See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/13794797

Classification and overview of the genera Streptococcus and Enterococcus

Article  in  Society for Applied Bacteriology symposium series · February 1997

Source: PubMed

CITATIONS READS

79 886

2 authors, including:

Robert A Whiley
Queen Mary, University of London
101 PUBLICATIONS   3,950 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

interactions between pseudomonas aeruginosa and oral streptococci cystic fibrosis isolates View project

All content following this page was uploaded by Robert A Whiley on 05 September 2014.

The user has requested enhancement of the downloaded file.

Journal of Applied Microbiology Symposium Supplement 1997, 83, 1S–11S

Classification and overview of the genera Streptococcus and

Enterococcus
J.M. Hardie and R.A. Whiley
Department of Oral Microbiology, St Bartholomew’s and the Royal London School of Medicine and Dentistry, Queen Mary and
Westfield College, London, UK

1. Introduction, 1S 3.1 Species and species groups, 5S

2. Historical review 3.2 Identification of Streptococcus species, 5S
2.1 Early history, 1S 4. Ecology and disease associations of Streptococcus
2.2 Early classifications, 2S 4.1 Ecology, 5S
2.3 Division of the genus Streptococcus and 4.2 Human diseases, 6S
creation of Streptococcus sensu stricto, 4.3 Animal diseases, 7S
Enterococcus and Lactococcus, 3S 5. Current classification of Enterococcus
2.4 Phenotypic characteristics of Streptococcus 5.1 Species and species groups, 7S
(sensu stricto), 4S 5.2 Identification of Enterococcus species, 7S
2.5 Phenotypic characteristics of Enterococcus, 4S 6. Ecology and disease associations of Enterococcus,
2.6 Phylogeny of Streptococcus and Enterococcus, 8S
4S 7. Conclusions, 9S
3. Current classification of Streptococcus 8. References, 9S

—
–––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––

1. INTRODUCTION estic, farm and aquatic animals (Devriese and Pot 1995; Har-
die and Whiley 1995).
The genera Streptococcus and Enterococcus both consist of
The development of antibiotic resistance amongst strains
Gram-positive, spherical or ovoid cells which are typically
of pneumococci and other streptococci, and the increasing
arranged in pairs or chains. They are non-sporing, facul-
occurrence of vancomycin resistance amongst enterococci, are
tatively anaerobic, catalase negative, homofermentative, and
worrying trends which have attracted considerable attention
have complex nutritional requirements. As described below,
during the 1990s and will be addressed by other contributors
they were for many years considered to belong to the same
to this symposium. Clear definition of the taxa involved in
genus (Streptococcus), but are now clearly recognized as being
human or animal infections is required for meaningful studies
distinct, alongside a number of other genera of lactic acid
on their epidemiology, pathogenic mechanisms and resistance
bacteria (LAB) (Schleifer and Ludwig 1995).
to antimicrobial agents. In this paper, the taxonomic history
The 40 or so currently recognized species of Streptococcus
of the streptococci and enterococci is reviewed briefly and
and 17 species of Enterococcus are widely distributed, mainly
their current classification described.
on mucosal surfaces of man and animals, including the gastro-
intestinal tract, but some are also found in soil, water, dairy
products and other foods, and on plants. Some species, such
2. HISTORICAL REVIEW
as Streptococcus pyogenes and Strep. pneumoniae, are well-
recognized as major human pathogens and many of the others
2.1 Early history
are capable of causing disease under appropriate circum-
stances. Similarly, there are many species within these genera It is over 100 years since the observation by Billroth (1874)
which are responsible for significant levels of disease in dom- of chain-forming cocci in wounds and his application of the
descriptive term streptococcos to these organisms. Since then
Correspondence to: Professor J. M. Hardie, Department of Oral
Microbiology, St Bartholomew’s and the Royal London School of Medicine and advances in our knowledge and understanding of each of the
Dentistry, Queen Mary and Westfield College, Turner Street, London E1 genera Streptococcus and Enterococcus have remained closely
2AD, UK. linked, largely because these bacteria were included within
© 1997 The Society for Applied Bacteriology
2S J .M . H A RD IE A ND R. A . W HI L EY
one genus (Streptococcus) from 1906 until 1984. The recog-
nition of Streptococcus and Enterococcus as distinct genera was
eventually made possible through the application of modern
molecular taxonomic approaches, as described below. For the
purposes of this historical review the terms streptococci and
Streptococcus are used to include species currently included
in both Streptococcus and Enterococcus.
By the end of the nineteenth century the importance of
Gram-positive, chain-forming cocci in infections of humans
and animals had been established. The name Streptococcus
had been used in the generic sense by Rosenbach (1884) to
describe such bacteria isolated from suppurative lesions in
man which he called Streptococcus pyogenes (see Jones 1978
and Colman 1990 for reviews of the early literature). Thier-
celin and Jouhaud (1903) had proposed the genus Enterococcus
for a potentially pathogenic Gram-positive diplococcus (Ent.
proteiformis) isolated from the intestine. The ‘enterocoque’ of
Thiercelin was later transferred to the genus Streptococcus
and given the species epithet faecalis by Andrewes and Horder
(1906). The early part of the twentieth century was marked by
several important technical developments and investigations
which were to have a great impact on streptococcal classi-
fication and the understanding of the clinical and economic
importance of the genus. Most notable of these innovations
were the demonstration of various types of haemolytic reac-
tion given by different strains when cultured on whole blood-
containing agar, the use of carbohydrate fermentation reac-
tions together with physiological and morphological tests for
characterization of streptococci from clinical, environmental
and dairy sources, and the detection of carbohydrate antigens
(‘c’ substance) in acid extracts of cell walls, by serological
testing. The latter approach developed by Lancefield (1933)
demonstrated among the streptococci which cause complete
or b-haemolysis that the distribution of the so-called group
antigens bore a relationship to the sources of the cultures and
gave excellent correlations with the groupings of streptococci
obtained by other workers using biochemical test reactions.
Indeed, one reviewer remarked that an unfortunate conse-
quence of the early success and ease of this serological tech-
nique in differentiating several important (pyogenic)
streptococci was to cause undue emphasis to be placed on the
possession of a Lancefield group antigen at the expense of
other taxonomic criteria, a trend which ‘. . . has therefore
hampered and is still hampering a better understanding of
the relationships between these bacteria’ (Jones 1978).
2.2 Early classifications
In 1937 Sherman published what was to become the most
widely accepted general classification of the streptococci. In
his scheme he incorporated the presence of a Lancefield group
antigen as one of 10 characteristics for separating the genus
into four primary divisions designated ‘pyogenic’, ‘viridans’,
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
‘lactic’ and ‘enterococci’. The other, mainly physiological,
characteristics consisted of the haemolytic reaction on blood
agar, growth at 10°C and at 45°C, in the presence of 6·5%
NaCl, at pH 9·6 and in 0·1% methylene blue, strong reducing
ability, survival at 60°C for 30 min and the production of
ammonia from peptone. The species or groups within the
divisions were characterized further on the basis of bio-
chemical tests. The ‘pyogenic’ division contained streptococci
associated with infections in man and animals, which were
strongly b-haemolytic and carried a Lancefield group antigen.
The species included here were Streptococcus pyogenes (Lance-
field group A), Strep. mastiditis (group B), Strep. equi (group
C), ‘animal pyogenes’ (group C), ‘human C’ (group C),
‘minute haemolytic streptococci’ (group F) together with
streptococci belonging to Lancefield groups G, E and H. The
latter were considered to be of doubtful status with respect
to haemolysis on blood agar and physiological characteristics.
In contrast with the ‘pyogenic’ division, Lancefield grouping
was not useful for discriminating between the ‘viridans’ strep-
tococci so that subdivision of these into species was based
entirely on biochemical and physiological characteristics.
Sherman considered his ‘viridans’ division to be the least
satisfactory of the four primary divisions with, he suspected,
only a fraction of the non-haemolytic (a- or g-) streptococci
outside the ‘lactic’ and ‘enterococci’ divisions being
represented. The ‘viridans’ division was made up of species
largely from the mouths and intestines of man and animals
and included Strep. salivarius, Strep. equinus, Strep. bovis,
‘varieties of Strep. bovis’ and Strep. thermophilus. Streptococci
from dairy sources comprised the ‘lactic’ division and
included Strep. lactis and Strep. cremoris. The fourth division
of Sherman termed ‘enterococci’ was made up of streptococci
of faecal origin and included Strep. faecalis, Strep. liquefaciens,
Strep. zymogenes and Strep. durans. Sherman noted that the
streptococci within the ‘enterococci’ division were markedly
different from the other species due to a combination of low
minimum and high maximum growth temperatures, greater
tolerance to both salt and alkali, high thermal death point,
resistance to methylene blue and greater reducing ability.
These observations anticipated by almost 50 years the event-
ual division of the genus Streptococcus along similar lines
into Streptococcus sensu stricto, Enterococcus and Lactococcus
(Schleifer and Kilpper-Bälz 1984; Schleifer et al. 1985).
The early success of the Lancefield grouping system and
its subsequent wider application within the streptococci led
eventually to the realization that, in some instances, organ-
isms that were physiologically heterogeneous could possess
a common group antigen, a situation which was to cause
considerable confusion in streptococcal taxonomy (Jones
1978). This difficulty was eventually overcome through the
application of alternative approaches to the problem by sev-
eral workers, marking a major transition in the nature of
studies undertaken on the streptococci. These new

approaches included cell wall composition studies, the com-
parison of strain collections by numerical taxonomy, meta-
bolic studies, DNA base composition determinations, base
sequence homology (DNA–DNA hybridization) and DNA
transformation. In the series of reports by Colman and Wil-
liams during this period (for a review of their studies see
Colman and Williams 1972) considerable progress was made
on the classification of the streptococci, in particular the
viridans group, which, until then, had remained problematic.
Indeed, the early difficulties encountered in classifying and
identifying the viridans streptococci, particularly those from
the oral cavity, had led many workers to refer to these simply
as ‘Streptococcus viridans’ with the result that this so-called
‘species’ was ill-defined, being biochemically and sero-
logically diverse. Using cell wall sugar analysis, numerical
taxonomy and DNA transformation, Colman and Williams
were able to recognize several species of viridans streptococci
that included Strep. mutans, Strep. sanguis, Strep. mitior, Strep.
salivarius, Strep. milleri and Strep. pneumoniae. Although some
of these species were not validly published and have sub-
sequently been re-classified, the proposals did introduce
order into a previously confused area and allowed working
identification schemes to be developed (Hardie and Bowden
1976; Jones 1978).
In the 8th edition of Bergey’s Manual of Determinative
Bacteriology (Deibel and Seeley 1974) the genus Streptococcus
was divided into four groups (I–IV) containing 21 named
species. Although these authors omitted Sherman’s original
designations ‘pyogenic’, ‘viridans’, ‘lactic’ and ‘enterococcus’
because some of the newly recognized species cut across these
divisions, nevertheless growth and tolerance tests, haemolytic
reaction and Lancefield grouping, supported by biochemical
reactions, were retained as major criteria in the classification
scheme and species groups formed therein. Several species
incertae sedis also described by these authors were listed prin-
cipally according to possession of a Lancefield group antigen
and, where possible, serotype, thus underlining the influence
that serological approaches still exerted in streptococcal
classification at this time.
Despite the considerable volume of literature accumulated
on the streptococci a classification reflecting the natural
relationships of the species was still required at the time that
Jones (1978) wrote her review of the genus. In this she
included ‘. . . the 21 named species in Deibel and Seeley
(1974), streptococci of serological groups T, U and V, the
group of oral streptococci referred to as Strep. mutans and in
addition the aerotolerant and the strictly anaerobic species of
Holdeman and Moore (1974) and Barnes et al. (1977)’ (the
anaerobic species comprised Strep. intermedius, Strep. con-
stellatus, Strep. morbillorum, Strep. hansenii and Strep. pleo-
morphus). For convenience Jones proposed purely artificial
divisions designated ‘pyogenic’, ‘pneumococci’, ‘oral’, ‘fae-
cal’, ‘lactic’, ‘anaerobic’ and ‘other streptococci’ (Table 1).
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
O VE RV I EW OF S TR EP T OC OC C US AN D EN TE R OC OC C US 3S
Twenty-seven streptococcal species were listed in the
Approved List of Bacterial Names (Skerman et al. 1980),
representing those species considered to be adequately
described and for which a type, neotype or reference strain
was available. These included: 17 of the named species in
Deibel and Seeley (1974) (Strep. equisimilis and Strep. zoo-
epidemicus, Strep. dysgalactiae and Strep. avium were
excluded), three of the five (then) genospecies of ‘mutans
streptococci’ (Strep. mutans, Strep. rattus and Strep. cricetus;
Coykendall 1977), the five species of the ‘anaerobic strep-
tococci’ listed by Jones (1978), Strep. iniae and Strep. raf-
finolactis.
2.3 Division of the genus Streptococcus and creation
of Streptococcus sensu stricto, Enterococcus
and Lactococcus
The introduction of DNA-based approaches during the 1960s
heralded an era when genotypic studies combined with
chemotaxonomic data allowed major developments to be
made in the classification of bacteria in general, and of Gram-
positive cocci in particular. DNA–DNA base pairing experi-
ments enabled genetic relationships within and between small
groups of species or within single species to be measured
while DNA–ribosomal (r)RNA homology studies and com-
parative oligonucleotide cataloguing of 16S rRNA provided
information concerning the genetic relationships of a wide
range of species of Streptococcus both intra- and inter-
generically (Hardie and Whiley 1992, 1994, 1995). The mid-
1980s marked a transition in streptococcal classification dur-
ing which several major studies were reported that, together,
can now be seen to reflect the shift away from traditional
approaches, including numerical taxonomy, towards chemo-
taxonomic techniques and, ultimately, nucleic acid hybrid-
ization and comparative gene sequence analyses. These
studies include, on the one hand, the large numerical taxo-
nomic study by Bridge and Sneath (1983) resulting in the
division of the genus into ‘pyogenic’, ‘parapyogenic’, ‘pneu-
mococci’, ‘thermophilic’, ‘viridans’, ‘paraviridans’, ‘entero-
coccal’ and ‘lactic’ species groups on biochemical and
physiological grounds (see Table 1) and, on the other, a series
of studies (reviewed by Schleifer and Kilpper-Bälz 1987) in
which data from cell wall and lipid chemical analyses, whole
genomic DNA–DNA base pairing, DNA–rRNA hybrid-
ization and 16S rRNA oligonucleotide cataloguing were to
result in a major revision of the genus. This transition is
also evident in the description of the genus Streptococcus
in Bergey’s Manual of Systematic Bacteriology (Hardie 1986)
which includes the traditional ‘pyogenic’, ‘oral’, ‘entero-
coccal’, ‘lactic acid’ and ‘anaerobic’ species but which also
carries an editorial note acknowledging publication of the
description of the genus Enterococcus at around the same time.
The studies briefly mentioned above finally revealed that
4S J .M . H A RD IE A ND R. A . W HI L EY

Table 1 Comparison of suggested groupings for streptococci and enterococci

–—–––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Sherman 1937 Jones 1978 Bridge and Sneath 1983 Bergey 1986 Schleifer and Kilpper-Bälz 1987
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
—
Pyogenic Pyogenic Pyogenic Pyogenic Pyogenic
Parapyogenic

Pneumococci Pneumococcal Strep. oralis group

(including ‘Strep. milleri’)
Viridans Oral Viridans Oral Strep. mutans group
Paraviridans

Other streptococci Thermophilic Other streptococci Other streptococci

Anaerobic streptococci Anaerobic Not streptococci

Enterococcus Faecal Enterococcal Enterococci Enterococcus

(separate genus)

Lactic Lactic Lactic Lactic acid Lactococcus

cocci (separate genus)
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
—

the streptococci consisted of three genetically distinct groups
at the generic level. The first, Streptococcus sensu stricto,
contained the majority of species and included the pyogenic,
‘mutans-like’, ‘milleri-like’ and viridans streptococci. The
second group, formed by members of the Lancefield group
D streptococci, conformed to the ‘enterococci’ division of
Sherman (1937) and were subsequently transferred to a new
genus Enterococcus (Schleifer and Kilpper-Bälz 1984). The
third group included the lactic streptococci which were also
transferred to a new genus, Lactococcus (Schleifer et al. 1985)
(Table 1).
2.4 Phenotypic characteristics of Streptococcus
(sensu stricto)
Cells are Gram-positive cocci or short rods occurring in
pairs or in chains. Species are non-motile and non-sporing.
Streptococci are facultatively anaerobic (some require CO2)
chemo-organotrophs with complex nutritional requirements
and a fermentative metabolism resulting in L(¦) lactic acid as
the major product of glucose fermentation. They are catalase
negative. Several peptidoglycan types are found within the
genus, which include Lys–Ala1–2, Lys–Ala1–3, Lys–Ala2–3,
Lys–Ala2(Ser), Lys–Thr–Ala, Lys–Thr–Gly, Lys–Thr–
Ala(Ser) and Lys-direct. The long-chain fatty acids of this
genus are made up of predominantly straight-chain or mono-
unsaturated types. Pyrrolidonylarylamidase is not produced
by the majority of species of Streptococcus. The guanine plus
cytosine content is from ¼33% to 46% although the majority
of reported values lie in the range of 35–43mol%.
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
2.5 Phenotypic characteristics of Enterococcus
Cells are Gram-positive, ovoid and non-sporing, occurring
either singly, in pairs or as short chains. Some species are
motile. Enterococci are facultatively anaerobic chemo-organ-
otrophs with complex nutritional requirements and a fer-
mentative metabolism resulting in L(¦) lactic acid as the
major product of glucose fermentation. They are benzidine
and catalase negative with some strains producing pseudo-
catalase. The majority of enterococcal species are able to grow
at 10°C, at 45°C and in the presence of 6·5% NaCl but with
some species unable to do so. Most species are characterized
by the possession of the Lancefield group D antigen with the
notable exceptions of Ent. cecorum, Ent. columbae and Ent.
dispar. The cell walls of the enterococci contain the lysine-D-
asparagine peptidoglycan type (with the exception of Ent.
faecalis) and the membrane-derived long-chain fatty acids of
this genus are predominantly straight-chain or mono-unsatu-
rated types, although some have cyclo-propane ring acids.
Pyrrolidonylarylamidase is produced by most species. The
guanine plus cytosine content is ¼38–45mol%.
2.6 Phylogeny of Streptococcus and Enterococcus
The results of the extensive 16S rRNA gene sequence analy-
ses carried out in recent years among streptococci, enterococci
and other Gram-positive bacteria have included the descrip-
tion of several new lactic acid bacterial genera and the deter-
mination of their phylogenetic positions. All belong in the low
G ¦ C (Clostridium–Bacillus) branch of the Gram-positive

eubacteria and besides Streptococcus and Enterococcus include
Lactococcus, Aerococcus, Carnobacterium, Globicatella, Lacto-
bacillus, Leuconostoc, Pediococcus, Tetragenococcus, Vagococcus,
Dolosigranulum, Alloiococcus, Atopobium, Gemella and Helco-
coccus (Schleifer and Ludwig 1995). In contrast with the close
historical link between them, Streptococcus and Enterococcus
are geneologically well separated from each other relative to
these other genera, with Streptococcus more closely related
to Lactococcus and with Enterococcus closer to Aerococcus,
Vagococcus, Dolosigranulum, Carnobacterium and Abiotrophia.
The differential characteristics and clinical importance of
these genera have been reviewed recently (Hardie and Whiley
1994, 1995; Facklam and Elliott 1995).
3. CURRENT CLASSIFICATION OF
STREPTOCOCCUS
3.1 Species and species groups
There are currently ¼40 species within this genus of which
the majority have been shown to form six species groups by
16S rDNA comparative sequence analysis (Kawamura et al.
1995a). These are the ‘pyogenic’, ‘mitis’, ‘salivarius’, ‘bovis’,
‘anginosus’ and ‘mutans’ groups. Table 2 lists those species
presently included in the genus arranged according to their
species groups. Two species, Strep. suis and Strep. acido-
minimus, have failed to cluster with any other streptococcal
species so far tested although they do exhibit a loose mutual
association by this method on the basis of rRNA sequence
analysis. The main 16S rDNA-based study of the genus was
by Bentley et al. (1991) and the database has recently been
extended by the inclusion within the ‘mitis species group’ of
both Strep. mitis and Strep. gordonii and by the determination
of the phylogenetic positions of the pyridoxal-dependent
(nutritionally variant, NVS) streptococci, Strep. adjacens and
Strep. defectivus (Kawamura et al. 1995a,b). The latter two
species have subsequently been transferred to a new genus
Abiotrophia as Abiotrophia adiacens and Abiotrophia defectiva,
respectively (Kawamara et al. 1995b). The position of several
newly recognized species, including Strep. caprinus from the
rumen of feral goats (Brooker et al. 1994), Strep. gallactolyticus
from the alimentary canal of various animals and from human
cases of endocarditis and septicaemia (Osawa et al. 1995),
Strep. difficile, a bacterium causing meningoencephalitis in
farmed fish (Eldar et al. 1994), and Strep. phocae, isolated
from seals with pneumonia (Skaar et al. 1994), along with the
well established species Strep. ferus, Strep. crista and Strep.
intestinalis, remain to be determined by 16S rDNA sequencing.
In addition, the transfer of the ‘anaerobic streptococcus’,
Strep. hansenii, to the genus Ruminococcus as Ruminococcus
hansenii (Ezaki et al. 1994) has been called into question by
Willems and Collins (1995) who have suggested that R.
(Strep.) hansenii is remotely related to the Ruminococcus-type
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
O VE RV I EW OF S TR EP T OC OC C US AN D EN TE R OC OC C US 5S
species R. flavefaciens and exhibited a far closer association
with Clostridium cluster XIVa (Collins et al. 1994) along
with several Clostridium, Eubacterium and Coprococcus species.
However, these authors have pointed out that the amount of
work necessary in order to clarify the taxonomy of Clostridium
cluster XIVa is such that the name Strep. hansenii should
be retained for the time being. Therefore Strep. hansenii is
currently listed in the genus Streptococcus but will almost
certainly be transferred elsewhere in the future. Similarly,
another of the anaerobic species, Strep. pleomorphus, has been
shown to be only distantly related to the streptococci by
16S rDNA sequence comparison and waits to be validly
transferred (Ludwig et al. 1988).
One other recent, short-lived, species designation, Strep.
shiloi, was given to a coccus causing septicaemic infection
(meningoencephalitis) in fish. However, this name has since
been shown to be a junior synonym of Strep. iniae (Eldar et
al. 1995). Streptococcus iniae is now recognized as a major
worldwide pathogen of fish and of captive freshwater dolphins.
The species of Streptococcus that are currently of uncertain
species grouping or genus are listed in Table 3.
3.2 Identification of Streptococcus species
Although no comprehensive identification scheme currently
exists for the streptococci, the use of chromogenic or fluoro-
genic substrate tests for detecting preformed enzymes com-
bined with more traditional biochemical tests such as
carbohydrate fermentation, aesculin and arginine hydrolysis
and acetoin production, has been particularly useful,
especially with the viridans species (Kilian et al. 1989; Beigh-
ton et al. 1991; Kikuchi et al. 1995). The standardization of
these differential tests as well as the attempt at a com-
prehensive scheme for the identification of all streptococcal
species has been through the development of commercial
identification test kits (Freney et al. 1992). However, there is
still some improvement required before a completely satis-
factory scheme is achieved.
The development of a comprehensive set of species gene
probes for identification is still awaited. Approaches centred
on the small (16)rRNA subunit hold most promise with
sequence data now available on most, but not all, species
(Bentley et al. 1991; Kawamura et al. 1995a) and some species-
specific oligonucleotide probes have been described (Bentley
et al. 1993; Bentley and Leigh 1995).
4. ECOLOGY AND DISEASE ASSOCIATIONS
O F STREPTOCOCCUS
4.1 Ecology
The streptococci are characteristically found on the mucous
membranes of the mouth, upper respiratory tract, alimentary
6S J .M . H A RD IE A ND R. A . W HI L EY

Table 2 Currently recognized —

–––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
species groups in genus Streptococcus Group* Species included Alternative designation†
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
Pyogenic Strep. pyogenes Pyogenic
Strep. agalactiae
Strep. canis
Strep. dysgalactiae
Strep. equi
Strep. hyointestinalis
Strep. iniae
Strep. parauberis
Strep. porcinus
Strep. uberis

Mitis Strep. gordonii Oral

Strep. mitis (Strep. sanguis/oralis group)
Strep. oralis (also includes Strep. crista)
Strep. parasanguis
Strep. pneumoniae
Strep. sanguis

Salivarius Strep. salivarius Oral

Strep. thermophilus (Strep. salivarius group)
Strep. vestibularis

Anginosus Strep. anginosus Oral

Strep. constellatus (‘Strep. milleri’ group)
Strep. intermedius

Mutans Strep. mutans Oral

Strep. cricetus (Strep. mutans group)
Strep. downei (also includes Strep. ferus)
Strep. macacae
Strep. rattus
Strep. sobrinus

Bovis Strep. bovis Other streptococci

Strep. alactolyticus
Strep. equinus
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
* Kawarmura et al. (1995a).
† Hardie and Whiley (1995).

tract and genitourinary tract, as well as on the skin, of man
and other animals (Skinner and Quesnel 1978). Some strepto-
coccal species are particularly associated with humans, whilst
others have only been reported from other animals, although
information on the distribution of streptococci throughout
the animal kingdom is limited (Devriese 1991; Hardie and
Whiley 1994).
4.2 Human diseases
Many streptococci are known to cause human disease, some
species being highly virulent and responsible for major
diseases. Streptococcus pyogenes, Strep. agalactiae and Strep.
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
pneumoniae are particularly notable as causes of serious acute
infections in man, but several other species are frequently
involved in infective endocarditis, abscesses and other con-
ditions (Hardie and Whiley 1995). Some of the less highly
virulent species, such as those in the Strep. mitis group, may
become more aggressively pathogenic in immunologically
compromised individuals, giving rise to septicaemia or the
adult respiratory distress syndrome (ARDS) (Hardie and
Whiley 1994). The Strep. anginosus group streptococci (also
known as ‘Strep. milleri’ group) are commonly associated with
abscesses in various parts of the body, including the mouth,
brain, liver and various other organs (Gossling 1988; Whiley
et al. 1992). Species in the Strep. mutans group, especially

Table 3 Streptoccal species of uncertain grouping or changed
designation
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––
Species Comments
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––
Strep. acidominimus Ungrouped by 16S rRNA sequence
homology*
Strep. suis Ungrouped by 16S rRNA sequence
homology*
Strep. pleomorphus Ungrouped by 16S rRNA sequence
homology*
(Cl. innocuum-like)†
Strep. hansenii Clostridium Cluster XIVa‡
Strep. ferus Phylogenetic relationships not known
Strep. crista Phylogenetic relationships not known
Strep. intestinalis Phylogenetic relationships not known
Strep. caprinus Phylogenetic relationships not known
Strep. difficile Phylogenetic relationships not known
Strep. gallolyticus Phylogenetic relationships not known
Strep. phocae Phylogenetic relationships not known
Strep. adjacens Transferred to genus Abiotrophia§
Strep. defectivus Transferred to genus Abiotrophia§
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––
* Kawamura et al. (1995a).
† Ludwig et al. (1988).
‡ Willems and Collins (1995).
§ Kawamura et al. (1995b).
Strep. mutans and Strep. sobrinus, are implicated in the aeti-
ology of dental caries (Hamada and Slade 1980; Loesche
1986). Further information on streptococcal infections in
humans is given in the papers in this supplement by Cart-
wright and Efstratiou (pp. 52S–61S; 72S–79S).
One of the enigmas of streptococcal diseases in humans is
that many of the potentially pathogenic species can be found
as part of the resident microflora, either as a commensal or
as a transient colonizer, without causing apparent ill-effects.
In the case of Strep. pyogenes (Lancefield group A) infections,
the initial acute infection may be followed by subsequent
complications such as rheumatic fever or glomerulonephritis,
both of which occur as a result of harmful immunological
responses to the original infection (Brooks et al. 1995). Con-
siderable progress has been made in understanding the patho-
genesis of disease caused by Strep. pyogenes (Kehoe 1991) and
Strep. pneumoniae (Boulnois 1992), and a number of their
virulence determinants have been characterized by molecular
methods (see Mitchell et al., pp. 62S–71S).
Until comparatively recently, antibiotic resistance amongst
streptococci was rarely observed and selection of anti-
microbial agents for treatment was not a major problem.
The increasing number of reported pneumococcal isolates
reported in the USA and elsewhere that are resistant to
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
O VE RV I EW OF S TR EP T OC OC C US AN D EN TE R OC OC C US 7S
penicillin is a particularly worrying trend (Spika et al. 1991;
see also Dowson et al., pp. 42S–51S).
4.3 Animal diseases
Streptococci of various species are known to be associated
with infections of cattle, pigs, horses, sheep, birds, aquatic
mammals and fish (Wilson and Salt 1978). In most instances
the streptococcal species involved are different from those
responsible for human disease although in a few cases, includ-
ing Strep. agalactiae, Strep. bovis and Strep. dysgalactiae, the
pathogens do cause both animal and human infections. Bovine
mastitis is one condition of considerable economic sig-
nificance to dairy farmers which can be caused by several
streptococcal species, including Strep. canis, Strep. agalactiae,
Strep. dysgalactiae, Strep. parauberis and Strep. uberis. Pigs are
particularly susceptible to streptococcal infections which may
present as arthritis, meningoencephalitis, cervical lymph-
adenitis, endocarditis, abscesses, pneumonia or septicaemia.
Such infections are commonly due to Strep. porcinus or Strep.
suis (Devriese 1991; see also Chanter, pp. 100S–109S).
5. CURRENT CLASSIFICATION OF
ENTEROCOCCUS
5.1 Species and species groups
Since the transfer of Strep. faecalis and Strep. faecium to the
revived genus Enterococcus (Schleifer and Kilpper-Bälz 1984),
the total number of species presently included here is 17.
The status of Ent. seriolicida was in doubt for some time
(Devriese and Pot 1995) but this species has now been shown
to be the same as Lactococcus garvieae which is a senior
subjective synonym (Teixeira et al. 1996). The taxonomic
status within the genus of another species, Ent. flavescens, is
also uncertain in that strains of this species display a very
close relationship to Ent. casseliflavus (Devriese and Pot 1995).
A further reduction in the number of species within the genus
was caused by the transfer of Ent. solitarius to the genus
Tetragenococcus (Collins et al. 1990).
16S rDNA comparative sequence analysis has revealed that
most of the species within Enterococcus fall into one of four
species groups (Williams et al. 1991). These are referred to
as the Ent. faecium-, Ent. avium-, Ent. gallinarum- and Ent.
cecorum- species groups by Devriese and Pot (1995) and are
listed in Table 4. The four species which remain unlinked
to any species group are Ent. faecalis, Ent. sulfureus, Ent.
saccharolyticus and Ent. dispar.
5.2 Identification of Enterococcus species
As with the streptococci, species identification using stan-
dardized commercial biochemical test identification kits that
8S J .M . H A RD IE A ND R. A . W HI L EY

Table 4 Currently recognized species groups in genus commonly and in higher numbers than Ent. faecium in most
Enterococcus studies (Murray 1990). Although they are less commonly
—
––––––––––––––––––––––––––––––––––––––––––––––––––––– found at other body sites, enterococci can also be recovered
Group* Species included from the vagina and the oral cavity. Enterococcal carriage
—
–––––––––––––––––––––––––––––––––––––––––––––––––––––
rates in the mouth appear to vary between different study
Ent. faecalis Ent. faecalis
groups, and may be increased in hospitalized patients and
Ent. faecium Ent. durans those on long-term haemodialysis (Campbell et al. 1983;
Ent. faecium Smyth et al. 1987).
Ent. hirae The involvement of enterococci in human clinical infec-
Ent. mundtii tions has been reviewed very thoroughly by Murray (1990),
who points out that their pathogenic potential was first recog-
Ent. avium Ent. avium nized around the turn of the century, the earlier studies being
Ent. pseudoavium discussed by Sherman (1937). The most common infections
Ent. malodoratus are those involving the urinary tract, in which enterococci
Ent. raffinosus are implicated in about 10% of cases (Felmingham et al.
1992), and up to 16% of nosocomial urinary tract infections
Ent. gallinarium Ent. gallinarum
(Schaberg et al. 1991).
Ent. casseliflavus
Ent. flavescens (similar to Ent. Enterococci are often found in intra-abdominal and pelvic
casseliflavus) wound infections, but since these are usually polymicrobial
it is difficult to assess their role in such conditions (Nicols and
Ent. cecorum Ent. cecorum Muzik 1992). Isolates of enterococci from wound infections
Ent. columbae appear to be on the increase, and this trend is associated
with the problem of antibiotic resistance amongst these cocci
Miscellaneous species Ent. saccharolyticus (Moellering 1992).
Ent. sulfureus Enterococci, especially Ent. faecalis, are responsible for
Ent. dispar a significant proportion of cases of bacterial endocarditis,
accounting for 5–20% of reported series (Megran 1992; Wat-
Altered taxonomic status Ent. solitarius (Tetragenococcus
solitarius)
anakunakorn and Burkert 1993). Bacteraemias due to entero-
Ent. seriolicida (Lactococcus species) cocci are more common than infective endocarditis, often
—
––––––––––––––––––––––––––––––––––––––––––––––––––––– occurring in elderly patients with serious underlying medical
* Devriese and Pot (1995) ; Williams et al. (1991). conditions or in immunocompromised individuals who have
undergone antimicrobial therapy (Awada et al. 1992; Gran-
inger and Ragette 1992). The source of infection in entero-
include a combination of rapid preformed enzyme detection coccal bacteraemia not associated with endocarditis is often
tests with more traditional biochemical tests have shown the urinary tract (Maki and Agger 1988).
considerable promise (Freney et al. 1992). The delineation of Enterococci are also known to cause neonatal, central nervous
species and species groups within the enterococci on the basis system and respiratory tract infection on occasions, although
of 16S rRNA gene sequences (Williams et al. 1991) indicates these are comparatively rare (Murray 1990). Of particular con-
that a DNA probe approach may be feasible. cern is the increasing prevalence of enterococci in hospital-
acquired infections and their increasing levels of resistance to
antimicrobial agents (Murray 1990; Facklam and Sahm 1995).
6. ECOLOGY AND DISEASE ASSOCIATIONS
Considerable attention is now being focused on the putative
O F ENTEROCOCCUS
virulence determinants of enterococci, which include a cytolysin,
Enterococci are typically found in the intestinal tract and aggregation substance, pheromones, lipoteichoic acid, a protease,
faeces of man and other animals (Murray 1990; Devriese and hyaluronidase and a bacteriocin, 45-48 (Jett et al. 1994).
Pot 1995). Some species have also been isolated from soil, As well as being well adapted for survival in the body,
food, water and plants, and their ability to grow and survive enterococci have an ability to exchange extrachromosomal
under a wide range of environmental conditions, including elements which encode virulence determinants or antibiotic
extremes of temperature and salt concentrations, probably resistance genes, by several genetic mechanisms (Schaberg
accounts for the almost ubiquitous distribution of the genus and Zervos 1986; Clewell 1990). It is clear that the increasing
(Facklam and Sahm 1995). difficulty of treating patients with resistant strains of entero-
In humans, enterococci can be isolated from almost 100% cocci necessitates the continuing study of these important
of faecal samples, with Ent. faecalis being reported more bacteria (Murray 1990; Jett et al. 1994).
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S

Further information about enterococcal infections in
humans is given in the paper by Morrison et al. in this
supplement, and on animal infections by Chanter (pp. 89S–
99S; 100S–109S).
7. CONCLUSIONS
After more than 100 years of investigation since the first
published descriptions of streptococci, it is now clear that
the chain-forming, catalase-negative, Gram-positive cocci fall
into several distinct genera which include Streptococcus and
Enterococcus. Both of these genera can be subdivided into
species groups on the basis of 16S rRNA sequence analyses,
supported by other taxonomic data.
Identification of individual species of streptococci and
enterococci by conventional phenotypic tests is possible in
most cases, although difficulties do occur within some species
groups. The development of species-specific oligonucleotide
probes, based on 16S rRNA sequence data, and the use of
PCR-based techniques, would seem to offer the best prospect
of improved identification methods for the future.
Species of Streptococcus and Enterococcus are widely dis-
tributed, most of them being found on mucous membranes
of man and other animals. Many of these species are associ-
ated with human infections, either in the form of acute con-
ditions caused by species such as Strep. pyogenes, Strep.
pneumoniae and Strep. agalactiae, or as opportunistic patho-
gens in infective endocarditis, urinary tract infections and
in many other situations. A number of important animal
infections are also caused by streptococci, but the role of
enterococci as pathogens in animals is less clear.
Interest is currently focused on the molecular epidemiology
and virulence determinants of some of the major disease-
causing species of Streptococcus and Enterococcus, and on the
worrying emergence of antibiotic resistance within these
genera. As mentioned earlier, several aspects of these issues
are considered in greater detail by other contributors to this
symposium.
8. REFERENCES
Andrewes, F.W. and Horder, J. (1906) A study of the streptococci
pathogenic for man. Lancet 2, 708–713.
Awada, A., van der Auwera, P., Meunier, F., Daneau, D. and
Klastersky, J. (1992) Streptococcal and enterococcal bacteraemia
in patients with cancer. Clinical Infectious Diseases 13, 33–48.
Barnes, E.M., Impey, C.S., Stevens, B.J.H. and Peel, J.L. (1977)
Streptococcus pleomorphus sp. nov: an anaerobic streptococcus iso-
lated mainly from the caeca of birds. Journal of General Micro-
biology 102, 45–53.
Beighton, D., Hardie, J.M. and Whiley, R.A. (1991) A scheme
for the identification of viridans streptococci. Journal of Medical
Microbiology 35, 367–372.
Bentley, R.W. and Leigh, J.A. (1995) Development of PCR-based
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
O VE RV I EW OF S TR EP T OC OC C US AN D EN TE R OC OC C US 9S
hybridization protocol for identification of streptococcal species.
Journal of Clinical Microbiology 33, 1296–1301.
Bentley, R.W., Leigh, J.A. and Collins, M.D. (1991) Intrageneric
structure of Streptococcus based on comparative analysis of small-
subunit rRNA sequences. International Journal of Systematic Bac-
teriology 41, 487–494.
Bentley, R.W., Leigh, J.A. and Collins, M.D. (1993) Development
and use of species-specific oligonucleotide probes for dif-
ferentiation of Streptococcus uberis and Streptococcus parauberis.
Journal of Clinical Microbiology 31, 57–60.
Billroth, T. (1874) Untersuchungen uber die Vegetationsformen von
Coccobacteria Septica. Berlin: G. Reimer.
Boulnois, G.J. (1992) Pneumococcal proteins and the pathogenesis
of disease caused by Streptococcus pneumoniae. Journal of General
Microbiology 138, 249–259.
Bridge, P.G. and Sneath, P.H.A. (1983) Numerical taxonomy of
Streptococcus. Journal of General Microbiology 129, 565–597.
Brooker, J.D., O’Donovan, L.A., Skene, I., Clarke, K., Blackall, L.
and Muslera, P. (1994) Streptococcus caprinus sp. nov., a tannin-
resistant ruminal bacterium from feral goats. Letters in Applied
Microbiology 18, 313–316.
Brooks, G.F., Butel, J.S. and Ornston, L.N. (1995) Jawetz, Melnick
and Adelberg’s Medical Microbiology, 20th edn. East Norwalk, CT:
Appleton and Lange.
Campbell, J., McGowan, D.A. and MacFarlane, T.W. (1983) The
prevalance of enterococci in the dental plaque of chronic hospital
patients. British Journal of Oral Surgery 21, 171–174.
Clewell, D.B. (1990) Movable genetic elements and antibiotic resist-
ance in enterococci. European Journal of Clinical Microbiology and
Infectious Disease 9, 90–102.
Collins, M.D., Williams, A.M. and Wallbanks, S. (1990) The phy-
logeny of Aerococcus and Pediococcus as determined by 16S rRNA
sequence analysis: description of Tetragenococcus gen. nov. FEMS
Microbiology Letters 70, 255–262.
Collins, M.D., Lawson, P.L., Willems, A. et al. (1994) The phylo-
geny of the genus Clostridium: proposal of five new genera and
eleven new species combinations. International Journal of
Systematic Bacteriology 44, 812–826.
Colman, G. (1990) Streptococcus and Lactobacillus. In Topley and
Wilson’s Principles of Bacteriology, Virology and Immunity, Vol. 2:
Systematic Bacteriology, 8th edn, ed. Parker, M.T. and Collier,
L.H. pp. 119–159. London, Melbourne Auckland: Edward
Arnold (a division of Hodder and Stoughton).
Colman, G. and Williams, R.E.O. (1972) Taxonomy of some human
viridans streptococci. In Streptococci and Streptococcal Diseases ed.
Wannamaker, L.W. and Matsen, J.M. pp. 281–299. New York
and London: Academic Press.
Coykendall, A.L. (1977) Proposal to elevate the subspecies of Strep-
tococcus mutans to species status, based on their molecular com-
position. International Journal of Systematic Bacteriology 27, 26–
30.
Deibel, R.H. and Seeley, H.W. (1974) Streptococcaceae fam. nov.
In Bergey’s Manual of Determinative Bacteriology, 8th edn, ed
Buchanan, R.E. and Gibbons, N.E. pp. 490–509. Baltimore: Wil-
liams and Wilkins.
Devriese, L.A. (1991) Streptococcal ecovars associated with dif-
ferent animal species: epidemiological significance of serogroups
and biotypes. Journal of Applied Bacteriology 71, 478–483.
10S J .M . H A RD IE A ND R. A . W HI L EY
Devriese, L.A. and Pot, B. (1995) The genus Enterococcus. In The
Genera of Lactic Acid Bacteria ed. Wood, B.J.B. and Holzapfel,
W.H. Vol. 2, pp. 327–367. Blackie Academic and Professional.
Eldar, A., Bejerano, Y. and Bercovier, H. (1994) Streptococcus shiloi
and Streptococcus difficile: two new streptococcal species causing
a meningoencephalitis in fish. Current Microbiology 28, 139–143.
Eldar, A., Frelier, P.F., Assenta, L., Lawhon, S. and Bercovier,
H. (1995) Streptococcus shiloi, the name for an agent causing
septicaemic infection in fish, is a junior synonym of Streptococcus
iniae. International Journal of Systematic Bacteriology 45, 840–842.
Ezaki, T., Li, N., Hashimoto, Y., Miura, H. and Yamamoto, H.
(1994) 16S ribosomal DNA sequences of anaerobic cocci and
proposal of Ruminococcus hansenii com. nov. and Ruminococcus
productus comb. nov. International Journal of Systematic Bac-
teriology 44, 130–136.
Facklam, R. and Elliott, J.A. (1995) Identification, classification
and clinical relevance of catalase-negative, Gram-positive cocci,
excluding the streptococci and enterococci. Clinical Microbiology
Reviews 8, 479–495.
Facklam, R.R. and Sahm, D.F. (1995) Enterococcus. In Manual of
Clinical Microbiology ed. Murray, P.R., Baron, E.J., Pfaller, M.A.,
Tenover, F.C. and Yolken, R.H. pp. 308–314. Washington, DC:
ASM Press.
Felmingham, D., Wilson, A.P.R., Quintanna, A.I. and Grüneberg,
R.N. (1992) Enterococcus species in urinary tract infection. Clinical
Infectious Diseases 15, 295–300.
Freney, J., Bland, S., Etienne, J., Desmonceaux, M., Boeufgras,
J.M. and Fleurette, J. (1992) Description and evaluation of the
semiautomated 4-hour Rapid ID 32 Strep method for identi-
fication of streptococci and members of related genera. Journal of
Clinical Microbiology 30, 2657–2661.
Gossling, J. (1988) Occurrence and pathogenicity of the Streptococcus
milleri group. Reviews of Infectious Diseases 10, 257–285.
Graninger, W. and Ragette, R. (1992) Nosocomial bacteremia due
to Enterococcus faecalis without endocarditis. Clinical Infectious
Diseases 15, 49–57.
Hamada, S. and Slade, H.D. (1980) Biology, immunology and cario-
genicity of Streptococcus mutans. Microbiology Reviews 44, 331–
384.
Hardie, J.M. (1986) Genus Streptococcus. In Bergey’s Manual of
Determinative Bacteriology ed. Sneath, P.H.A., Mair, N.S. and
Sharpe, M.E. Vol. 2, pp. 1043–1071. Baltimore: Williams and
Wilkins.
Hardie, J.M. and Bowden, G.H. (1976) Physiological classification
of oral viridans streptococci. Journal of Dental Research 55 (Special
issue A), A166–A176.
Hardie, J.M. and Whiley, R.A. (1992) The genus Streptococcus-oral.
In The Prokaryotes, 2nd edn, ed. Balows, A., Trüper, H.G.,
Dworkin, M., Harder, W. and Schleifer, K.H. Vol. II, pp. 1421–
1449. New York: Springer-Verlag.
Hardie, J.M. and Whiley, R.A. (1994) Recent developments in
streptococcal taxonomy: their relation to infections. Reviews in
Medical Microbiology 5, 151–162.
Hardie, J.M. and Whiley, R.A. (1995) The genus Streptococcus. In
The Genera of Lactic Acid Bacteria ed. Wood, B.J.B. and Holz-
apfel, W.H. Vol. 2, pp. 55–124. Blackie Academic and
Professional.
Holdeman, L.V. and Moore, W.E.C. (1974) New genus, Copro-
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
coccus, twelve new species and emended description of four pre-
viously described species of bacteria from human faeces.
International Journal of Systematic Bacteriology 24, 260–277.
Jett, B.D., Huycke, M.M. and Gilmore, M.S. (1994) Virulence of
enterococci. Clinical Microbiology Reviews 7, 462–478.
Jones, D. (1978) Composition and differentiation of the genus Strep-
tococcus. In Streptococci ed. Skinner, F.A. and Quesnel, L.B. pp.
1–49. Society for Applied Bacteriology Symposium Series No. 7.
London, New York, San Francisco: Academic Press.
Kawamura, Y., Hou, X., Sultana, F., Miura, H. and Ezaki, T.
(1995a) Determination of 16S rRNA sequences of Streptococcus
mitis and Streptococcus gordonii and phylogenetic relationships
among members of the genus Streptococcus. International Journal
of Systematic Bacteriology 45, 406–408.
Kawamura, Y., Hou, X.-G., Sultana, F., Liu, S., Yamamoto, H.
and Ezaki, T. (1995b) Transfer of Streptococcus adjacens and
Streptococcus defectivus to Abiotrophia gen. nov. as Abiotrophia
adiacens comb. nov. and Abiotrophia defectiva comb. nov., respec-
tively. International Journal of Systematic Bacteriology 45, 798–
803.
Kehoe, M.A. (1991) New aspects of Streptococcus pyogenes patho-
genicity. Reviews in Medical Microbiology 2, 147–152.
Kikuchi, K., Enari, T., Tosuka, K.-I. and Shimizu, K. (1995)
Comparison of phenotypic characteristics, DNA-DNA hybrid-
isation results, and results with a commercial rapid biochemical
and enzymatic reaction system for identification of viridans group
streptococci. Journal of Clinical Microbiology 33, 1215–1222.
Kilian, M., Mikkelsen, L. and Henrichsen, J. (1989) Taxonomic
study of viridans streptococci: description of Streptococcus gordonii
sp. nov. and emended descriptions of Streptococcus sanguis (White
and Niven 1946), Streptococcus oralis (Bridge and Sneath 1982)
and Streptococcus mitis (Andrewes and Horder 1906). International
Journal of Systematic Bacteriology 39, 471–484.
Lancefield, R.C. (1933) A serological differentiation of human and
other groups of hemolytic streptococci. Journal of Experimental
Medicine 57, 571–595.
Loesche, W.J. (1986) Role of Streptococcus mutans in human dental
decay. Microbiological Reviews 50, 353–380.
Ludwig, W., Weizenegger, M., Kilpper-Bälz, R. and Schleifer,
K.H. (1988) Phylogenetic relationships of anaerobic streptococci.
International Journal of Systematic Bacteriology 38, 15–18.
Maki, D.G. and Agger, W.A. (1988) Enterococcal bacteremia: clini-
cal features, the risk of endocarditis, and management. Medicine
67, 248–269.
Megran, D.W. (1992) Enterococcal endocarditis. Clinical Infectious
Diseases 15, 63–71.
Moellering, R.C. (1992) Emergency of Enterococcus as a significant
pathogen. Reviews in Infectious Diseases 14, 1173–1178.
Murray, B.E. (1990) The life and times of the Enterococcus. Clinical
Microbiology Reviews 3, 46–65.
Nicols, R.L. and Muzik, A.C. (1992) Enterococcal infections in
surgical patients: the mystery continues. Clinical Infectious Dis-
eases 15, 72–76.
Osawa, R., Fujisawa, T. and Sly, L.I. (1995) Streptococcus gallolyticus
sp. nov.; gallate degrading organisms formerly assigned to Strep-
tococcus bovis. Systematic and Applied Microbiology 18, 74–78.
Rosenbach, F.J. (1884) Mikro-organismen bei den Wund-Infections-
Krankheiten des Menschen. Weisbaden: J.F. Bergman.
 O VE RV I EW OF S TR EP T OC OC C US AN D EN TE R OC OC C US 11S
Schaberg, D.R. and Zervos, M.J. (1986) Intergeneric and inter-
species gene exchange in gram-positive cocci. Antimicrobial Agents
and Chemotherapy 30, 817–822.
Schaberg, D.R., Culver, D.H. and Gaynes, R.P. (1991) Major trends
in the microbial etiology of nosocomial infection. American Jour-
nal of Medicine 91 (Suppl. 3B), 725–755.
Schleifer, K.H. and Kilpper-Bälz, R. (1984) Transfer of Strep-
tococcus faecalis and Streptococcus faecium to the genus Enterococcus
nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus
faecium comb. nov. International Journal of Systematic Bacteriology
34, 31–34.
Schleifer, K.H. and Kilpper-Bälz, R. (1987) Molecular and chemo-
taxonomic approaches to the classification of streptococci, entero-
cocci and lactococci: a review. Systematic and Applied Microbiology
10, 1–19.
Schleifer, K.H. and Ludwig, W. (1995) Phylogenetic relationships
of lactic acid bacteria. In The Genera of Lactic Acid Bacteria ed.
Wood, B.J.B. and Holzapfel, W.H. Vol. 2, pp. 7–18. Blackie
Academic and Professional.
Schleifer, K.H., Kraus, J., Dvorak, C., Kilpper-Bälz, R., Collins,
M.D. and Fischer, W. (1985) Transfer of Streptococcus lactis and
related streptococci to the genus Lactococcus gen. nov. Systematic
and Applied Microbiology 6, 183–195.
Sherman, J.M. (1937) The streptococci. Bacteriological Reviews 1,
3–97.
Skaar, I., Grustad, P., To njum, T., Holm, B. and Stenwig, H.
(1994) Streptococcus phocae sp. nov., a new species isolated from
clinical specimens from seals. International Journal of Systematic
Bacteriology 44, 646–650.
Skerman, V.B.D., McGowan, V. and Sneath, P.H.A. (1980)
Approved lists of bacterial names. International Journal of Sys-
tematic Bacteriology 30, 225–420.
Skinner, F.A. and Quesnel, L.B. (1978) Streptococci. London, New
York, San Francisco: Academic Press.
Smyth, C.J., Halpenny, M. and Ballagh, S.J. (1987) Carriage rates
of enterococci in the dental plaque of haemodialysis patients in
© 1997 The Society for Applied Bacteriology, Journal of Applied Microbiology Symposium Supplement 83, 1S–11S
View publication stats
Dublin. British Journal of Oral and Maxillofacial Surgery 25, 21–
33.
Spika, J.S., Facklam, R.R., Plikaytis, B.D. and Oxtoby, M.J. (1991)
Antimicrobial resistance of Streptococcus pneumoniae in the United
States, 1979–1987. The Pneumococcal Surveillance Working
Group. Journal of Infectious Diseases 163, 1273–1278.
Teixeira, L.M., Merquior, V.L.C., Da Conceicao, E. et al. (1996)
Phenotypic and genotypic characterization of atypical Lactococcus
garvieae strains isolated from water buffaloes with subclinical
mastitis and confirmation of L. garvieae as a senior subjective
synonym of Enterococcus seriolicida. International Journal of
Systematic Bacteriology 46, 664–668.
Thiercelin, E. and Jouhaud, L. (1903) Reproduction de l’en-
terocoque; taches centrales; granulations peripheriques et micro-
blasts. Comptes Rendus des Seances de la Societé de Biologie, Paris
55, 686–688.
Watanakunakorn, C. and Burkert, T. (1993) Infective endocarditis
at a large community teaching hospital, 1980–1990. Medicine 72,
90–102.
Whiley, R.A., Beighton, D., Winstanley, T.G., Fraser, H.Y. and
Hardie, J.M. (1992) Streptococcus intermedius, Streptococcus con-
stellatus, and Streptococcus anginosus (the Streptococcus milleri
group): association with different body sites and clinical infec-
tions. Journal of Clinical Microbiology 30, 243–244.
Willems, A. and Collins, M.D. (1995) Phylogenetic analysis of
Ruminococcus flavefaciens, the type species of the genus Rumi-
nococcus, does not support the reclassification of Streptococcus
hansenii and Peptostreptococcus productus as ruminococci. Inter-
national Journal of Systematic Bacteriology 45, 572–575.
Williams, A.M., Rodrigues, U.M. and Collins, M.D. (1991) Intra-
generic relationships of enterococci as determined by reverse
transcriptase sequencing of small-subunit rRNA. Research in
Microbiology 142, 67–74.
Wilson, C.D. and Salt, G.F.H. (1978) Streptococci in animal
disease. In Streptococci ed. Skinner, F.A. and Quesnel, L.B. pp.
143–156. Society for Applied Bacteriology Symposium Series
No. 7. London, New York, San Francisco: Academic Press.