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Origin and Diversification of Eukaryotes Annu. Rev. Microbiol. 2012.66. Downloaded from www.annualreviews.org by University of Bristol on 09/13/12. For personal use only.
Laura A. Katz Department of Biological Sciences, Smith College, Northampton, Massachusetts 01063; email:
[email protected] Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts 01003
Annu. Rev. Microbiol. 2012. 66:411–27
Keywords
The Annual Review of Microbiology is online at micro.annualreviews.org
eukaryotic diversity, protists, tree of life, nucleus, cytoskeleton, mitochondria
This article’s doi: 10.1146/annurev-micro-090110-102808 c 2012 by Annual Reviews. Copyright All rights reserved 0066-4227/12/1013-0411$20.00
Abstract The bulk of the diversity of eukaryotic life is microbial. Although the larger eukaryotes—namely plants, animals, and fungi—dominate our visual landscapes, microbial lineages compose the greater part of both genetic diversity and biomass, and contain many evolutionary innovations. Our understanding of the origin and diversification of eukaryotes has improved substantially with analyses of molecular data from diverse lineages. These data have provided insight into the nature of the genome of the last eukaryotic common 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.
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Contents INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST EUKARYOTIC COMMON ANCESTOR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin of Eukaryotic Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin of the Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin of the Cytoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin of Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PART II: EVOLUTION OF PHOTOSYNTHESIS WITH EUKARYOTES . . . . . . . PART III: RELATIONSHIPS AMONG MAJOR LINEAGES . . . . . . . . . . . . . . . . . . . . . Root of the Eukaryotic Tree of Life . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Major Eukaryotic Clades . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . CONCLUSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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INTRODUCTION Eukaryote: a cell with a nucleus Last eukaryotic common ancestor (LECA): lineage that gave rise to extant eukaryotes Cytoskeleton: complex structure in eukaryotes that provides for shape and motility
We live on a microbial planet. Microbes have dominated Earth’s history and continue to represent the majority of both biodiversity and biomass on our planet. Two of the three domains of life, the Bacteria and Archaea, are virtually exclusively microbial, and microbial forms dominate among the third domain, Eukaryota, which is the focus of this review. Yet despite their importance, much remains to be learned about microbial life in terms of discovering of new forms, understanding major innovations, and incorporating the biology of microorganisms into theories and models across disciplines within biology. Eukaryotes are named for one of their defining features—the presence of a nucleus (eu, “true,” and karyo, “kernel” or “seed”). A defining feature is one that is found in every eukaryote and that was present in the last eukaryotic common ancestor (LECA). A second defining feature is the presence of a cytoskeleton, which is a complex set of structures underlain by a tremendous 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 dividing 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
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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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PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST EUKARYOTIC COMMON ANCESTOR LGT: lateral gene transfer, also called horizontal gene transfer
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Chimerism: the presence of genes of varying ancestries within eukaryotic genomes Homologs: shared characteristics present in last common ancestor of a group of organisms
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Beyond the ubiquitous nucleus and cytoskeleton, we can infer that LECA was complex in terms of its morphology and genome. Insights into LECA emerge from a long history of study of diverse eukaryotic organisms coupled with more recent inferences from molecular data. These data reveal that LECA had complex morphology, with a nucleus, mitochondria, and a cytoskeleton plus associated features (e.g., flagella). As argued in detail below, LECA also had a genome that was both chimeric, with respect to bacteria and archaea, and dynamic, with epigenetic phenomena playing key roles during life cycles.
Origin of Eukaryotic Genomes 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, 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, extrachromosomal DNA, and life-cycle-dependent chromosomal rearrangements are widespread among extant eukaryotes (91, 92, 128). For example, extrachromosomal ribosomal DNAs are Katz
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e d f c LECA Nucleus
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Modern eukaryote
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Mitochondrion
b Eukaryogenesis
Chimeric genome
h a 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 (‘Plantae’), 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 genomes [e.g., V(D)J systems in vertebrates; 60]; here, a combination of DNA rearrangements and epigenetic mechanisms govern these dynamic genome features. The existence of dynamic features across diverse eukaryotes suggests that all eukaryotes are able to distinguish the portion of their genome that will be inherited (i.e., a germline genome) from the remainder of the genome that is more malleable (i.e., a somatic genome; Table 1). This www.annualreviews.org • Origin and Diversification of Eukaryotes
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‘SAR’: hypothesized major clade of eukaryotes containing Stramenopila, Alveolata, and Rhizaria
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Table 1
Evidence for germline/soma distinctions among diverse eukaryotes
Category Chromosomal rearrangements
Feature Extrachromosomal rDNA
Other extrachromosomal DNAs Antigenic variation Adaptive immune response [V(D)J] Distinct germline and somatic nuclei
Sequestered germline Processing of somatic chromosomes
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Changes in DNA content
Zerfall (see text) Cyclical polyploidization
Exemplar taxa
References
Many including Euglena, Entamoeba, Dictyostelium, and Xenopus Various plants and animals
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Trypanosoma Vertebrates
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Triploblast animals, ciliates, and some foraminiferans Ciliates, nematodes, copepods, and hagfish
49, 50, 65, 87
Various foraminiferans Various lineages including Foraminifera, Phaeodaria, some Lobosea, Oxymonadida, and Apicomplexa
14, 54, 90 92
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15, 86, 92, 128
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 foraminiferans, 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 polyploidy, 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
Endosymbiosis: symbiosis in which one organism lives within another
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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. Cavalier-Smith (30) presents an extensive discussion on the evolution of the nucleus that builds from details on both the cell and the molecular biology of eukaryotic cells. Another hypothesis focuses on the potential benefit in separating nucleoplasm and cytoplasm functions following 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 Katz
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numbers of introns) from translation; these two processes can occur nearly simultaneously in bacteria and archaea. Amitochondriate: describes organisms lacking mitochondria
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Origin of the Cytoskeleton As with the nucleus, few data support existing hypotheses on the origin of the eukaryotic cytoskeleton 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 motility, 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, eukaryotic 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). Numerous 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 retention, gene transfer to nucleus, and redirection of non-alphaproteobacterial proteins to the mitochondrial 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 www.annualreviews.org • Origin and Diversification of Eukaryotes
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Monophyly: a group of organisms that includes an ancestor and all descendants
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handful of mitochondrially encoded genes, a relatively small number of genes of alphaproteobacterial 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 underlying the mitochondrial proteome may have provided the energetic leap required for the evolution of complex and ultimately macrobial eukaryotic lineages (74).
PART II: EVOLUTION OF PHOTOSYNTHESIS WITH EUKARYOTES
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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 (nucleomorph) 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 haptophytes (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
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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 analyses (88, 89, 94), though exceptions certainly exist. With the advent of phylogenetic analyses based on DNA sequence data, the field of eukaryotic systematics has gone through considerable turmoil, though hypotheses do seem to be coalescing in recent years. Molecular analyses of eukaryotic diversity were launched with analyses of the ubiquitous 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).
Paralogs: duplicated copies of a gene ssu-rDNA: small subunit ribosomal DNA
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 www.annualreviews.org • Origin and Diversification of Eukaryotes
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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
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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 combination 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, phylogenies 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
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Polycystinea Acantharea Foraminifera Vampyrellids Plasmodiophora Haplosporidia Core Cercozoa* Diatoms* Brown algae* Chrysophytes* Oomycetes Labyrinthulids Blastocystis Dinoflagellates* Apicomplexa* Ciliates
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Haptophytes* Centroheliozoa Glaucophytes* Red algae* Green algae* Cryptomonads* Euglenozoa* Heterolobosea Jakobids Preaxostyla Fornicata Parabasalia Malawimonas Thecamoebae Vannellids Centramoebida Myxogastrids Dictyostelids Pelobionts Mastigamoebida Tubulinea Ancyromonas Apusomonads Breviata + Subulatomonas Animals Choanoflagellates Ichthyosporea Fungi Chytrids
SAR Rhizaria
Stramenopila
Alveolata
Plantae
Excavata
Amoebozoa
Opisthokonta
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 photosynthetic and nonphotosynthetic lineages. Synapomorphies for these clades include hair-like www.annualreviews.org • Origin and Diversification of Eukaryotes
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Synapomorphy: a shared, derived characteristic marking a monophyletic group
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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. The stramenopiles and alveolates, along with the haptophytes and cryptomonads, had been argued to be part of the ‘Chromalveolata’ on the basis of a hypothesis that the last common 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
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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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