Origin and Diversificationof Eukaryotes

MI66CH20-Katz ARI 21 June 2012 17:22
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Review in Advance first posted online
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C E
I N
A
D V A
Origin and Diversification

of Eukaryotes
Laura A. Katz
Department of Biological Sciences, Smith College, Northampton, Massachusetts 01063;
Annu. Rev. Microbiol. 2012.66. Downloaded from www.annualreviews.org
email: lkatz@smith.edu
Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst,
Massachusetts 01003
by Brown University on 07/14/12. For personal use only.
Annu. Rev. Microbiol. 2012. 66:411–27 Keywords

The Annual Review of Microbiology is online at eukaryotic diversity, protists, tree of life, nucleus, cytoskeleton,
micro.annualreviews.org
mitochondria
This article’s doi:
10.1146/annurev-micro-090110-102808 Abstract
Copyright c 2012 by Annual Reviews. The bulk of the diversity of eukaryotic life is microbial. Although the larger
All rights reserved
eukaryotes—namely plants, animals, and fungi—dominate our visual land-
0066-4227/12/1013-0411$20.00 scapes, microbial lineages compose the greater part of both genetic diversity
and biomass, and contain many evolutionary innovations. Our understand-
ing of the origin and diversification of eukaryotes has improved substan-
tially with analyses of molecular data from diverse lineages. These data have
provided insight into the nature of the genome of the last eukaryotic com-
mon ancestor (LECA). Yet, the origin of key eukaryotic features, namely
the nucleus and cytoskeleton, remains poorly understood. In contrast, the
past decades have seen considerable refinement in hypotheses on the major
branching events in the evolution of eukaryotic diversity. New insights have
also emerged, including evidence for the acquisition of mitochondria at the
time of the origin of eukaryotes and data supporting the dynamic nature of
genomes in LECA.
411
Changes may still occur before final publication online and in print
Contents
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412
PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST
EUKARYOTIC COMMON ANCESTOR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 414
Origin of Eukaryotic Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 414
Origin of the Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 416
Origin of the Cytoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417
Origin of Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417
PART II: EVOLUTION OF PHOTOSYNTHESIS WITH EUKARYOTES . . . . . . . 418
PART III: RELATIONSHIPS AMONG MAJOR LINEAGES . . . . . . . . . . . . . . . . . . . . . 418
Root of the Eukaryotic Tree of Life . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
Major Eukaryotic Clades . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420
CONCLUSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
INTRODUCTION
We live on a microbial planet. Microbes have dominated Earth’s history and continue to represent
Eukaryote: a cell with the majority of both biodiversity and biomass on our planet. Two of the three domains of life, the
a nucleus Bacteria and Archaea, are virtually exclusively microbial, and microbial forms dominate among
Last eukaryotic the third domain, Eukaryota, which is the focus of this review. Yet despite their importance, much
common ancestor remains to be learned about microbial life in terms of discovering of new forms, understanding
(LECA): lineage that major innovations, and incorporating the biology of microorganisms into theories and models
gave rise to extant
eukaryotes
across disciplines within biology.
Eukaryotes are named for one of their defining features—the presence of a nucleus (eu, “true,”
Cytoskeleton:
complex structure in
and karyo, “kernel” or “seed”). A defining feature is one that is found in every eukaryote and
eukaryotes that that was present in the last eukaryotic common ancestor (LECA). A second defining feature is
provides for shape and the presence of a cytoskeleton, which is a complex set of structures underlain by a tremendous
motility diversity of proteins (e.g., actins, tubulins, dyneins). The cytoskeleton gives eukaryotes their diverse
morphologies (Figure 1), variable motility, and ability to engulf other organisms.
Early attempts to reconstruct the tree of life focused on macroscopic organisms, first di-
viding living things between Plantae and Animalia, and then adding Protista as a grab bag of
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 1
Representative eukaryotic lineages, with quotes around taxon names that are either controversial or as yet lack robust support,
following suggestions in References 88 and 126: (a–c) ‘Plantae.’ (a) Eremosphaera viridis, a green alga. (b) Cyanidium sp., a red alga.
(c) Cyanophora sp., a glaucophyte, (d ) Chroomonas sp., a cryptomonad. (e) Emiliania huxleyi, a haptophyte. ( f–m) ‘SAR’ (Stramenopila,
Alveolata, and Rhizaria). ( f ) Akashiwo sanguinea, a dinoflagellate. ( g) Trithigmostoma cucullulus, a ciliate. (h) Colpodella perforans, an
apicomplexan. (i ) Thalassionema sp., a colonial diatom. ( j–m) ‘Rhizaria.’ ( j ) Chlorarachnion reptans, a core cercozoan. (k) Acantharea sp.,
formerly known as a radiolarian. (l ) Ammonia beccarii, a calcareous foraminiferan. (m) Corallomyxa tenera, a reticulate rhizarian amoeba.
(n–p) ‘Excavata.’ (n) Jakoba sp., a jakobid with two flagella. (o) Chilomastix cuspidata, a flagellate in Fornicata. ( p) Euglena sanguinea, an
autotrophic Euglenozoa. (q–s) ‘Amoebozoa.’ (q) Trichosphaerium sp., a naked stage (lacking surface spicules) of an unusual amoeba with
alternation of generations, one naked and one with spicules. (r) Stemonitis axifera, a dictyostelid. (s) Arcella hemisphaerica, a testate
amoeba in Tubulinea. (t–w) Opisthokonta. (t) Homo sapiens, animal. (u) Campyloacantha sp., a choanoflagellate. (v) Amanita flavoconia, a
basidiomycete fungus. (w) Chytriomyces sp., a chytrid. All images are provided by micro∗ scope (http://starcentral.mbl.edu/
microscope/portal.php) except panel t, which is provided by the author. Redrawn from Reference 116, BioScience 59(6), Copyright
2009, American Institute of Biological Sciences.
412 Katz
organisms that did not clearly fit in either category (reviewed in Reference 103). Beginning in the
mid-twentieth century, biodiversity was seen as belonging to five kingdoms: macroscopic plants,
animals, and fungi, and microscopic monera (bacteria) and protists (80, 121, 122). With the advent
of better microscopes and, more recently, the explosion of molecular studies, the tree of life has
been divided into three major domains—Bacteria, Archaea, and Eukaryota (124, 125)—with a
still-disputed number of major clades within each.
The review discusses current ideas on the origin and diversification of eukaryotes through
evaluation of evidence, review of recent hypotheses, and indication of open questions. To this
end, I focus on three topics: the origin of eukaryotes based on insights from analyses of features
present in LECA, the acquisition of photosynthesis among eukaryotes, and the relationships
among extant eukaryotes.
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www.annualreviews.org • Origin and Diversification of Eukaryotes 413
PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST

EUKARYOTIC COMMON ANCESTOR
LGT: lateral gene Beyond the ubiquitous nucleus and cytoskeleton, we can infer that LECA was complex in terms
transfer, also called of its morphology and genome. Insights into LECA emerge from a long history of study of
horizontal gene diverse eukaryotic organisms coupled with more recent inferences from molecular data. These
transfer
data reveal that LECA had complex morphology, with a nucleus, mitochondria, and a cytoskeleton
Chimerism: the plus associated features (e.g., flagella). As argued in detail below, LECA also had a genome that
presence of genes of
was both chimeric, with respect to bacteria and archaea, and dynamic, with epigenetic phenomena
varying ancestries
within eukaryotic playing key roles during life cycles.
genomes
Homologs: shared
characteristics present Origin of Eukaryotic Genomes
in last common
ancestor of a group of Evidence of the evolutionary history of eukaryotic genomes provides a backdrop for interpretation
of all other eukaryotic features. For example, the genomes of extant eukaryotes are chimeric,
organisms
containing genes with ancestries among both the bacteria and archaea (38, 44, 45, 47, 117).
Interpreting the history of lineages that contributed to LECA’s genome is complicated given the
extensive lateral gene transfer (LGT) that occurred before and after the origin of eukaryotes. In a
recent genome-scale study, eukaryotic genes were related most frequently to either Euryarchaeota
or Alphaproteobacteria but there were many other sister relationships that reflect the complex history
of LGT across the tree of life (117).
Models of the origins of eukaryotes account for this chimerism by hypothesizing a fusion or
similar event between an archaeon and a bacterium. In the simplest forms, these models refer to
just the fusion of unspecified bacterial and archaeal lineages (127) or, in the case of the hypothesis
on the ring of life, a fusion between a proteobacterium and an archaeal eocyte (96). In their more
refined forms, such models aim to explain multiple features of eukaryotes beyond the origin of
the chimeric genome, including the acquisition of mitochondria (Figure 2); under these versions,
the players are generally an archaeon and a proteobacterium (83).
LGTs that occurred after the origin of eukaryotes have also contributed to the chimeric nature
of eukaryotic genomes. In contrast to previous beliefs that LGT is a property of bacterial and
archaeal life, recent analyses of individual genes and complete genomes indicate that eukaryotes
have also been impacted by LGT because eukaryotic genomes contain genes transferred from
bacteria, archaea, and other eukaryotes (e.g., 4, 5, 63, 66, 69). The transfer of genes is likely
enhanced by the ability of eukaryotes to engulf other organisms, and this feature inspired the
application of the phrase “you are what you eat” as a descriptor of the mechanism underlying the
chimeric nature of eukaryotic genomes (43) (Figure 2).
Beyond chimerism, we can infer that LECA had a complex genome including spliceosomal
introns and diverse epigenetic mechanisms (70, 116), which suggest an important role for RNAs in
shaping eukaryotic genome structure. The presence of a spliceosome (a complex structure made of
both RNA and proteins) in LECA is supported by the broad distribution of spliceosomal introns
across the eukaryotic tree of life (reviewed in Reference 100). Homologs to many spliceosomal
components are not apparent in bacteria or archaea, and it is not clear how these complex structures
evolved (97, 119). Similarly, the machinery for RNAi and other epigenetic phenomena was also
likely present in LECA, as components such as Dicer and Argonaute are widespread among
eukaryotes (35, 104).
The genome of LECA was likely also dynamic. Features such as cyclic polyploidization, ex-
trachromosomal DNA, and life-cycle-dependent chromosomal rearrangements are widespread
among extant eukaryotes (91, 92, 128). For example, extrachromosomal ribosomal DNAs are
414 Katz
e
d
f
c LECA
Nucleus
i Modern eukaryote g
Mitochondrion
b Eukaryogenesis Chimeric
genome
h
Proteobacterium
Archaeon
Figure 2
The chimeric nature of genome in extant eukaryotes (center image, i ) is consistent with a fusion of an
archaeon and a bacterium at the time of the origin of eukaryotes (83) coupled with subsequent aberrant
lateral transfers of genes from food items (43). (a) An archaeon and a proteobacterium that are potential
symbiotic partners in the origin of eukaryotes. (b) Eukaryogenesis, the origin of the nucleus, cytoskeleton,
and mitochondria through as yet unknown mechanisms and events. (c) Last eukaryotic common ancestor
(LECA) with nucleus, mitochondria, and chimeric genome (i.e., purple portions of chromosome). (d–h)
Repeated engulfment of food and incorporation of genes into the host nucleus. (i ) Modern eukaryote whose
chimeric genome is the product of panels a–h. Redrawn from Reference 116, BioScience 59(6), Copyright
2009, American Institute of Biological Sciences.
found in diverse lineages such as Euglena (‘Excavata’), Dictyostelium (‘Amoebozoa’), ciliates (‘SAR,’
Stramenopila, Alveolata, and Rhizaria), and Xenopus (Opisthokonta), among others (128). The
presence of extrachromosomal copies of other genes also appears widespread, at least among
plants and animals (36), and has also been hypothesized to exist among foraminiferans (‘SAR’;
54, 92). Life-cycle-dependent chromosomal rearrangements occur in ciliates (‘SAR’), flax (‘Plan-
tae’), and some animal lineages including copepods, nematodes, and hagfish (92, 128). A special
case of genome dynamics involves antigenic variation in parasites seeking to escape host immune
systems [e.g., trypanosomes (‘Excavata’); 115] and in the adaptive immune responses of the host
‘SAR’: hypothesized
genomes [e.g., V(D)J systems in vertebrates; 60]; here, a combination of DNA rearrangements
major clade of
and epigenetic mechanisms govern these dynamic genome features. eukaryotes containing
The existence of dynamic features across diverse eukaryotes suggests that all eukaryotes are Stramenopila,
able to distinguish the portion of their genome that will be inherited (i.e., a germline genome) Alveolata, and Rhizaria
from the remainder of the genome that is more malleable (i.e., a somatic genome; Table 1). This
Table 1 Evidence for germline/soma distinctions among diverse eukaryotes

Category Feature Exemplar taxa References
Chromosomal Extrachromosomal rDNA Many including Euglena, 128
rearrangements Entamoeba, Dictyostelium, and
Xenopus
Other extrachromosomal Various plants and animals 36
DNAs
Antigenic variation Trypanosoma 115
Adaptive immune Vertebrates 60
response [V(D)J]
Distinct germline and Sequestered germline Triploblast animals, ciliates, 49, 50, 65, 87
somatic nuclei and some foraminiferans
Processing of somatic Ciliates, nematodes, copepods, 15, 86, 92,
chromosomes and hagfish 128
Changes in DNA content Zerfall (see text) Various foraminiferans 14, 54, 90
Cyclical polyploidization Various lineages including 92

Foraminifera, Phaeodaria,
some Lobosea, Oxymonadida,
and Apicomplexa
distinction is most obvious in eukaryotes such as triploblast animals, which generally sequester
their germline genomes early in development (49, 50), and in ciliates as well as some foraminifer-
ans, which have distinct germline and somatic nuclei within a single cell (65). Beyond these
sequestered genomes, a long list of broadly distributed lineages with features such as cyclical poly-
ploidy, extrachromosomal gene copies, and developmentally regulated genome rearrangements
demonstrates the considerable flexibility among eukaryotic genomes (91, 92, 128) (Table 1).
For example, during the life cycle of foraminiferans, portions of the genome are eliminated prior
to nuclear division; this process, termed zerfall, may be indicative of the removal of amplified
chromosomes or portions of chromosomes prior to the separation of germline material (14, 54,
91). We hypothesize that eukaryotes use epigenetic markers to distinguish the germline genome
from the somatic genome through dynamic processes described above (91, 92, 128).
Origin of the Nucleus

The origin of the nucleus, the feature that gives eukaryotes their name, remains a mystery. The
nucleus is a complex structure with an outer membrane that is generally contiguous with the
endoplasmic reticulum and has a system of multiprotein pores that enable transport from cytoplasm
to nucleoplasm. As with the origin of eukaryotes themselves, hypotheses on the origin of the
nucleus can be divided into those that focus on endosymbiosis and those that focus on autogenous
origins (reviewed in Reference 81). Few data support either hypothesis, and phylogenomic studies
have not provided much help as most genes encoding the nuclear proteome lack clear homologs
in bacteria and archaea.
Several recent hypotheses have emerged supporting the autogenous origin of the nucleus.
Endosymbiosis: Cavalier-Smith (30) presents an extensive discussion on the evolution of the nucleus that builds
symbiosis in which one from details on both the cell and the molecular biology of eukaryotic cells. Another hypothesis
organism lives within focuses on the potential benefit in separating nucleoplasm and cytoplasm functions following
another expansion of the number of group II introns in the genome (82). Under this hypothesis, the nuclear
compartment evolved as a way of separating the processing of RNAs (e.g., removal of expanding
416 Katz
numbers of introns) from translation; these two processes can occur nearly simultaneously in
bacteria and archaea.
Amitochondriate:
describes organisms
Origin of the Cytoskeleton
lacking mitochondria
As with the nucleus, few data support existing hypotheses on the origin of the eukaryotic cy-
toskeleton and its many diverse proteins. Perhaps even more important for cell function than the
nucleus, the cytoskeleton provides eukaryotic cells with their diverse structures, forms of motil-
ity, and the ability to engulf other cells. Margulis and colleagues (e.g., 77–79) argued that the
eukaryotic cytoskeleton is specifically descended from structures in spirochetes. In this scenario,
early eukaryotic cells moved first in a loose association with these highly motile bacteria, and this
association later transformed into an endosymbiosis, with the spirochete proteins evolving into
the eukaryotic cytoskeleton (79). This hypothesis is not supported by available data, as there is no
strong footprint of spirochete ancestry among eukaryotic cytoskeletal genes (7). Instead, eukary-
otic cytoskeletal proteins either lack bacterial/archaeal homologs or have distant homologs as is
the case for actin/MreB and tubulin/FtsZ (123).

Origin of Mitochondria
In contrast with knowledge on the origin of the nucleus and cytoskeleton, both the timing of and
the source for the acquisition of mitochondria are now well understood. Mitochondria are derived
from an alphaproteobacterium, as evidenced by similarities in their morphology and genomes (48,
55). Phylogenetic analyses of mitochondrial genes place eukaryotic mitochondria as a single clade
nested among extant Alphaproteobacteria (52, 98). The bacterium that gave rise to mitochondria
may have been either a parasite, related to the extant alphaproteobacterial lineage Rickettsia, or a
partner in early symbiosis (Figure 2).
The phylogenetic distribution of mitochondria plus mitochondria-derived organelles indicates
that mitochondria were acquired prior to the divergence of extant eukaryotes (105). Numer-
ous amitochondriate lineages, including the parasitic genera Trichomonas and Giardia, some
free-living ciliates (e.g., Trimyema and Metopus), and several fungal genera (e.g., Neocallimastix,
Encephalitozoon), are restricted largely to anaerobic or microaerophilic environments (46, 58,
61, 85, 105). All these lineages nest within larger clades of mitochondria-containing lineages.
For example, Trichomonas and Giardia are placed within the ‘Excavata,’ which contain numerous
mitochondria-containing lineages such as Euglenozoa, Jakobida, and Heterolobosea. Moreover,
mitochondria-derived organelles have been found in many lineages that had previously been
considered amitochondriate; these organelles are alternatively called hydrogenosomes [e.g.,
in Neocallimastix, Nyctotherus (ciliate), and Trichomonas] or mitosomes (e.g., in Encephalitozoon,
Giardia, and Cryptosporidium) (61, 85, 105). Finally, genes of alphaproteobacterial origin have been
found in the nuclear genomes of amitochondriate eukaryotes, again consistent with secondary
loss of this organelle (61, 105). However, interpretation of the last observation is complicated by
the tremendous exchange of genes among lineages across the tree of life (117).
Following the acquisition of mitochondria, there have been complex patterns of gene reten-
tion, gene transfer to nucleus, and redirection of non-alphaproteobacterial proteins to the mito-
chondrial proteome (71, 113). Gene number within mitochondrial genomes is small (i.e., 7–90
genes) (16) relative to the complexity of mitochondrial proteome, and mitochondrial genomes
are often reduced to a handful of proteins, most of which are involved in cellular respiration
(55). Phylogenetic reconstructions indicate that there have been many parallel losses of genes
from mitochondria since LECA (55). Today, the proteome of mitochondria is derived from the
handful of mitochondrially encoded genes, a relatively small number of genes of alphaproteobac-

terial origin that are now encoded in the nucleus, and numerous other nuclear genes from varying
sources whose products have been redirected to the mitochondria (113). This complexity underly-
Monophyly: a group
of organisms that ing the mitochondrial proteome may have provided the energetic leap required for the evolution
includes an ancestor of complex and ultimately macrobial eukaryotic lineages (74).
and all descendants
PART II: EVOLUTION OF PHOTOSYNTHESIS WITH EUKARYOTES
Plastids, the generic name for chloroplasts, are present in a diverse array of lineages across the
eukaryotic tree of life (Figure 3) and were likely acquired after diversification of major lineages (93).
Plastids are derived from cyanobacteria, as evidenced by both structural similarities and sequence
analysis of plastid genomes (24). There is still, however, debate on the number and timing of the
acquisitions of this organelle and on the contributions of genes from other photosynthetic lineages
in shaping photosynthesis among eukaryotes (12, 51, 75). The current popular view is that there
was a single primary acquisition of chloroplasts in the last common ancestor of a clade alternatively
named ‘Plantae’ or ‘Archaeplastida’ containing green algae, red algae, and glaucophytes (2, 28, 39).
Evidence for a single primary acquisition of plastids includes the phylogeny of plastid genes, which
tend to form a monophyletic group within extant cyanobacteria (37, 42), and a shared Tic-Toc
transport system for moving proteins across plastid membranes (64).

Contradictory evidence does exist, including the multiple origins of the key photosynthetic
enzyme RuBisCo and the complex origins of the varying plastid pigments (12, 40, 75, 114).
Further, there appears to have been a major bottleneck among cyanobacteria after the acquisition
of plastids in eukaryotes, making it impossible to distinguish between single and multiple origins
by looking at the history of plastid genes, as close relatives of potential donor lineages may have
gone extinct (37). An alternative model for the evolution of photosynthesis among eukaryotes,
termed the shopping bag model, suggests that photosynthesis among eukaryotes relies on the
products of genes acquired from multiple sources by LGT over evolutionary time (75).
The remaining lineages of photosynthetic eukaryotes (e.g., diatoms, brown algae, euglenids,
cryptomonads, haptophytes, and dinoflagellates) acquired plastids by engulfing either a red or
green alga in a process called secondary endosymbiosis (6, 39). That secondary endosymbioses
have occurred is indisputable, but the number of these events is more contentious. Two lineages,
cryptomonads and chlorarachniophytes (core Cercozoa), have retained a remnant nucleus (nu-
cleomorph) from a red and green algal endosymbiont, respectively (6, 25). Sequencing of these
remnant nuclei reveals that these highly reduced genomes contain few genes involved in plastid
function (8, 53, 84).
The history of plastid acquisition among lineages that lack a nucleomorph remains debated.
One convenient hypothesis, which has now been rejected by many independent analyses, is that
there was a single acquisition of a red algal symbiont at the base of the ‘Chromalveolate’ clade,
which was originally described to include alveolates, stramenopiles, cryptomonads, and hapto-
phytes (23). However, numerous analyses of these host genomes fail to support the monophyly of
this group (13, 56, 62, 89). Multigene analyses indicate stramenopiles and alveolates fall in a clade
with the Rhizaria, and there is no compelling evidence of an ancestral red algal plastid within the
Rhizaria (18, 19, 57). Finally, as discussed below, the position of haptophytes and cryptomonads
remains uncertain, as the relationships of these lineages are unstable in many analyses (88, 89).
PART III: RELATIONSHIPS AMONG MAJOR LINEAGES

Because of their incredible morphological diversity, eukaryotic microorganisms (protists) have
been the subject of intense study since the time of the earliest microscopes. These earliest studies
418 Katz
focused primarily on describing taxa rather than estimating higher-level relationships (1, 103). My
interpretation of this rich history is that many of the shallower (i.e., more recent) clades defined
by morphology and/or ultrastructural features have remained robust to more recent molecular
Paralogs: duplicated
analyses (88, 89, 94), though exceptions certainly exist. copies of a gene
With the advent of phylogenetic analyses based on DNA sequence data, the field of eukaryotic
ssu-rDNA: small
systematics has gone through considerable turmoil, though hypotheses do seem to be coalescing subunit ribosomal
in recent years. Molecular analyses of eukaryotic diversity were launched with analyses of the ubiq- DNA
uitous small-subunit ribosomal RNA (ssu-rRNA, and later ssu-rDNA) sequences, which initially
suggested the idea that eukaryotic diversity consisted of a base of microbial lineages topped by a
crown of plants, animals, and fungi and their microbial relatives (109, 118). As additional genes
were sequenced and revealed conflicting topologies, there was a brief period in which arguments
were made for why one gene was better than another, and then the field launched into combined
analyses of multiple genes (11). In most of these analyses, an individual sequence is chosen to
represent each taxon (i.e., paralogs removed) and these sequences are concatenated to yield many
characters per taxon. Such multigene studies have led to a plethora of hypotheses about eukaryotic
diversity (17–19, 28, 29, 33, 34, 59, 76, 101, 111).
One somewhat discouraging aspect of eukaryotic systematics is the heterogeneity in philosophy
for naming higher taxa (i.e., more inclusive clades), which I describe in overly simplistic terms
below to highlight the differences in approaches. There is a tendency to subscribe to what could
be called the “Chupacabra” approach, whereby clades are named on the basis of only very limited
data and upon first sighting. (The Chupacabra is a mythical creature that has been reported in the
Americas, parallel to sightings of Big Foot in the Pacific Northwest of the United States). A second
discouraging approach is one whereby researchers set out to find data to support a hypothesis,
often of the Chupacabra type. Here, a researcher might sift among thousands of observations (e.g.,
expressed sequence tags, genome sequences) to find a half dozen or so that support a hypothesis
and then use these data to conclude that a hypothesis is correct regardless of the insights from
the remaining observations. Fortunately, the approaches described above are not adopted by the
majority of the field, as most focus on analyses of all available data and draw conclusions based on
the preponderance of evidence in manuscripts that discuss both caveats and alternative hypotheses.
Because the field of eukaryotic systematics is in flux, I focus on a subset of hypotheses below,
including those that are best supported by current data. Numerous reviews exist for readers wanting
to know more about specific lineages and hypotheses (1, 2, 10, 18, 27–30, 68, 73, 88, 99, 108,
112).
Root of the Eukaryotic Tree of Life

The root of the eukaryotic tree of life remains unknown, largely because numerous characters
conserved among eukaryotes lack homologs in bacteria and archaea. As a result, it is difficult to
find appropriate outgroup sequences for most molecular studies. Added to this complexity is the
impact of LGT on the history of individual genes within bacteria, archaea, and those eukaryotes
that lack sequestered germline genomes (4, 69). Hypotheses on the location of the root either
have focused on characters argued to be primitive or have emerged from analyses of molecular
data. For example, the “Archezoa” hypothesis (21, 31) argued that the root of eukaryotes lay
among putatively primitive amitochondriate lineages such as Trichomonas and Giardia, which are
now known to be nested in clades of mitochondria-containing lineages. Similarly, a root between
‘Amoebozoa’ + Opisthokonta (the so-called unikonts, as many members with flagella have only
a single flagellum) and all remaining eukaryotes has been proposed on the basis of a gene fusion
event (26, 111). Alternatively, several studies suggest that the root of the eukaryotic tree of life lies
between Opisthokonta and all remaining eukaryotes (9, 41, 110), which is what we found based
on gene tree parsimony analyses of ∼20 genes (67). Our understanding of the location of the root
of the eukaryotic tree of life will likely change with the addition of data, from both genes and yet
unsampled taxa, and the development of new analytical tools.
Major Eukaryotic Clades

Estimates on the nature of major clades in the eukaryotic tree of life have stabilized in recent
years (Figure 3). Early molecular studies led to a slew of hypotheses, often based on very few
data, that have seen varying fates with collection of additional data. These major clades have been
named supergroups (2, 108), creating a novel taxonomic hierarchy that lacks rigorous definition.
In more recent years, these major clades have been subjected to more evaluation, moving beyond
resampling the same data (i.e., ssu-rDNA and a few genes) to more gene- and taxon-rich approaches
(18). Comprehensive taxon sampling is key to characterizing the eukaryotic tree of life, and we can
anticipate changes as additional lineages are sampled. On the basis of the current understanding of
molecular and morphological characters, several major eukaryotic lineages have emerged, albeit
with varying levels of support. Details on membership and support for these groups have been
reviewed elsewhere (1, 88, 108), so I provide only highlights here, with quotes around taxon names
that are either controversial or lack robust support.
The best supported of the major clades is the Opisthokonta, which unites animals, fungi, and
their microbial relatives (32, 112, 120). The name Opisthokonta reflects the posterior (“opistho”)
position of the flagellum (“kont”) in lineages that have maintained flagella (32). The monophyly
of this group is supported by numerous molecular characters (59, 88, 89, 112). The strong support
for this clade is also consistent with hypotheses that place the root of the eukaryotic tree of life
between opisthokonts and all remaining eukaryotes (9, 41, 67, 110).
The ‘Amoebozoa’ were first proposed from early molecular analyses (22), and this clade has
generally remained robust in light of additional sampling of genes and taxa (59, 72, 89, 95). This
diverse clade contains the classic lobose amoeba (e.g., Amoeba proteus), the beautiful testate (shelled)
amoebae in the Arcellinida, the slime molds (e.g., Physarum and Dictyostelium), and the causative
agent of dysentery (Entamoeba histolytica).
The ‘Excavata’ were hypothesized on the basis of a morphological feature, an excavate grove,
in the last common ancestor of this clade (26, 106, 107). Whereas early molecular trees failed
to support this clade (88), more recent analyses do recover ‘Excavata,’ albeit with low support at
deep nodes (59, 89). Many members of this clade, such as the human parasites Giardia lamblia
and Trichomonas vaginalis, have elevated rates of evolution across their genomes, which likely
contributes to the instability of the ‘Excavata.’
The placement of photosynthetic lineages remains more problematic, likely due to the com-
bination of multiple secondary (and tertiary and quaternary) endosymbiotic transfer events and
endosymbiotic gene transfer from plastid to host (6, 13, 62, 102). As discussed above, the ‘Plantae’
(or ‘Archaeplastida’) (2) unite three lineages—green algae, red algae, and glaucophytes—that are
believed to be descended from the eukaryote that first evolved plastids through symbiosis with a
cyanobacterium (20, 39). Evidence in support of the hypothesis of a single primary endosymbiosis
at this time includes the shared machinery for transport across plastid membranes. However, phy-
logenies based on genes in the nucleus are not consistent in recovering the monophyly of these
lineages, as red algae often fall outside of this clade (89).
Perhaps most unstable in recent years has been our understanding of relationships among
members of what has recently been called the ‘SAR’ clade: Stramenopila, Alveolata, and Rhizaria
(18, 19, 57). Each of these three clades appears to represent diverse monophyletic assemblages,
420 Katz
Polycystinea SAR
Acantharea
Foraminifera
Vampyrellids Rhizaria
Plasmodiophora
Haplosporidia
Core Cercozoa*
Diatoms*
Brown algae*
Chrysophytes*
Stramenopila
Oomycetes
Labyrinthulids
Blastocystis
Dinoflagellates*
Apicomplexa* Alveolata
Ciliates
Haptophytes*
Centroheliozoa
Glaucophytes*
Red algae*
Plantae
Green algae*
Cryptomonads*
Euglenozoa*
Heterolobosea
Excavata
Jakobids
Preaxostyla
Fornicata
Parabasalia
Malawimonas
Thecamoebae
Vannellids Amoebozoa
Centramoebida
Myxogastrids
Dictyostelids
Pelobionts
Mastigamoebida
Tubulinea
Ancyromonas
Apusomonads
Breviata + Subulatomonas
Animals
Opisthokonta
Choanoflagellates
Ichthyosporea
Fungi
Chytrids
Figure 3
Phylogenetic relationships among representatives of major lineages of eukaryotes. Lineages with members
that have plastids are marked with an asterisk. The figure synthesizes information from literature discussed
in the text.
with greater support for the first two than for Rhizaria. Yet, relationships among these lineages
and their putative relatives have been more controversial. Both stramenopiles and alveolates are
supported by morphological and molecular data, and both represent diverse assemblages of pho-
tosynthetic and nonphotosynthetic lineages. Synapomorphies for these clades include hair-like
structures on one flagellum in the stramenopiles (3) and alveolar sacs in the alveolates (94). In
contrast, the Rhizaria were originally proposed on the basis of molecular analyses (57) and this
major clade lacks clear morphological or molecular synapomorphies.
Synapomorphy:
a shared, derived The stramenopiles and alveolates, along with the haptophytes and cryptomonads, had been
characteristic marking argued to be part of the ‘Chromalveolata’ on the basis of a hypothesis that the last common
a monophyletic group ancestor of this group engulfed a red algal symbiont (23). Although a few genes can be found to
support this hypothesis, the preponderance of evidence fails to support the monophyly of these
host lineages. Instead, the stramenopiles and alveolates appear to fall in a clade with the Rhizaria,
and the placement of cryptomonads and haptophytes remains as yet unclear (89).
Given that our understanding of the structure of eukaryotic diversity is dependent on the
available taxon sampling to date, data from additional lineages will likely transform our views
on deep relationships. Additional taxon sampling may also stabilize the list of orphan lineages
(lineages without clear sister taxa and without clear placement in eukaryotic tree of life), which
includes cryptomonads, haptophytes, centroheliozoans, and breviates (89). Moreover, there are
likely additional, as yet undiscovered lineages to be added to the eukaryotic tree of life.
CONCLUSION
The greatest diversity of eukaryotes on Earth exists among microbial lineages, and analyses of these
lineages have yielded many insights into basic principles of biology. Innovations among eukaryotes
include the acquisition of organelles through endosymbioses (i.e., mitochondria and plastids),
dynamic genomes marked by chromosomal rearrangements and cyclical polyploidization, and
myriad diverse morphologies underlain by a complex cytoskeleton. With the rise of studies on
eukaryotic diversity coupled with powerful tools in molecular biology and microscopy, we are
poised to collect additional data that will illuminate details on the origin and diversification of
eukaryotic life on Earth.
SUMMARY POINTS
1. The bulk of eukaryotic diversity is microbial, with lineages marked by a dazzling array
of morphological and genomic innovations.
2. Despite recent advances, many aspects of the origin of eukaryotes (e.g., origin of nucleus
and cytoskeleton) remain unknown.
3. The last common ancestor of extant eukaryotes had a complex and dynamic genome that
may have been able to distinguish between DNA to be passed on to future generations
(i.e., germline) and more flexible ‘somatic’ DNA.
4. The shape of the eukaryotic tree of life has come into clearer focus in recent years,
although many open questions remain.
DISCLOSURE STATEMENT
The author is not aware of any affiliations, memberships, funding, or financial holdings that might
be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
I am grateful to numerous students and colleagues, including Jessica Grant, Daniel Lahr, Bill
Martin, and Laura Wegener Parfrey, for discussions of the concepts in this manuscript. This work
422 Katz
was supported by grants from the National Science Foundation (OCE-0648713, ATOL-043115,
DEB-0919152) and the National Institutes of Health (1R15GM081865-01).
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Origin and Diversificationof Eukaryotes

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Origin and Diversificationof Eukaryotes

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MI66CH20-Katz ARI 21 June 2012 17:22

Origin and Diversiﬁcation

Annu. Rev. Microbiol. 2012. 66:411–27 Keywords

www.annualreviews.org • Origin and Diversification of Eukaryotes 413

PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST

www.annualreviews.org • Origin and Diversification of Eukaryotes 415

Table 1 Evidence for germline/soma distinctions among diverse eukaryotes

Cyclical polyploidization Various lineages including 92

Origin of the Nucleus

the case for actin/MreB and tubulin/FtsZ (123).

www.annualreviews.org • Origin and Diversification of Eukaryotes 417

handful of mitochondrially encoded genes, a relatively small number of genes of alphaproteobac-

transport system for moving proteins across plastid membranes (64).

PART III: RELATIONSHIPS AMONG MAJOR LINEAGES

Root of the Eukaryotic Tree of Life

www.annualreviews.org • Origin and Diversification of Eukaryotes 419

Major Eukaryotic Clades

www.annualreviews.org • Origin and Diversification of Eukaryotes 421

www.annualreviews.org • Origin and Diversification of Eukaryotes 423

Trans. R. Soc. Lond. B 363:2675–85

www.annualreviews.org • Origin and Diversification of Eukaryotes 425

www.annualreviews.org • Origin and Diversification of Eukaryotes 427

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