].

development and sexuality of algae and fungi established

his early distinction in the scienti¢c community [18,20^
25,56,57,65]. The leading role of Cohn in the evolution
of the principles of modern bacterial taxonomy was de-
scribed in Sections 4.1 and 5 [66,76,79,81,84^86] and his
comprehensive studies of bacterial physiology were de-
tailed in Section 7 [65,66,76,82,85]. In addition, Cohn
was an important promoter of applied microbiology. He
gave lectures in agricultural botany, advised farmers on
the diagnosis and treatment of plant diseases caused by
fungal infections, became a pioneer in the analysis of
water as one possible source of infectious diseases, and
described in detail the damage to trees by hurricanes
and lightning [80,197^200].
In 1875 on the 50th anniversary of the doctorate of his
mentor Professor Go«ppert, Cohn initiated the work on the
£ora of cryptogams in Silesia and then published the work
in several volumes between 1877 and 1908 [201]. In the
`Schlesische Gesellschaft fu«r Vaterla«ndische Kultur' (the
Silesian Society of National Culture), a type of academy
in which he served as the secretary of the botanical section Fig. 7. The new Institute of Plant Physiology and Museum of Botany,
for more than 30 years, it was decided that the develop- opened 29 April 1888. Photographed 25 June 1998.

FEMSRE 678 29-5-00

 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249 245

One of the postulates that Cohn defended during his

oral doctoral examination was the need for an Institute
of Plant Physiology. During his academic career, he never
neglected this goal, but the realization was impeded by
many obstacles. By his continuous e¡ort, he was allowed
in 1866 to use several empty and dark rooms in the old
convent of the university located in the center of the town
to set up a laboratory of plant physiology (Fig. 6). By
di¤cult and continuous negotiations with the ministers
of agriculture and culture, he received a small amount of
¢nancial support for the costs of the equipment, lighting,
sanitary installation, and the salary of a technician. Very
often, Cohn himself laid out the money and was reim-
bursed after many months [211^213]. Many students and

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

scientists came from abroad to study with him and many
of these students later obtained leading positions. The in-
adequacy of rooms for research and teaching and the need
for a museum of botany ¢nally led, after many years of
planning and discussion, to a successful proposal for a
new building, which was opened with a ceremony on April
29, 1888. The new building, located in the botanical gar-
den, contained the herbarium and the museum, a lecture
room, the Institute of Plant Physiology with laboratories
and the library, the o¤ce for the director of the botanical
garden, and apartments for employees [213]. The building
is still in use (Fig. 7).

Fig. 9. Gravesite of Ferdinand Cohn and his wife Pauline Cohn in the
Jewish Cemetery in Breslau (Wroclaw). The German and Polish texts of
the inscription on the tablet translate as follows: Ferdinand Julius
Cohn, 1828^1898. Botanist and Microbiologist, Pioneer in Modern Mi-
crobiology and the Taxonomy of Microorganisms, Founder of the Insti-
tute of Plant Physioloy of the University of Breslau (1866), Promoter of
Robert Koch. On the 100th Anniversary of his Death on June 25, 1998
in Breslau. Vereinigung fu«r Allgemeine und Angewandte Mikrobiologie,
Deutsche Gesellschaft fu«r Hygiene und Mikrobiologie, und Gesellschaft
fu«r Virologie, Muzeum Historyczne we Wroclawin.

From the beginning of his career, Cohn communicated

Fig. 8. Ferdinand Cohn (from [214]).
with many of his contemporaries by letter and by personal
contact during meetings and private journeys [214]. Dur-
ing the last decade of his life, when he was no longer at the
forefront of science, he published articles on historical
aspects and overview articles, e.g. on Tabaschir or man-
dragora [215], the history of botany and botanical gardens
[216^218], Caspar Schwenckfeld [219], and Laurentius
Scholz von Rosenau [220]. Cohn was honored by numer-
ous distinctions from academies, societies, universities, and
his home town Breslau. The German Society of Hygiene
and Microbiology awarded a Ferdinand Cohn medal in
the 1980s. His great personality and his important work
have been illuminated in several articles [35,79,196,212,
221^227].
Cohn was a personality molded by an education in clas-
sical art. His Jewish faith and his modesty led him to

FEMSRE 678 29-5-00

246 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249

avoid political activities, although as a student he partici-
pated actively in the 1848 revolution in Berlin. His sus-
[23]
tained importance in biology was in two ¢elds: the sex-
uality and development of lower plants and the concept [24]
that bacteria are organisms with distinct, heritable charac-
teristics. He proposed principles of bacterial taxonomy, [25]
knowing that at his time the methodical means to elabo-
[26]
rate a modern taxonomy on a phylogenetic basis were not
available. Cohn discovered the development and heat re- [27]
sistance of bacterial endospores.
[28]
[29]
References
Sphaeroplea annulina. Monatsber. K. Akad. Wissensch. Berlin, pp.
335^351.
ë ber Stephanosphaera pluvialis.
Cohn, F. and Wichura, M. (1856) U
Acad. Caes. Leopold. Nova Acta 26, 3^31.
Cohn, F. (1855) U ë ber das Geschlecht der Algen. Jahrb. Schles. Ges.
Vaterl. Kultur 33, 95^105.
Cohn, F. (1856) Beobachtungen u«ber den Bau und die Fortp£anzung
von Volvox globator. Ann. Sci. Nat. (Bot.) 5, 323^332.
Cohn, F. (1875) Die Entwicklungsgeschichte der Gattung Volvox.
Beitr. Biol. P£anz. 1, 93^115.
Farley, J. (1977) The Spontaneous Generation Controversy from
Descartes to Oparin. John Hopkins University Press, Baltimore, MD.
Mayr, E. (1982) The Growth of Biological Thought. Harvard Uni-
versity Press, Cambridge, MA.
Lechevalier, H.A. and Solotorovsky, M. (1965) Three Centuries of
Microbiology. McGraw-Hill, New York.

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

[1] Wilson, C. (1995) The Invisible World. Princeton University Press,
Princeton, NJ.
[2] Sloan, P.R. (1992) Organic molecules revisited; and Roe, S.A. (1992)
Bu¡on and Needham: Diverging views on life and matter. In: Bu¡on
88 (Beaune, J.-C., Benoit, S., Gayon, J., Roger, J. and Worono¡, D.,
Eds.), pp. 415^438 and 440^450. J. Vrin, Paris.
[3] Shapin, S. (1996) The Scienti¢c Revolution. The University of Chi-
cago Press, Chicago, IL.
[4] Ruestow, E.G. (1984) Leeuwenhoek and the campaign against spon-
taneous generation. J. Hist. Biol. 17, 225^248.
[5] Schipperges, H. (1968) Die Versammlung Deutscher Naturforscher
und A î rzte im 19. Jahrhundert. Wissenschaftliche Verlagsgesellschaft,
Stuttgart.
[6] Schipperges, H. (1998) Weltbild und Wissenschaft im Spiegel der
`Naturforscherversammlungen'. In: Zwei Jahrhunderte Wissenschaft
und Forschung in Deutschland (D. v. Engelhardt, Ed.), pp. 151^159.
Wissenschaftliche Verlagsgesellschaft, Stuttgart.
[7] Pfe¡er, W. (1897) P£anzenphysiologie, Bd. I., Wilhelm Engelmann
Verlag, Leipzig.
[8] Auerbach, F. (1922) Ernst Abbe, 2nd edn. Leipzig.
[9] von Rohr, M. (1930) Zur Geschichte der ZeiMischen Werksta«tten bis
zum Tode Ernst Abbe's. Im Selbstverlag, Jena.
[10] Weigert, C. (1878) Zur Technik der mikroskopischen Bakterienunter-
suchungen. Arch. Mikrosk. Anat. 15, 258^260.
[11] Reichardt, O. and Stu«renburg, C. (1868) Lehrbuch der Mikroskopi-
schen Photographie. Verlag von Quandt and Ha«ndel, Leipzig.
[12] Koch, R. (1877) Untersuchungen u«ber Bakterien VI. Verfahren zur
Untersuchung, zum Conservieren und Photographieren. Beitr. Biol.
P£anz. 2, 399^434.
[13] Heymann, B. (1932) Robert Koch, 1. Teil 1843^1882. Akademische
Verlagsgesellschaft, Leipzig.
[14] Koch, R. (1878) Untersuchungen u«ber die A ë tiologie der Wundinfec-
tionskrankheiten. F.C. Vogel, Leipzig.
[15] Harris, H. (1999) The Birth of the Cell. Yale University Press, New
Haven, CT.
[16] Purkinje, J.E. (1839) U ë ber die Analogie in den Strukturelementen des
p£anzlichen und tierischen Organismus. Breslau.
[17] Schleiden, M.J. (1845) Grundzu«ge der wissenschaftlichen Botanik,
2nd edn. Leipzig.
[18] Cohn, F. (1850) Zur Lehre vom Wachstum der P£anzenzelle. Acad.
Caes. Leopold. Nova Acta 22, 509^540.
[19] Sachs, J. (1860) Geschichte der Botanik vom 16. Jahrh. bis 1860.
Oldenbourg Verlag, Munich.
[20] Cohn, F. (1854) Untersuchungen u«ber die Entwicklungsgeschichte
der mikroskopischen Algen und Pilze. Acad. Caes. Leopold. Nova
Acta 24, 101^256.
[21] Cohn, F. (1850) Nachtrag zur Naturgeschichte des Protococcus plu-
vialis, Ku«tzing. Acad. Caes. Leopold. Nova Acta 22, 607^764.
[22] Cohn, F. (1855) U ë ber die Entwicklung und Fortp£anzung der
[30] Darwin, C. (1859) On the Origin of Species by Means of Natural
Selection. J.M. Dent and Sons, London.
[31] Haeckel, E. (1866) Allgemeine Entwicklungsgeschichte der Organis-
men. Georg Reiner, Berlin.
[32] Cheesman, D.F. (1964) Varro and the small beasts: a bimillennium
for microbiologists. Nature 203, 911^912.
[33] Eckart, W.U. (1998) Geschichte der Medizin, 3rd edn. Springer Ver-
lag, Berlin.
[34] van Leeuwenhoek, A. (1684) Microscopical observations about ani-
mals in the scurf of the teeth. Trans. R. Soc. Lond. 14, 568^574.
[35] Bulloch, W. (1938) The History of Bacteriology, 2nd edn. 1960. Ox-
ford University Press, Oxford.
[36] Lo«¥er, F. (1887) Vorlesungen u«ber die geschichtliche Entwicklung
der Lehre von den Bacterien, erster Teil. Verlag R.C.W. Vogel, Leip-
zig.
[37] Mu«ller, O.F. (1786) Animalcula Infusoria £uviatilia et marina. Hau-
niae.
[38] Ehrenberg, C.G. (1838) Die Infusionsthierchen als vollkommene Or-
ganismen. Leopold Voss, Leipzig.
[39] Dujardin, F. (1841) Histoire Naturelle des Zoophytes. Paris.
[40] Perty, M. (1852) Zur Kenntnis kleinster Lebensformen nach Bau,
Funktionen, Systematik mit Spezialverzeichnis der in der Schweiz
beobachteten. Bern.
[41] Clusius, C. (1601) Fungorum in Pannoniis observatorum brevis his-
toria. Antwerpen, reprinted 1983, Graz.
[42] Bauhin, C. (1620) Prodromus theatri botanici. Frankfurt ; (1623) Pi-
nax theatri botanici. Basel.
[43] de Tournefort, J.P. (1700) Institutiones rei herbariae. Parisiis. Editio
tertia. Paris 1719.
[44] Malpighi, M. (1675, 1679) Anatome plantarum. I^II. London, re-
printed Brussels 1968.
[45] Micheli, P.A. (1729) Nova plantarum genera juxta Tournefortii meth-
odum disposita. Florentiae, repr. Richmond 1976.
[46] von Linnë, C. (1744) Systema naturae, 4th edn. David, Paris.
[47] Schro«ter, J. (1908) Pilze. In: Kryptogamen£ora von Schlesien (Cohn,
F., Ed.), Vol. 3.1, J.U. Kern Verlag, Breslau; Vol. 3.2 (1893^1897).
[48] Tillet, M. (1755) Dissertation on the cause of the corruption and
smutting of the kernels of wheat in the head, translated by: Phyto-
pathological Classics no. 5, Am. Phytopathol. Soc. 1937.
[49] Targioni-Tozzetti, G. (1767) Alimurgia, part V, Phytopathological
Classics no. 9, Am. Phytopathol. Soc. 1952.
[50] Prëvost, B. (1807) Mëmoire sur la cause immëdiate de la carie ou
charbon de blës, et de plusieurs autres maladies des plantes, et sur les
prëservatifs de la carie. Paris. Engl. Transl. Phytopathological Clas-
sics no. 6, Am. Phytopathol. Soc. 1939.
[51] Millardet, P.M.A. (1885) The discovery of Bordeaux mixture. Phyto-
pathological Classics no. 3, Am. Phytopathol. Soc. 1933.
[52] de Bary, A. (1866) Morphologie und Physiologie der Pilze, Flechten
und Myxomyceten. Leipzig.
[53] de Bary, A. (1884) Vergleichende Morphologie und Biologie der
Pilze, Myzetozoen und Bacterien, Verlag Engelmann, Leipzig.

FEMSRE 678 29-5-00

 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
[54] Brefeld, O. (1872) Botanische Untersuchungen u«ber Schimmelpilze.
Arthur Felix, Leipzig.
[55] Orlob, G.B. (1964) Vorstellungen u«ber die A ë tiologie in der Ge-
schichte der P£anzenkrankheiten. P£anzenschutz Nachr. Bayer 17,
185^272.
[56] Cohn, F. (1851) Die Entwicklungsgeschichte des Pilobolus crystalli-
nus. Acad. Caes. Leopold. Nova Acta 23, 493^536.
[57] Cohn, F. (1855) Empusa muscae und die Krankheit der Stuben£iegen.
Acad. Caes. Leopold. Nova Acta 25, 299^360.
[58] Persoon, C.H. (1801) Synopsis Methodica Fungorum. Go«ttingen.
[59] Fries, E. (1821^1832) Systema Mycologicum, Vol. 3. Uppsala.
[60] Brefeld, O. (1872^1908) Untersuchungen aus dem Gesamtgebiete der
Mykologie, Heft I^XIV. Felix, Leipzig.
[61] Raulin, J. (1869) Chemical studies on growth. Ann. Sci. Nat. Bot. 11,
93^299.
[62] Henle, J. (1840) Von den Miasmen und Contagionen, in: Pathologi-
sche Untersuchungen. August Hirschwald Verlag, Berlin.
[63] Pasteur, L. (1861) Mëmoire sur les corpuscules organisës qui existent
dans l'atmosphe©re. Examen de la doctrine des gënërations sponta-
nëes. Ann. Sci. Nat. 16, 5^98 ; Ann. Chim. Phys. 64, 5^110 (1862).
[64] Pasteur, L. (1861) Animalcules infusoires vivant sans gaz oxyge©ne
libre et dëterminant des fermentations. C.R. Acad. Sci. 52, 344^347.
[65] Cohn, F. (1851) Beitra«ge zur Entwicklungsgeschichte der Infusorien.
Ztschr. Wiss. Zool. 3, 257^279; 4, 253^281.
[66] Cohn, F. (1875) Untersuchungen u«ber Bakterien I. Beitr. Biol. P£anz.
1, 127^224.
[67] Schroeter, J. (1875) U ë ber einige durch Bacterien gebildete Pigmente.
Beitr. Biol. P£anz. 1, 109^126.
[68] de Bary, A. (1854) Ueber die Entwicklung und den Zusammenhang
von Aspergillus glaucus und Eurotium. Bot. Ztg. 12, 425^434, 441^
451, 465^476.
[69] Koch, R. (1878) Neuere Untersuchungen u«ber die Mikroorganismen
bei infectio«sen Wundkrankheiten. Dtsch. Med. Wochenschr. 4, 531^
532.
[70] Esmarch, E. (1886) U ë ber die Modi¢kation des Koch'schen Platten-
verfahrens zur Isolierung und zum quantitativen Nachweis von Mik-
roorganismen. Cbl. Bakt. Parasitenkd. 1, 293^301.
[71] Esmarch, E. (1887) U ë ber die Reinkultur eines Spirillum. Cbl. Bakt.
Parasitenkd. 1, 225^230.
[72] Frankland, P.F. (1886) Proc. R. Soc. Lond. 40, 509^544.
[73] Petri, R.J. (1887) Eine kleine Modi¢kation des Koch'schen Platten-
verfahrens. Zbl. Bakteriol. 1, 279^286.
[74] Hesse, W. (1992) Walther and Angelina Hesse. ASM News 58, 425^
428.
[75] Ho¡mann, H. (1869) U ë ber die Kultur und Fa«rbung von Bakterien.
Bot. Ztg. p. 252, cited in Lo«¥er, F., 1887.
[76] Cohn, F. (1875) Untersuchungen u«ber Bakterien II. Beitr. Biol.
P£anz. 1, 141^207.
[77] Billroth, T. (1874) Untersuchungen u«ber die Vegetationsformen von
Coccobacteria septica und den Antheil welchen sie an der Entstehung
und Verbreitung der accidentellen Wundkrankheiten haben. Berlin.
[78] Billroth, T. and Ehrlich, P. (1877) Untersuchungen u«ber Coccobac-
teria septica. Langenbeck's Arch. Chir. 20, 403^418.
[79] Drews, G. (1999) Ferdinand Cohn: a promoter of modern micro-
biology. Nova Acta Leopold. 312, 13^43.
[80] Cohn, F. (1872) Ueber Bacterien, die kleinsten lebenden Wesen. In:
Sammlung Gemeinversta«ndlicher Wissenschaftlicher Vortra«ge (Virch-
ow, R. and v. Holtzendor¡, F., Eds.), pp. 2^35, Lu«deritz'sche Ver-
lagsbuchhandlung, Berlin.
[81] Cohn, F. (1879) U ë ber die morphologische Einheit der Spaltpilze.
Dtsch. Med. Wochenschr. 5, 73^76.
[82] Cohn, F. (1877) Untersuchungen u«ber Bakterien IV. Beitra«ge zur
Biologie der Bacillen. Beitr. Biol. P£anz. 2, 249^276.
[83] Staley, J.T., Bryant, M.P., Pfennig, N. and Holt, J.G. (1989) Bergey's
Manual of Systematic Bacteriology, Vol. 3. Williams and Wilkins,
Baltimore, MD.
FEMSRE 678 29-5-00
247
[84] Cohn, F. (1866) U ë ber die Physiologie und Systematik der Oscillari-
neen und Florideen. Jahrb. Schles. Ges. Vaterl. Kultur 44, 134^139.
[85] Cohn, F. (1867) Beitra«ge zur Physiologie der Phycochromaceen. M.
Schultze's Arch. Mikrosk. Anat. 3, 1^60.
[86] Cohn, F. (1879) U ë ber ein Thallophytensystem. Jahrb. Schles. Ges.
Vaterl. Kultur 57, 279^289.
[87] Hallier, E. (1868) Researches into the nature of vegetable parasitic
organisms. Med. Times Gaz. Lond. 2, 222^223.
[88] de Bary, A. (1868) Zur Beurteilung der Pilzschriften des Herrn Hal-
lier. Bot. Ztg. 26, 294^296.
[89] Lister, J. (1872) On the germ theory of putrefaction and other fer-
mentative changes. Nature, July 10 and 17.
[90] Klebs, E. (1873) Beitra«ge zur Kenntnis der Micrococcen. Arch. Exp.
Pathol. Pharmakol. 1, 31^64.
[91] Klebs, E. (1875) Beitra«ge zur Kenntnis der pathogenen Schistomy-
ceten. Arch. Exp. Pathol. Pharmakol. iv, 107, 207, 409, cited in
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
Bulloch, 1960.
[92] Lankester, E.R. (1873) On a peach-coloured bacterium ^ Bacterium
rubescens. Q. J. Microsc. Sci. 13, 408^425.
[93] Lankester, E.R. (1885) The pleomorphism of the Schizophyta. Q. J.
Microsc. Sci. 26, 499^505.
[94] Koch, R. (1877) Die A ë tiologie der Milzbrandkrankheit, begru«ndet
auf die Entwicklungsgeschichte des Bacillus anthracis. Beitr. Biol.
P£anz. 2, 277^310.
[95] Winogradsky, S. (1890) Sur les organismes de la nitri¢cation. C.R.
Acad. Sci. 110, 1013^1016.
[96] Winogradsky, S.N. (1891) U ë ber die Organismen der Nitri¢kation.
Vierteljahrsschr. Naturforsch. Ges. Zu«rich 36, 176^208.
[97] Winogradsky, S.N. (1896) Zur Mikrobiologie des Nitri¢kations-
prozesses. Zentralbl. Bakteriol. (II) 2, 415^428, 449^458.
[98] Stanier, R.Y. and van Niel, C.B. (1962) The concept of a bacterium.
Arch. Mikrobiol. 42, 17^35.
[99] Woese, C.R. and Fox, G.E. (1977) Phylogenetic structure of the
prokaryotic domain : the primary kingdoms. Proc. Natl. Acad. Sci.
USA 74, 5088^5090.
[100] Woese, C.R., Kandler, O. and Wheelis, M.L. (1990) Towards a
natural system of organisms : proposal for the domains Archaea,
Bacteria, and Eucaria. Proc. Natl. Acad. Sci. USA 87, 4576^4579.
[101] Krieg, N.R. and Holt, J.G. (1984) Bergey's Manual of Systematic
Bacteriology, Vol. 1, p. 1. Williams and Wilkins, Baltimore, MD.
[102] Stackebrandt, E., Tindall, B., Ludwig, W. and Goodfellow, M.
(1999) Diversity and systematics, in: Biology of the Prokaryotes,
(Lengeler, J., Drews, G. and Schlegel, H.G., eds.), pp. 699^700,
Thieme, Stuttgart.
[103] Gupta, R.S. (1998) Protein phylogenies and signature sequences: a
reappraisal of evolutionary relationships among archaebacteria, eu-
bacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62, 1435^1491.
[104] Gason, G.L. (1995) The Private Science of Louis Pasteur. Princeton
University Press, Princeton, NJ.
[105] Joblot, L. (1718) Descriptions et Usages de Plusieurs Nouveaux
Microscopes. Paris.
[106] Needham, T. (1749) A summary on some late observations upon the
generation, composition, and decomposition of animal and vegeta-
ble material. Phil. Trans. R. Soc. Lond. 490, 615.
[107] Bu¡on, G.L.L. (1749^1804) Histoire Naturelle. Paris.
[108] Spallanzani, L. (1765) Saggio di osservazioni microscopiche concer-
nenti il sistema della generazione dei Signori di Needham e Bu¡on.
Modena.
[109] Spallanzani, L. (1776) Opuscoli de ¢sica animale e vegetabile. Mod-
ena.
[110] Schulze, F. (1836) Vorla«u¢ge Mittheilung der Resultate einer exper-
imentellen Beobachtung u«ber Generatio aequivoca. Ann. Phys.
Chem. Leipzig 34, 487^489.
[111] Schro«der, H. and von Dusch, T. (1854) Ueber Filtration der Luft in
Beziehungen auf Fa«ulniss und Ga«hrung. Ann. Chem. Pharm. 39,
232^243.
248 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
[112] Pouchet, F.A. (1859) Hëtërogënie ou Traitë de la Gënëration Sspon-
tanëe, Basë sur de Nouvelles Expëriences. Baillie©re, Paris.
[113] Mi£et, D. (1883) Untersuchungen u«ber die in der Luft suspendierten
Bakterien. Beitr. Biol. P£anz. 3, 119^140.
[114] Pasteur, L. (1857) Mëmoire sur la fermentation appelëe lactique.
C.R. Acad. Sci. 45, 913^916.
[115] Pasteur, L. (1860) Mëmoire sur la fermentation alcoolique. Ann.
Chim. phys. 3e Ser. 48, 323^426.
[116] Pasteur, L. (1876) Etudes sur la Bie©re, Ses Maladies, Causes qui les
Provoquent, Procëdë pour la Rendre Inaltërable avec une Thëorie
Nouvelle de la Fermentation. Paris.
[117] Pasteur, L. (1864) Mëmoire sur la fermentation acëtique. Ann. Sci.
Ec. Norm. Supër. 1, 113^158.
[118] Tyndall, J. (1881) Essays on the Floating Matter of the Air in
Relation to Putrefaction and Infection. London.
[119] Roberts, W. (1874) Studies on biogenesis. Phil. Trans. R. Soc. Lond.
164, 457^477.
[120] Eidam, E. (1875) Untersuchungen u«ber Bakterien III. Beitr. Biol.
P£anz. 1, 208^224.
[121] Tyndall, J. (1877) Further researches on the deportment and vital
persistence of putrefactive and infective organisms from a physical
point of view. Phil. Trans. R. Soc. Lond. 167, 149^206.
[122] Giovannoni, S.J., Turner, S., Olsen, G.J., Barns, S., Lane, D.J. and
Pace, N.R. (1988) Evolutionary relationship among cyanobacteria
and green chloroplasts. J. Bacteriol. 170, 3584^3592.
[123] Doolittle, R.F. (1995) Of Archae and Eo: What's in a name? Proc.
Natl. Acad. Sci. USA 92, 2421^2423.
[124] Forterre, P. (1997) Protein versus rRNA: problems in rooting the
universal tree of life. ASM News 63, 89^95.
[125] Brown, J.R. and Doolittle, W.F. (1995) Root of the universal tree of
life based on ancient aminoacyl-tRNA synthetase gene duplication.
Proc. Natl. Acad. Sci. USA 92, 2441^2445.
[126] Olsen, G.J. and Woese, C. (1997) Archaeal genomics, an overview.
Cell 89, 991^994.
[127] Dennis, P.P. (1997) Ancient ciphers: Translation in Archaea. Cell
89, 1007^1010.
[128] Blankenship, R.E. (1992) Origin and early evolution of photosyn-
thesis. Photosynth. Res. 33, 91^111.
[129] Schubert, W-D., Klukas, O., Saenger, W., Witt, H.T., Fromme, P.
and KrauM, N. (1998) A common ancestor for oxygenic and anoxy-
genic photosynthetic systems: A comparison based on the structural
model of photosystem I. J. Mol. Biol. 280, 297^314.
[130] Xiong, J., Inoue, K. and Bauer, C.E. (1998) Tracking molecular
evolution of photosynthesis by characterization of a major photo-
synthesis gene cluster from Heliobacillus mobilis. Proc. Natl. Acad.
Sci. USA 95, 14851^14856.
[131] Smith, J.M., Szathmäry, E. (1995) The Major Transitions in Evo-
lution. W.H. Freeman and Co., New York.
[132] Bintrim, S.B., Donohue, T.J., Handelsman, J., Roberts, G.P. and
Goddman, R.M. (1997) Molecular phylogeny of archaea from soil.
Proc. Natl. Acad. Sci. USA 94, 277^282.
[133] Overmann, J. and Tuschak, C. (1997) Phylogeny and molecular
¢ngerprinting of green sulfur bacteria. Arch. Microbiol. 167, 302^
309.
[134] Hillis, D.M. (1997) Biology recapitulates phylogeny. Science 276,
218^219.
[135] Imho¡, J.F. (1999) A phylogenetically oriented taxonomy of anoxy-
genic phototrophic bacteria. In: The Phototrophic Prokaryotes (Pe-
schek et al., Eds.), pp. 763^774, Kluwer Academic/Plenum, New
York.
[136] Liebig, J. (1846) Die Chemie in ihrer Anwendung auf Agricultur
und Physiologie, 6. edn. F. Vieweg, Braunschweig.
[137] von Liebig, J. (1839) U ë ber die Erscheinungen der Ga«hrung, Fa«ulniss
und Verwesung und ihre Ursachen. Ann. Phys. Chem. 18, 106^150.
[138] Lavoisier, A.L. (1789) Traitë Elëmentaire de Chymie. Paris.
[139] Gay-Lussac, J. (1810) Extrait d'un mëmoire sur la fermentation.
Ann. Chim. 76, 245^259.
FEMSRE 678 29-5-00
[140] Bëchamp, A. (1868) Sur les granulations molëculaires des fermenta-
tions et des tissues des animaux. C.R. Acad. Sci. 66, 366; De l'or-
igine et du dëveloppement des bactëries. C.R. Acad. Sci. 66, 859.
[141] Fabbroni, A. (1787) Dell'Arte de Fare il Vino. Florence.
[142] Cagniard-Latour, C. (1837) Mëmoire sur la fermentation vineuse.
Ann. Chim. Phys. 68, 206^222.
[143] Schwann, T. (1837) Vorla«u¢ge Mittheilung betre¡end Versuche u«ber
die Weinga«hrung und Fa«ulnis. Ann. Phys. Chem. 41, 184.
[144] Ku«tzing, F. (1837) Microscopische Untersuchungen u«ber die Hefe
und Essigmutter nebst mehreren andern dazu geho«rigen vegetabili-
schen Gebilden. J. Prakt. Chem. 11, 385^409.
[145] Mitscherlich, E. (1841) U ë ber die chemische Zersetzung und Verbin-
dung vermittelst Contac-Substanzen. Ber. Verhandl. K. Preuss.
Akad. Wiss. Berlin, pp. 379^396.
[146] Traube, M. (1858) Theorie der Fermentwirkung. Berlin.
[147] Buchner, E., Buchner, H. and Hahn, M. (1903) Die Zymasega«rung.
Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023
Untersuchungen u«ber den Inhalt der Hefezellen und die biologische
Seite des Ga«rungsproblems. Munich.
[148] Ingenhousz, J. (1779) Experiments upon Vegetables. P. Elmsly in the
Strand and H. Payne in Pall Mall, London.
[149] Ingenhousz, J. (1798) U ë ber die Nahrung der P£anzen und die Du«ng-
ung des Bodens. Voigt Mag. I, 97^105.
[150] Saussure, N.T. (1804) Recherches Chimiques sur la Vëgëtation.
Nyon, Paris.
[151] Sachs, J. (1865) Handbuch der Experimental Physiologie der P£an-
zen. Leipzig.
[152] Huzisige, H. and Ke, B. (1993) Dynamics of the history of photo-
synthetic research. Photosynth. Res. 38, 185^209.
[153] Ruben, S., Randall, M., Kamen, M.D. and Hyde, J.L. (1941) Heavy
oxygen as tracer in the study of photosynthesis. J. Am. Chem. Soc.
63, 877^878.
[154] Molisch, H. (1907) Die Purpurbakterien nach neueren Untersuchun-
gen. Gustav Fischer Verlag, Jena.
[155] Engelmann, T.W. (1882) U ë ber Licht- und Farbenperzeption nieder-
ster Organismen. P£u«ger's Arch. Ges. Physiol. 29, 387^400.
[156] Engelmann, T.W. (1883) Bacterium photometricum, ein Beitrag zur
vergleichenden Physiologie des Licht- und Farbensinns. P£u«ger's
Arch. Ges. Physiol. 30, 95^124.
[157] Engelmann, T.W. (1888) Die Purpurbakterien und ihre Beziehungen
zum Licht. Bot. Ztg. 46, 661^669, 677^689, 693^701, 709^720.
[158] Winogradsky, S. (1889) Recherches physiologiques sur les sulfobac-
tëries. Ann. Inst. Pasteur 3, 49^60.
[159] Beijerick, M.W. (1895) U ë ber Spirillum desulfuricans als Ursache von
Sulfatreduktion. Zbl. Bakteriol. Parasitenkd. Infektionskr. Hyg.
Abt. I Orig. 1, 1^9, 49^59, 104^114.
[160] Beijerinck, M.W. (1888) Cultur des Bacillus radicola aus den Kno«ll-
chen. Bot. Ztg. 46, 740^750.
[161] Beijerinck, M.W. and van Delden, A. (1902) U ë ber die Assimilation
des freien Sticksto¡s durch Bakterien. Zbl. Bakteriol. Parasitenkd.
Infektionskr. Hyg. Abt. II 9, 3^43.
[162] Beijerinck, M.W. (1901) On oligonitrophilic microbes. Centralb.
Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. II 7, 561^582.
[163] Winogradsky, S. (1895) Recherches sur l'assimilation de l'azote libre
de l'atmosphe©re par les microbes. Arch. Sci. Biol. St. Petersburg 3,
297^352.
[164] Kluyver, A.J. (1931) The Chemical Actions of Microorganisms.
University Press, London.
[165] Kluyver, A.J. and van Niel, C.B. (1956) The Microbes Contribution
to Biology. Harvard University Press, Cambridge, MA.
[166] Goodsir, J. (1842) History of a case in which a £uid periodically
ejected from the stomach contained vegetable organisms of an un-
described form. Edinb. Med. Sci. J. 57, 430^443.
[167] Virchow, R. (1856) Thrombose und Embolie. Gefa«ssentzu«ndung
und septische Infection. Ges. Abh. Wiss. Med., Frankfurt a.M.
[168] Gussenbauer, C. (1882) Septha«mie, Pyoha«mie und Pyo-septha«mie.
Dtsch. Chir. (Billroth and Luecke, Eds.), Vol. 4.
[169] Davaine, C.-J. (1854) Sur des animalcules infusoires trouvës dans les
 G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249 249

selles de malades atteints du cholëra et d'autres a¡ections. C.R. Soc.
Biol. 2e Sër. 1, 129.
[170] Bassi, A. (1837) Del Mal del Segno Calcinaccio o Moscardino, Ma-
lattia che A¥ige i Bacchi da Seta e sul Modo di Liberarne le Be-
gattaje anche le piu© Infestate. Milan.
[171] Obermeier, O. (1873) Vorkommen feinster, eine Eigenbewegung zei-
gender Fa«den im Blut von Recurrenskranken. Zbl. Med. Wissensch.
XI, 10.
[172] Rosenbach, F.J. (1884) Mikro-Organismen bei den Wund-Infek-
tions-Krankheiten. J.F. Bergmann, Wiesbaden.
[173] Hallier, E. (1867) Das Cholera Contagium. Botanische Untersu-
chungen Aerzten und Naturforschern Mitgetheilt. Leipzig.
[174] Hallier, E. (1869) Die Parasiten der Infectionskrankheiten. Zeitschr.
Parasitenkd. Jena, 117, 291.
[175] Koch, R. (1881) Zur Untersuchung von pathogenen Organismen.
Mitt. Kais. Gesundheitsamt 1, 1^48.
[198] Cohn, F. (1858) U ë ber die Wettersa«ule von Mangschu«tz. Jb. Schles.
Ges. Vaterl. Kultur 36, 79^89.
[199] Cohn, F. (1872) U ë ber den Brunnenfaden Crenothrix polyspora mit
Bemerkungen u«ber die mikroskopische Analyse des Brunnenwass-
ers. Beitr. Biol. P£anz. 1, 108^132.
[200] Cohn, F. (1876) U ë ber die in Schlesien im Getreide beobachteten
Brandpilze. Jb. Schles. Ges. Vaterl. Kultur 54, 135^137.
[201] Cohn, F. (Ed.) Kryptogamen-Flora von Schlesien. Vol. 1: Stenzel,
K.G. (1877) Gefa«M-Kryptogamen, Limprecht, K.G. (1877) Laub-
und Lebermoose, Braun, A. (1877) Characeen. Vol. 2.1: Kirchner,
O. (1878) Algen. Vol. 3.1: Schro«ter, J. (1893^97) Pilze. Vol. 3.2:
Schro«ter, J. (1908) Pilze. J.U. Kern Verlag, Breslau.
[202] Cohn, F. (1851, 1853) Bericht u«ber die Entwicklung der Vegetation
in Schlesien. Jb. Schles. Ges. vaterl. Kultur. 29, 1^24, 53^76; 31,
113^151.
[203] Cohn, F. (1850) U ë ber Aldrovanda vesiculosa. Flora 33, 673^683.
ë ber die Bewegung der Bla«tter bei unseren einhei-

Downloaded from https://academic.oup.com/femsre/article/24/3/225/561657 by guest on 22 August 2023

[176] Escherich, T. (1885) Die Darmbakterien des Neugeborenen und [204] Cohn, F. (1859) U
Sa«uglings. Fortschr. Med. 3, 515^522, 547^554. mischen Oxalis Arten. Jb. Schles. Ges. Vaterl. Kultur 37, 84^89.
[177] Koch, R. (1884) Die A ë tiologie der Tuberkulose. Mitt. Kais. Gesund- [205] Cohn, F. (1861) Contractile Gewebe im P£anzenreich. Jb. Schles.
heitsamt 2, 1^88. Ges. Vaterl. Kultur 39, 1^48.
[178] Koch, R. (1882) Die A ë tiologie der Tuberculose. Berl. Klin. Wschr. [206] Cohn, F. (1865) U ë ber die Gesetze der Bewegung der microscopi-
19, 221^230. schen P£anzen und Thiere unter Ein£uM des Lichtes. Jb. Schles. Ges.
[179] Lo«¥er, F. (1884) Mitt. Reichsgesundheitsamt 2, 421^499. Vaterl. Kultur 42, 35^37.
[180] Koch, R. (1884) U ë ber die Cholerabakterien. Dtsch. Med. Wschr. 10, [207] Cohn, F. (1875) U ë ber die Function der Blasen von Aldrovanda und
725^728. Utricularia. Beitr. Biol. P£anz. 1, 71^89.
[181] Ogston, A. (1880) U ë ber Abscesse. Arch. Klin. Chir. 25, 588^600. [208] Cohn, F. (1882) U ë ber die mechanische Wirkung des Lichtes bei den
[182] Ogston, A. (1882) Micrococcus poisoning. J. Anat. Physiol. 16, 526^ P£anzen. Jb. Schles. Ges. Vaterl. Kultur 60, 179^186.
567. [209] Cohn, F. (1882) Die P£anze. J.U. Kern, Breslau, 2nd edn. 1897.
[183] Pasteur, L. (1880) Sur les maladies virulentes et en particulier sur la [210] Cohn, F. (1898) Die P£anze in der bildenden Kunst. Dtsch.
maladie appelëe vulgairement cholëra des poules. C.R. Acad. Sci. Rundsch. 97, 55^68.
90, 239^248. [211] Cohn, F. (1869) Bericht u«ber das p£anzenphysiologische Institut der
[184] Pasteur, L. (1883) Sur la vaccination charbonneuse. C.R. Acad. Sci. Universita«t Breslau. Jb. Schles. Ges. Vaterl. Kultur 47, 162^168.
96, 979^982. [212] Rosen, F. (1899) Ferdinand Cohn. Ber. Dtsch. Bot. Ges. 17, 162^
[185] Pasteur, L. and Thullier, L. (1882) Sur le rouget ou mal rouge de 168.
porcs. C.R. Acad. Sci. 95, 1120^1121. [213] Rosen, F. (1911) Das p£anzenphysiologische Institut. In: Festschrift
[186] Pasteur, L., Chamberland, C. and Roux, E. (1880) Sur l'etiologie du zur Feier des hundertja«hrigen Bestehens der Universita«t Breslau
charbon. Bull. Acad. Mëd. 2e Sër. 9, 682^692. (Kaufmann, G., Ed.), pp. 486^499. Ferdinand Hirt, Breslau.
[187] Lemaire, J. (1865) De l'Acide Phënique, de son Action sur les Vëg- [214] Cohn, P. (1901) Ferdinand Cohn, Bla«tter der Erinnerung. J.U.
ëtaux, les Animaux, les Ferments, les Venins, les Virus, les Miasmes Kern, Breslau.
et de ses Applications a© l'Industrie, a© l'Hygie©ne, aux Sciences Anat- [215] Cohn, F. (1887) Ueber Tabaschir. Beitr. Biol. P£anz. 4, 365^407.
omiques et a© la Thërapeutique. Paris. [216] Cohn, F. (1881) Beitrag zur Geschichte der Botanik. Jb. Schles. Ges.
[188] Lister, J. (1867) On a new method of treating compound fracture, Vaterl. Kultur 59, 302^311.
abscess. With observations on the conditions of suppuration Lancet [217] Cohn, F. (1888) Die Ga«rten in alter und neuer Zeit. Dtsch.
1, 364^373, 418^420. Rundsch. 5, 250^266.
[189] Lister, J. (1867) On the antiseptic principle in the practice of sur- [218] Cohn, F. (1856) Die Geschichte der Ga«rten. Jonas Verlagsbuch-
gery. Br. Med. J. 2, 246. handlung, Berlin.
[190] Koch, R. (1881) U ë ber Desinfection. Mitt. Kais. Gesundheitsamt 1, [219] Cohn, F. (1889) Caspar Schwenkfeld. In: Lebensbilder schlesischer
234^282. Aë rzte aus den letzten Jahrhunderten (Graetzer, D.J., Ed.), pp. 1^17.
[191] Cohn, F. (1894) Formaldehyd und seine Wirkungen auf Bakterien. Schottla«nder, Breslau.
Jb. Schles. Ges. Vaterl. Kultur 71, 23^31. [220] Cohn, F. (1890) Dr. Laurentius von Rosenau. Dtsch. Rundsch. 7,
[192] Metchniko¡, E. (1884) U ë ber die Beziehung der Phagocyten zu Milz- 109^126.
brandbacillen. Arch. Pathol. Anat. 97, 502^526. [221] Farmer, J.B. (1898) Ferdinand Cohn. Nature 58, 275.
[193] Behring, E. and Kitasato, S. (1890) U ë ber das Zustandekommen der [222] Geison, G.L. (1971) Cohn, Ferdinand Julius. Dict. Sci. Biogr. (Gil-
Diphtherie-Immunita«t und der Tetanus-Immunita«t bei Thieren. lispie, C.C., Ed.) Vol. III, pp. 336^341.
Dtsch. Med. Wchschr. 16, 1113. [223] Hoppe, B. (1983) Die Biologie der Mikroorganismen von F.J. Cohn.
[194] Ehrlich, P. (1897) Die Wertbemessung des Diphtherieheilserums und Sudho¡'s Arch. 67, 158^189.
deren theoretische Grundlagen. Klin. Jahrb. 6, 299^326. [224] Mez, C. (1900) Cohn, Ferdinand. Biogr. Jahrb. Dtsch. Nekrolog III,
[195] Ehrlich, P. (1900) On immunity with special reference to cell life. 284^296.
Proc. R. Soc. Lond. 66, 424^448. [225] Neisser, M. (1898) Ferdinand Cohn. Mu«nch. Med. Wschr. 45, 1005^
[196] Drews, G. (1998) Ferdinand Cohn, ein Wegbereiter der modernen 1007.
Mikrobiologie und P£anzenphysiologie. Freiburger Universita«tsbla«t- [226] Anon. (1898) Nekrolog F.J. Cohn. Jahrb. Schles. Ges. Vaterl. Kul-
ter 142, 29^84, Rombach, Freiburg. tur 76, 1^7.
[197] Cohn, F. (1857) Ein interessanter Blitzschlag. Acad. Caes. Leopold. [227] Drews, G. (1999) Ferdinand Cohn, a founder of modern microbi-
Nova Acta 26, 177^188. ology. ASM News 65, 547^553.

FEMSRE 678 29-5-00