sign in sign up
<<
Home , Acantharea, Alveolate, Amorphea, Ancyromonas, Apicomplexa, Archezoa

Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Eukaryotic Tree of from a Global Phylogenomic Perspective

Fabien Burki

Canadian Institute for Advanced Research, Department of , University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada Correspondence: [email protected]

Molecular has revolutionized our knowledge of the eukaryotic . With the advent of , a new discipline of phylogenetics has emerged: phylogenom- ics. This method uses large alignments of tens to hundreds of to reconstruct - ary histories. This approach has led to the resolution of ancient and contentious relationships, notably between the building blocks of the tree (the supergroups), and allowed to place in the tree enigmatic yet important lineages for understanding evolution. Here, I discuss the pros and cons of and review the eukaryotic supergroups in light of earlier work that laid the foundation for the current view of the tree, including the position of the . I conclude by presenting a picture of eukaryote evolution, summarizing the most recent progress in assembling the global tree.

t is redundant to say that are di- ticellular . Eukaryotes have occupied Iverse. , , and fungi are the char- just about every ecological niche on . ismatic representatives of the eukaryotic do- Some actively gather food from the environ- main of life, but this narrow view does not do ment, others use () to de- justice to the eukaryotic diversity. Microscop- rive from the light; many can adapt to ic eukaryotes, often unicellular and known as variable conditions by switching between auto- the , represent the bulk of most major trophy and the predatory consumption of prey groups, whereas multicellular lineages are con- by phagotrophy. Eukaryotes also show a great fined to small corners on the global tree of eu- deal of genomic variation (Lynch and Conery karyotes. If all eukaryotes possess structures 2003). Some amoebozoan protists, for instance, enclosed within intracellular membranes (the have the largest known —more than ), an infinite variation of forms and 200 larger than that of (Keeling feeding strategies has evolved since their origin. and Slamovits 2005). Conversely, microbial Eukaryotic cells can wander on their own, some- parasites can have highly compact, bacterial- times forming hordes of free-living pico-sized size genomes (Corradi et al. 2010). Even smaller organisms that flourish in . They can be are the remnant nuclear genomes (nucleo- parasites or symbionts, or come together by the morphs) of what were once free-living microbi- billions in tightly packed, highly regulated mul- al . At around 500,000 and

Editors: Patrick J. Keeling and Eugene V. Koonin Additional Perspectives on The Origin and Evolution of Eukaryotes available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a016147 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147

1 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

hardly encoding a few hundreds genes, nucleo- easy to amplify and contains both hypervaria- morphs are the smallest nuclear of all ble and conserved regions, allowing researchers (Douglas et al. 2001; Gilson et al. 2006; Lane to investigate different depths of phylogenet- et al. 2007). ic resolution. As a result, the SSU rRNA domi- Recognizing this great diversity and pushed nates molecular databases, and the majority of by a desire to establish order, have the known eukaryotic diversity, when character- long attempted to assemble a global eukaryotic ized molecularly, is still defined solely by this tree of life. A fully resolved marker. including all organisms is not only the ultimate The pioneering molecular phylogenies con- goal of , it would also provide the sistently recovered a handful of deeply diverging foundation to infer the acquisition and evolu- protist lineages (e.g., , parabasal- tion of countless characters through the history ids, microsporidians, ), progres- of long-dead . But early attempts to re- sively emerging from the distant prokaryot- solve the eukaryotic tree, most of which were ic root, and followed by a densely branched based on comparisons of morphology and nu- “crown,” nesting the more familiar eukaryotic trition modes, faced the impossible challenge diversity (Sogin et al. 1986, 1989; Friedman of describing in an evolutionary sensitive way et al. 1987; Woese et al. 1990; Sogin 1991). a world in which most of the diversity occurs This was an appealing picture of evolution be- among tiny microbes. For decades, text- cause these early diverging species were seem- books assigned the eukaryotes to evolutionary ingly morphologically simple single- organ- entities called “kingdoms” in which the lords isms that lacked mitochondria and other were the animals, plants, and fungi (Copeland typical eukaryotic structures, such as peroxi- 1938; Whittaker 1969; Margulis 1971). This is somes (Keeling 1998). These phylogenies were not to say that ignored protists, and also consistent with the hypothesis, they have been in fact recognized as a which postulated that amitochondriate eukary- for more that a century (Haeckel 1866), but ote lineages diverged before the endosymbiotic protists were considered to be "simple" organ- event that gave rise to mitochondria (Cavalier- isms from which more elaborate, multicellular Smith 1983, 1987, 1989). Even more convincing species emerged. Although these early propos- was that other molecular markers, including als succeeded in recognizing several major as- various elongations factors and RNA polymer- semblages, such as animals and plants, they ase subunits, corroborated the deep-branching were less successful in resolving the relation- position of archezoan taxa, altogether sup- ships between the groups and, with the benefit porting the prediction that they should branch of hindsight, failed to account for the funda- earlier than the -containing mental paraphyletic and complex of eukaryotes if they predate the origin of this or- the protist lines. ganelle (Brown and Doolittle 1995; Klenk et al. 1995; Kamaishi et al. 1996; Yamamoto et al. 1997). A MOLECULAR (R)EVOLUTION At the other end of the tree, the so-called The backbone of the eukaryotic tree has gone crown, contain the major of eukaryotes, through some profound rearrangements in the appearing tightly bunched together as if they past 20 . Comparing or amino diverged almost simultaneously (Sogin 1991; acid sequences is now the tool of choice for re- Knoll 1992). These clades included animals, constructing evolutionary histories. This is par- fungi, and plants as well as diverse protist line- ticularly true for protists because the interpre- ages such as and (see tation of their morphological characters alone below). The branching among the SSU is problematic. For years, the go-to molecular rRNA crown taxa, however, could not be re- marker for phylogenetics has been the small solved even with the help of several subunit ribosomal RNA (SSU rRNA). It is markers (Baldauf 1999; Hirt et al. 1999; Roger

2 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

et al. 1999; Moreira et al. 2000). This lack of mo- karyotic crown, and no longer supported the lecular resolution was interpreted as evidence idea that the -to-eukaryote transi- that not enough phylogenetic signal could accu- tion was a progressive transformation involving mulate in the sequences because most phyla intermediate amitochondriate forms. emerged in a very short period of , like in More generally, the whole eukaryotic tree a “big-bang” explosion of species diversification was shaken up by important discrepancies be- (Philippe et al. 2000a,b). tween SSU rRNA-based phylogenies and those inferred from a growing number of protein- coding genes, as well as discrete molecular char- TRIMMING THE TREE acters such as shared indels (insertion/dele- The early molecular-based interpretation of tions) or fusions, or the systematic analysis the eukaryotic tree showing the archezoan- of light and data (e.g., Bal- crown dichotomy did not last very long. First, dauf and Palmer 1993; Keeling and Doolittle as more and more lineages were being se- 1996; Fast et al. 1999; Baldauf et al. 2000; Mo- quenced, mitochondriate protist groups such reira et al. 2000; Cavalier-Smith 2002; Simpson as and squeezed in 2003; Nikolaev et al. 2004; Harper et al. 2005). between the archezoan taxa and the crown (So- The integration of these various kinds of data gin et al. 1986; Clark and Cross 1988; Pawlowski led to the conception that most, if not all, eu- et al. 1996). Moreover, the archezoans were karyotic diversity can be assigned to one of sev- characterized byelevated rates of molecular evo- eral major assemblages, called “supergroups” lution, which translates into long branches in (Baldauf 2003; Keeling 2004; Simpson and Rog- phylogenetic trees (Philippe et al. 2000b). This er 2004; Adl et al. 2005; Keeling et al. 2005; meant that for these “basal” taxa, most standard Parfrey et al. 2006). In this framework, animals molecular markers such as the SSU rRNA were occupy just one branch among hundreds, and mutationally saturated, a feature that can lead are far outnumbered at the level of major line- to the notorious (LBA) ages by unicellular eukaryotes. In its original artefact in which distantly related species with form, this new tree of eukaryotes was an un- fast evolving sequences are erroneously clus- rooted polytomy with six main stems, each rep- tered together (Felsenstein 1981). Ultimately, resenting a supergroup: Opisthokonta, Amoe- new genes, more taxa, and better phylogenetic bozoa, , , and methods showed that if the archezoan taxa ap- . All six of these supergroups peared to diverge early, it was not because they emerged from a common point, and their order were “primitive” eukaryotes but rather because of divergence was mostly unknown. of their artificial attraction to the base of the tree by distant outgroups (Embley and Hirt 1998; PHYLOGENETICS þ GENOMICS ¼ Roger 1999; Baldauf et al. 2000; Philippe et al. PHYLOGENOMICS 2000a,b). At the same time, mitochondrial-de- rived genes were progressively discovered in ar- Fast forward to present day, we are well into the chezoan genomes, the products of which were genomic era and reconstructing the tree of eu- shown to be targeted to reduced double-mem- karyotes is no longer the job of a few genes. brane-bounded organelles of mitochondrial Instead, huge phylogenomic data sets contain- ancestry ( and ), ing hundreds of genes for an always-increasing suggesting that all “amitochondriate” eukary- number of taxa can now be used. The tedious otes once possessed mitochondria (Clark and and expensive Sanger of the early Roger 1995; Bui et al. 1996; Keeling 1998; Tovar 2000s (the genome cost in the range of et al. 1999, 2003; Williams et al. 2002; Embley a billion U.S. dollars) has been replaced by fast and Martin 2006; Goldberg et al. 2008; Hjort and cheap next-generation sequencing, which et al. 2010). This marked the end of both the can produce genome-scale data at unprecedent- archezoa hypothesis and the concept of a eu- ed depths for a taxonomically broad sampling.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 3 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

Once strongly biased toward organisms relevant such as saturated positions in the data set (sto- for human well-being (of economical or medi- chastic errors) or model misspecifications (sys- cal importance), there has been an explosion of tematic errors). Stochastic errors arise when the the taxonomic distribution of species for which number of positions in an alignment is small extensive genomic data are available. As of 2012, meaning that the random background noise, at least one species from each major of which inevitably accumulates through time be- eukaryotes has had its genome fully sequenced, cause of homoplasy, will have a neutralizing ef- not to mention the numerous smaller scale fect on the positions that contain the genuine genomic surveys and transcriptomic data sets phylogenetic signal. Model misspecifications that have been generated. With this wealth of leading to systematic errors include, for exam- sequence data at hand, phylogenomics started ple, the heterogeneity of nucleotide or amino off as a way to predict gene functions by evolu- acid composition, which tends to incorrectly tionary analysis in which uncharacterized genes cluster together species sharing the same com- were predicted by their phylogenetic position position, or the heterogeneity of the evolution- relative to genes with known functions (Eisen ary rates, which can result in the LBA artefact 1998). Although this area of phylogenomics is (Felsenstein 1981; Philippe 2000; Lopez et al. still very active, it also rapidly emerged as a new 2002; Foster 2004; Ho and Jermiin 2004; Jermiin of phylogenetics and became an essen- et al. 2004). tial tool for addressing controversial evolution- Logically, the goal of a phylogenetic infer- ary questions, such as the transitions that led to ence is to minimize the noise and maximize the the current diversity of eukaryotes. true phylogenetic signal (Philippe et al. 2005, In its most popular application to phyloge- 2011). Single-gene phylogenies, because of the ny, phylogenomics relies on multiple-sequence limited information they contain, are especial- alignments, much like the single-gene ap- ly susceptible to stochastic errors; to counter proach, but here the genes are often concatenat- this, the obvious solution is to gather more ed into large supermatrices (Delsuc et al. 2005). data in the hope that enough phylogenetic sig- With this approach, too, it is important to en- nal is recovered (i.e., synapomorphy will dom- sure the of the characters inate homoplasy). Systematic errors, on the oth- (orthology)—that the genes in related species er hand, tend not to vanish with the addition are inherited from a common ancestor. This is of more data as their causes do not average out not an easy task because the genes available from over longer alignments (Rodriguez-Ezpeleta genomic-scale projects are still poorly sampled, et al. 2007b). Yet, the key advantage of phyloge- substantially more so than for widely used phy- nomics is precisely that more data is available logenetic protein markers such as , a- and to start with, making it possible to apply strat- b-, or 2. egies to diminish the known sources of system- Consequently, differentiating between orthol- atic errors while still maintaining most of the ogy and, for example, the undesirable horizon- phylogenetic signal (see Delsuc et al. 2005; Phi- tally transferred genes (HGTs), independent lippe et al. 2005, 2011 for reviews). Thus, when gene losses or partially sampled genes can be combined with other options developed and difficult to achieve with a limited selec- tested on smaller data sets to increase the phy- tion. Moreover, many of the general biases that logenetic accuracy, such as the use of more ac- apply to single-gene phylogenetics are exacer- curate phylogenetic methods or better taxon bated in a phylogenomic context (Jeffroy et al. samplings, phylogenomics becomes a very pow- 2006; Rodriguez-Ezpeleta et al. 2007b; Philippe erful tool. et al. 2011). Phylogenetic reconstruction in- Phylogenomics has confirmed the existence volves two opposing forces: the true phyloge- of most supergroups, although various degrees netic signal carrying the evolutionary history, of controversy remain for each of them. The and the nonphylogenetic signals (noise) result- increased power in resolution has also led to ing from a combination of one or more causes some important shuffling among the super-

4 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

groups and allowed the placement in the tree of the amoeboid cells, evidence that they form of several “orphan” lineages. Below, in the next a monophyletic group is based on single-gene section, I briefly introduce each supergroup, phylogenies (e.g., Fahrni et al. 2003; Smirnov and discuss the eukaryote phylogeny in light et al. 2005), phylogenomics (Bapteste et al. of the most recent advances (see Fig. 1). 2002; Minge et al. 2009; Brown et al. 2012), and similarities in mitochondrial genome ar- THE EUKARYOTIC SUPERGROUPS chitecture between and Dictyos- telium (Lonergan and Gray 1996; Iwamoto et al. Opisthokonta 1998). This supergroup contains animals (Metazoa) and are often and fungi, as well as several lines of hetero- united in a larger supergroup called the uni- trophic protists. Animals emerged from within konts (Cavalier-Smith 2002) or, more recently, a paraphyletic assemblage of protists, includ- (Adl et al. 2012), which is supported ing the choanoflagellates (e.g., Monosiga), Filas- by a /fusion (Stechmann and terea (e.g., ), and Ichthyosporea (e.g., Cavalier-Smith 2002, 2003) as well as single- Sphaeroforma; Steenkamp et al. 2006; Ruiz- gene phylogenies (e.g., Baldauf and Palmer Trillo et al. 2008; Shalchian-Tabrizi et al. 2008; 1993) and phylogenomics (Rodriguez-Ezpeleta del Campo and Ruiz-Trillo 2013). Fungi, in- et al. 2007a; Hampl et al. 2009; Brown et al. cluding the monophyletic and early assemblage 2012; Derelle and Lang 2012). Amorphea also comprising Cryptomycota (e.g., ), aphe- contains protist lineages of unclear placement, lids, and microsporidians (Lara et al. 2010; such as the apusomonads, ancryomonads, Jones et al. 2011a,b; James et al. 2013; Karpov and breviate amoebae. Based on phylogenomic et al. 2013) are closely related to nucleariid analysis, opisthokonts, apusomonads, and bre- ( simplex) and the aggregative viates were recently grouped into a larger entity (Brown et al. 2009; Liu named (Brown et al. 2013). The validity et al. 2009, 2012). Opisthokonts are putative- of this assemblage, however, relies on the posi- ly united by the presence of a single posterior tion of the eukaryotic root, which remains hy- flagellum in several representatives (Cavalier- pothetical (see below). Smith and Chao 1995), and many molecular- based evidences (single-gene phylogenies, phy- Excavata logenomics, and indels) have consistently sup- ported the existence of this group (e.g., Baldauf This supergroup is composed of diverse and and Palmer 1993; Wainright et al. 1993; Baldauf mainly heterotrophic protists, many of which et al. 2000; Brown et al. 2009; Liu et al. 2009). It are anaerobes and/or parasites and possess hy- is one of the most reliable supergroups. drogenosomes or mitosomes instead of mito- chondria (e.g., , ). A group including lineages with plastids of green algal Amoebozoa origin, the (e.g., ), also belongs This supergroup includes mostly amoeboid, to this assemblage. Excavates were originally heterotrophic protists such as the classical na- proposed based on a distinctive feeding groove ked and testate lobose amoebae with broad supported by a particular set of cytoskeletal fea- pseudopods (e.g., Amoeba), but also contains tures that are found in some, but not all, of these some amitochondriate parasitic lineages of crit- organisms (Simpson 2003). A strong molecular ical medical importance (e.g., ), fla- confirmation of this grouping is currently lack- gellated cells (e.g., , ), ing, which is at least, in part, attributable to the or the mycetozoan slime molds capable of ag- high rates of sequence evolution of most of its gregative multicellularity (e.g., ; putative constituent lineages. Single-gene phy- see Pawlowski and Burki 2009 for a recent re- logenies (e.g., Kolisko et al. 2008; Takishita et al. view). In addition to morphological similarities 2012) and phylogenomics (Rodriguez-Ezpeleta

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 5 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

Cryptophytes Cyanidiophytes Bangiophytes Palpitomonas Floridiophytes Trebouxiophytes Telonemids Chlorophyceans Rappemonads Ulvophytes Prasinophytes s e Zygnemophyceans k c ti Charophyceans e r Red o h algae Angiosperms p Vitrella ia D Green Colpodellids plants Kinetoplastids Chromera Diplonemids Colponemids Alveolates Euglenids Heteroloboseans Bicosoecids Labyrinthulids Archaeplastida Thraustochytrids Excavates Opalinids Diplomonads Actinophryids Stramenopiles Phaeophytes Dictyochophytes Opisthokonts Zygomycetes Pelagophytes SAR Ascomycetes Fungi Basidiomycetes Pinguiophytes Chytrids Chrysophytes Cryptomycota Nucleariids Fonticula Cercomonads Rhizaria Ichthyosporea Euglyphids Animals Thaumatomonads Amoebozoa Porifera Coelenterata Paradinium Haplosporidia ea Ancyromonads ph or Apusomonads Am Foraminifera Arcellinids Archamoebae Tubulinids Vannellids Leptomyxids Dactylopodids Acanthomyxids

Figure 1. Global tree of eukaryotes from a consensus of phylogenetic evidence (in particular, phylogenomics), rare genomic signatures, and morphological characteristics. Numerous eukaryotic groups are shown (not exhaustively), regardless of their . Cartoons illustrate the diversity constituting the largest assemblages (colored boxes). The branching pattern does not necessarily represent the inferred relationships between the lineages. Dotted lines denote uncertain relationships, including conflicting positions. Note the solid branch leading to haptophytes and rappemonads: This illustrates the strong support for placing haptophytes as sister to SAR(stramenopiles, alveolates, and Rhizaria) in a recent study (Burki et al. 2012b), but this lineage is not included in a colored assemblage because confirmation is needed. The arrows point to possible positions for the eukaryotic root; the solid arrow corresponds to the most popular hypothesis (Amorphea- rooting), the broken arrows represent the alternative hypotheses discussed in the text. (This figure was inspired by a template provided by Y. Eglit.)

et al. 2007a; Hampl et al. 2009) have generally Archaeplastida (Plantae) recovered the of the group when the fast-evolving taxa are excluded, but some This supergroup is composed of the three main lineages, such as Malawimonas, have eluded ro- lineages of primary photosynthetic taxa: organ- bust placement (Hampl et al. 2009; Zhao et al. isms that harbor plastids directly derived from 2012). the cyanobacterial endosymbiosis. (1) The glau-

6 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

cophytes (e.g., Cyanophora) are a small group opposing flagella with tripartite flagellar hairs of enigmatic freshwater microscopic algae with (mastigonemes) on the forward flagellum, but uniquely cyanobacterial-like plastids (they have also include many lineages that lost one or both retained the prokaryotic layer flagella (Cavalier-Smith 1986). They are well between the two membranes). (2) The supported by molecular data (Ben Ali et al. (rhodophytes) form a diverse group of 2002; Cavalier-Smith and Chao 2006; Riisberg unicellular algae and large , for exam- et al. 2009). Alveolates are also extremely di- ple, the Porphyra commonly used to wrap verse, notably including the dinoflagellate algae, sushi (nori). (3) The “green” organisms (Viri- but also apicomplexan parasites such as the ma- diplantae), including the , with laria agent or protozoans mostly free-living unicellular (e.g., Chlamydo- (e.g., ). The cortical alveoli, a sys- ) and colonial or multicellular taxa (e.g., tem of vesicles supporting the plasma mem- , Caulerpa), but nonphotosynthetic para- brane, constitute a morphological synapomor- sitic taxa (e.g., Prototheca, Helicosporidum), are phy for the alveolates (Cavalier-Smith 1991). also known, as well as the land plants (, Molecular phylogenies strongly support the , angiosperms, etc.). Single-gene phyloge- monophyly of alveolates (e.g., Fast et al. 2002; nies and phylogenomics of plastid genes have Harper et al. 2005). Rhizaria is based on molec- strongly supported a common origin of the ular characters only (e.g., Keeling 2001; Archi- primary plastids in the ancestor of Archae- bald et al. 2003; Nikolaev et al. 2004; Bass et al. plastida (Chu et al. 2004; Hagopian et al. 2004; 2005; Burki and Pawlowski 2006; Burki et al. Rodriguez-Ezpeleta et al. 2005). 2010; Brown et al. 2012; Sierra et al. 2013). also supports a unique endosymbiosis with It includes naked and testate amoeboid, het- a shared plastid protein import machinery erotrophic protists with filose or reticulose (Palmer 2003; McFadden and van Dooren pseudopods such as foraminiferans and radio- 2004; Price et al. 2012). Nuclear phylogenies larians. Some rhizarians are photosynthetic, are less supportive (Moreira et al. 2000; Rodri- including lineages in the euglyphids (e.g., Pau- guez-Ezpeleta et al. 2005; Nozaki et al. 2007, linella) and chlorarachniophytes (e.g., Bigelo- 2009), but this supergroup is generally widely wiella). A large diversity of free-living flagellates recognized. and amoeboflagellates, sorocarpic (e.g., Guttu- linopsis), and parasite protists also belong to this group (see Pawlowski and Burki 2009 for SAR a review). One enigmatic parasite, Mikrocytos This vast assemblage is the most recently recog- mackini, which infects and kills , was re- nized supergroup and, contrary to the other cently shown to belong to Rhizaria and attracted supergroups, its existence is exclusively sup- attention because it likely possesses highly re- ported by molecular data (i.e., phylogenomic duced mitochondrion-derived (Burki analyses (Burki et al. 2007, 2008; Hackett et et al. 2013). al. 2007; Rodriguez-Ezpeleta et al. 2007a) and a derived RAB1 paralog (Elias et al. 2009). It THE RISE OF SAR was originally named SAR as an acronym of its constituents: stramenopiles, alveolates, and Before being members of SAR, stramenopiles Rhizaria (Burki et al. 2007). Stramenopiles and alveolates were part of another supergroup, (also known as ) embrace a very chromalveolates, which has played a central large diversity of protists, including, for exam- role in shaping our understanding of eukaryotic ple, ecologically important algal groups such as evolution, particularly the origin and spread of diatoms or large multicellular seaweeds (e.g., secondary plastids of red algal origin (Keeling ), as well as heterotrophic, often parasitic 2009). In addition to stramenopiles and alve- species such as oomycetes and Blastocystis. Stra- olates, the four original constituent chromal- menopiles are typically characterized by two veolate lineages also included two important

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 7 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

protist groups: haptophytes and nouskovec et al. 2010). Early nuclear phyloge- (Keeling 2004; Reyes-Prieto et al. 2007). Al- nies based on single genes also recovered a close though many of these lineages are nonphoto- association between alveolates and strameno- synthetic or lack plastid altogether, the rational piles (Van de Peer et al. 1996; Harper et al. for grouping them into a monophyletic entity 2005). Phylogenomics largely confirmed this was based on the idea that the plastids of the observation and, at the same time, produced chromalveolate taxa, which all share chloro- trees in which haptophytes and cryptomonads phyll c, can be traced back to a single endosym- shared a common ancestor, congruent with the biotic event with a red alga (Cavalier-Smith plastid topology (Hackett et al. 2007; Patron 1999). Under this hypothesis, the secondary et al. 2007; Burki et al. 2009). This latter asso- red plastid origin is unique and took place in ciation was also supported by a unique shared the chromalveolate ancestor, and the numerous insertion of a laterally transferred gene nonphotosynthetic lineages scattered among into the plastids of haptophytes and cryptomo- the chromalveolate tree were inferred to have nads (Rice and Palmer 2006), which led some to lost their plastid and/or (Cava- propose the name to accommodate lier-Smith 1999). However, because of the ab- the body of evidence in favor of a common or- sence of integrative molecular evidence sup- igin between these two groups (Okamoto et al. porting it, the chromalveolates have long been 2009). a controversial supergroup and it was recently However, what appeared to be a consistent remodeled in such a way that it has disappeared scenario rapidly became challenged by the ac- from the current consensus of the eukaryotic cumulating genetic data from diverse species tree (Fig. 1) (Adl et al. 2012; Keeling 2013; Paw- as well as evidence against the monophyly of lowski 2013). its original constituents. First, several phyloge- In phylogenetic terms, one condition of the nomic studies showed that Rhizaria branched chromalveolate hypothesis is that both the plas- together with alveolates and stramenopiles (the tid and (i.e., nuclear) trees must be consis- SAR group) to the exclusion of haptophytes and tent in showing the monophyly of alveolates, cryptomonads, whose exact positions remained stramenopiles, haptophytes, and cryptomo- unresolved (Burki et al. 2007, 2008, 2009; Hack- nads. From the plastid side, the monophyly ett et al. 2007; Rodriguez-Ezpeleta et al. 2007a). has usually been recovered for three of these This was significant because Rhizaria include groups (Yoon et al. 2002; Khan et al. 2007). mostly heterotrophic groups and only two Alveolates, however, have proven nearly impos- known photosynthetic lineages (chlorarachnio- sible to fit into this molecular framework be- phytes and ), neitherof which possess- cause their plastid genomes are generally highly es plastids of red algal origin. Thus, under the reduced, providing only few genes for compar- chromalveolate hypothesis, the SAR relation- ative analyses (Ko¨hler et al. 1997; Green 2004). ships imply that the ancestor of Rhizaria had But this was before the recent unexpected dis- a red-algal-derived plastid, which was lost be- covery of deep-branching relatives of apicom- fore their diversification. At first glance, this plexans (e.g., Chromera, Vitrella) (Moore et al. might not substantially alter the chromalveo- 2008), members of alveolates, which possess late hypothesis: Regardless of how many species more gene-rich plastid genomes (Janouskovec belong to Rhizaria, only one more loss of an et al. 2010). When the genomes of these species ancestral red plastid (out of many genuinely as- were compared to those of other chromalveo- sumed) is required to explain the current plastid lates, the tree that emerged showed a robust distribution, provided that SAR is closely related union between the and to Hacrobia. plastids, and recovered the global monophyly of In addition to Rhizaria, however, phyloge- the red plastids also including haptophytes and netic analyses showed that several other het- cryptomonads (which were most closely related erotrophic lineages were linked to the chromal- to each other), albeit with lower support (Ja- veolates, further challenging the hypothesis.

8 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

Specifically, telonemids, centrohelids, katable- al. 2010). Altogether, these observations have pharids, and picobiliphytes (now Picozoa) (See- forged the basis for alternative scenarios to the nivasan et al. 2013)have all been inferred as sister chromalveolate hypothesis: scenarios in which to either haptophytes or cryptomonads (Shal- red plastids spread across the tree not by means chian-Tabrizi et al. 2006; Not et al. 2007; Burki of vertical inheritance, but through more com- et al. 2009), but these associations are generally plex serial eukaryote-to-eukaryote endosymbi- poorly resolved, with the exception of katable- oses (Lane and Archibald 2008; Sanchez Puerta pharids, which is robustly related to cryptomo- and Delwiche 2008; Archibald 2009; Bodyl et al. nads (Okamoto and Inouye 2005; Burki et al. 2009; Baurain et al. 2010; Dorrell and Smith 2012b). Nevertheless, the addition of new plas- 2011). tid-lacking lineages compromised both the ha- crobian and chromalveolate hypotheses because DIGGING FOR THE ROOT both are based on a common plastid origin (Cavalier-Smith 1999; Okamoto et al. 2009). In addition to improving the resolution of the Proponents of the chromalveolate hypothesis, eukaryotic tree, knowing precisely where the however, can always put forward the argument root lies is essential to give directionality to evo- of plastid loss to explain these relationships, an lution and go beyond the classical star-like rep- argument that is difficult to refute until the prev- resentation of the supergroups. This funda- alence of plastid loss among eukaryotes is better mental issue has proven extremely difficult to understood. tackle because it refers to a prohibitively ancient More problematic is evidence calling into event: the last eukaryotic common ancestor. question the existence of Hacrobia; in contrast The position of the root is generally considered to earlier reports, a recent phylogenomic study unresolved, but a few hypotheses have emerged. did not recover the association between hapto- The most straightforward approach to root a phytes and cryptomonads, but instead showed phylogenetic tree is to use an outgroup, which haptophytes branching closer to SAR, whereas often consists of one or several lineages known cryptomonads were sister to Archaeplastida to stem from the base of the group of interest. (Burki et al. 2012b). These relationships were In the case of eukaryotes, one possible outgroup generally weakly supported, in particular, the is to be found within . This is prob- position of cryptomonads, and thus require lematic because even the closest prokaryotic further testing before one can safely dismantle outgroup (Archaebacteria) represents a consid- theHacrobiahypothesis.But,byrecoveringcryp- erable evolutionary distance from eukaryotes, tomonads distantly related to SAR and hap- which could potentially lead to the LBA arte- tophytes, this study shifted attention on the fact (Felsenstein 1981). If fact, analyses includ- position of this group as key to infer red plastid ing prokaryotes usually produced suspicious evolution (Burki et al. 2012b). Indeed, if the phylogenies in which the fastest evolving eu- -Archaeplastida grouping is con- karyotes branched off close to the base of the firmed, it would not only invalidate the con- tree, attracted to the distant outgroup (Philippe dition of a shared origin between all chromal- et al. 2000b; Ciccarelli et al. 2006; Williams et al. veolate lineages in both nuclear and plastid 2012). phylogenies, it would also conflict with plastid To reduce the outgroup-to-ingroup dis- phylogenies that strongly group haptophytes tance, some researchers have used genes derived and cryptomonads (Janouskovec et al. 2010). from the a-proteobacterium endosymbiotic Furthermore, a study evaluating the phyloge- progenitor of mitochondria (Derelle and Lang nomic signal across the three genomic compart- 2012). This analysis placed the eukaryotic root ments (nuclear, plastid, and mitochondrial) in between unikonts and everything else (often re- chromalveolate taxa reported discrepancies too ferred to as ) (Cavalier-Smith 2002), high to be explained by a common origin of supporting what is perhaps the most prevailing both the plastid and host lineages (Baurain et view for the original bifurcation in the eukary-

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 9 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

otic tree. Two rare genomic changes have also tochondria encounter structure, which tethers supported the basal unikont–bikont split: (1) mitochondria to the ER membrane, showed unikonts have ancestral, bacterial-like dihydro- that the root is most consistently placed be- folate reductase (DHFR) and thymidylate syn- tween Amorphea þ excavates and all other thase (TS) genes, whereas bikonts have derived eukaryotes (Wideman et al. 2013). Researchers and fused version of these two genes (Philippe investigating a new of rare genomic chang- et al. 2000b; Stechmann and Cavalier-Smith es involving multiple, conserved 2002, 2003); and (2) unikonts have a unique residues inferred the initial split in eukaryote insertion to class II, whereas evolution between Archaeplastida and every- this paralog is absent from bikonts (Richards thing else (Rogozin et al. 2009). A different ap- and Cavalier-Smith 2005). Following a parsi- proach showed that by minimizing the number monious argumentation, these two signatures of gene duplications and loss across 20 genes, were taken as evidence for the monophyly of the most parsimonious root was found to lie in- unikonts and bikonts, and a root position out- between opisthokonts and the rest of eukaryotes side of both groups. The unikont–bikont bifur- (Katz et al. 2012). In yet another scenario, the cation was proposed to coincide with a funda- root was proposed to be deep within excavates mental difference of the flagellar apparatus: (thus invalidating the monophyletic origin of unikonts have retained the ancestral organiza- this supergroup), possibly between Euglenozoa tion with one anchoring one flagel- and all other eukaryotes, based on the absence lum, whereas bikonts are ancestrally biflagellated of the mitochondrial outer-membrane chan- with two basal bodies (Cavalier-Smith 2002; nel Tom40 and the DNA replication origin-rec- Stechmann and Cavalier-Smith 2002, 2003). ognition complexes, both ancestral bacterial However, the sequencing of new enigmatic features (Cavalier-Smith 2010b). Most recent- lineages has repetitively challenged the unikont- ly, the use of 37 nuclear-encoded of bikont bifurcation. For example, although the close bacterial ancestry, most of which are of protistean apuzomonads (e.g., Thecamonas)are mitochondrial function, positioned the root be- by essence bikonts (with two basal bodies and tween excavates and the rest of eukaryotes (He two flagella) and possess the fused TS-DHFR, et al. 2014). The list of hypotheses goes on, and they were shown to be related to unikonts (Kim it may be some time before the root is dug out, et al. 2006; Brown et al. 2012; Derelle and Lang but when its position is revealed with more con- 2012). Similarly, the breviate amoeba (e.g., Bre- sistency, it will have a fundamental impact on viata), which harbors two basal bodies (but only our understanding of how the eukaryotic super- one flagellum), turned out to be a deep-branch- groups relate to one another. ing unikont (Minge et al. 2009; Roger and Simpson 2009; Brown et al. 2013). These data DEEP RELATIONSHIPS AMONG suggest that the true unikonts, in addition to EUKARYOTES some protists not fitting with the original de- scription of a monoflagellated ancestry and sep- In an attempt to best reflect the current view arate TS and DHFR genes, may form a , of eukaryotic relationships, I present a rooted but it seems increasingly untenable that this tree with the origin of eukaryotes between group was ancestrally unikont with one basal Amorphea and everything else, but also indi- body. To formalize this taxon without reflecting cate five alternative rooting positions (Fig. 1). the controversial ancestral state, the name Amorphea includes opisthokonts, Amoebozoa, Amorphea was recently introduced (Adl et al. and several protist lineages of uncertain phylo- 2012). genetic placement, such as apusomonads, an- Other analyses have further exacerbated the cryomonads, and the breviate amoebae. (Heiss uncertain position of the eukaryotic root. Re- et al. 2011; Katz et al. 2011; Brown et al. 2013). cently, a study looking at the taxonomic distri- The rest of eukaryotes comprises excavates and bution of the (ER)-mi- the recently erected mega-clade Diaphoretickes

10 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

(Adl et al. 2012), which recognizes the SAR and CONCLUDING REMARKS Archaeplastida clade (Burki et al. 2008) and cor- responds to the corticates of Cavalier-Smith Over the last 10 years, phylogenomics has led to (2010a). Other lineages, such as important refinements of the global tree of eu- haptophytes,cryptomonads,katablepharids,te- karyotes. Most of the large building blocks of lonemids, centrohelids, Rappemonads, and Pal- the tree (the supergroups) predating the geno- pitomonas, may also belong to Diaphoretickes, mic era have been reinforced by the analyses of as compiled from several phylogenetic results larger data sets, but some were also shuffled into (Rodriguez-Ezpeleta et al. 2007a; Burki et al. different arrangements. The increased phyloge- 2009; Hampl et al. 2009; Yabuki et al. 2010; netic power of phylogenomics helped resolve Kim et al. 2011; Brown et al. 2012). The branch- the relationships between the supergroups, pro- ing pattern within Diaphoretickes is generally viding new hypotheses for the deep backbone of poorly resolved, but haptophytes may be sister the tree. It also allowed the placement of orphan to SAR (Burki et al. 2012b). The position of taxa that had eluded proper classification until cryptomonads, although ambiguous, has re- more data became available. At the same time, cently shown affinities to Archaeplastida (Burki new challenges have appeared and several key et al. 2012b). The other lineages have failed to lineages remain of unknown evolutionary ori- show reliable phylogenetic placement and re- gin. It is clear that the dawn of eukaryote evo- main enigmatic. lution and subsequent diversification will not With this evolutionary framework in mind, be fully understood until these enigmatic line- one group, Collodictyon, stands out as particu- ages find a home and the root of the tree is larly remarkable. Collodictyon is an omnivorous characterized. What’s more, as we explore incer- amoeboflagellated cell with a mysterious posi- tae sedis taxa, classical microscopy as well as tion in the tree of eukaryotes. It possesses an next-generation environmental surveys and sin- eclectic mix of cellular features, such as a ventral gle-cell genomics will undoubtedly reveal new feeding groove typical of excavates and amoebo- essential protist taxa. But the exciting news is: zoan-like pseudopods, which make pinpoint- Technological advancements such as sequenc- ing its phylogenetic position difficult but desir- ing preparation from nano-quantities of mate- able (Klaveness 1995; Brugerolle et al. 2002). rial now allow one to tackle these taxa from a When its position was investigated using a large genomic perspective, even when cell cultures phylogenomic data set, Collodictyon branched cannot be established (Yoon et al. 2011). off early in eukaryote evolution, close to the Resolving the tree of eukaryotes will ne- Amorphea-bikont bifurcation (Fig. 1), suggest- cessitate continuing the integrative approach ing that its morphological characteristics may blending morphology, single-gene phylogeny, represent some of the ancestral conditions of and phylogenomics including all diversity. It the eukaryotic cell (Zhao et al. 2012). With the will also require more reliable ways of assem- potential exception of the contentious excavate bling genomic data and the development of Malawimonas, which has proven impossible to new methods to extract the phylogenetic infor- unambiguously assign to any large group of eu- mation contained in these genomes. Impor- karyotes and showed affinities to Collodictyon, tantly, the pervasiveness of HGT in eukaryotes, this branch of the eukaryotic tree is known to in particular, the genes transferred from plastids include onlyone other genus (), aview (endosymbiotic gene transfer), will need to be supported by observations of very low genetic systematically evaluated. Presently, the fierce de- diversity of Collodictyon-like sequences in envi- bate over the global impact of HGTon eukary- ronmental surveys (Zhao et al. 2012). Given a ote evolution and its harmful consequences on root as in Figure 1, this group may represent the phylogenomics is far from a consensus (Mou- first confirmed case of a lineage that diverged stafa et al. 2009; Stiller 2011; Burki et al. 2012a; after the Amorphea-bikont split, but before the Chan et al. 2012; Deschamps and Moreira subsequent diversification of these two groups. 2012). Eukaryote evolution started off more

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 11 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

than a billion years ago and reconstructing the Philippe HH. 2010. Phylogenomic evidence for separate twists and turns that led to the diversity we ob- acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27: 1698–1709. serve today is a tremendously difficult task, but Ben Ali A, De Baere R, De Wachter R, Van de Peer Y. 2002. a task that is both fascinating and on its way to Evolutionary relationships among algae (the be deciphered. autotrophic stramenopiles) based on combined analyses of small and large subunit ribosomal RNA. Protist 153: 123–132. Bodyl A, Stiller JW, Mackiewicz P. 2009. Chromalveolate ACKNOWLEDGMENTS plastids: Direct descent or multiple endosymbioses? Trends Ecol Evol 24: 1–119; author reply 121–122. I express my deepest gratitude to Yana Eglit, Brown JR, Doolittle WF. 1995. Root of the universal tree of Thierry Heger, Jan Pawlowski, David Smith, life based on ancient aminoacyl-tRNA synthetase gene and Barbara Yermen for critical and construc- duplications. Proc Natl Acad Sci 92: 2441–2445. tive reading of an earlier version of this manu- Brown MW, Spiegel FW, Silberman JD. 2009. Phylogeny of script. My research is supported by a grant from the “forgotten” cellular slime mold, Fonticula alba, re- veals a key evolutionary branch within Opisthokonta. the Tula Foundation to the Centre for Microbial Mol Biol Evol 26: 2699–2709. Diversity and Evolution. Brown MW, Kolisko M, Silberman JD, Roger AJ. 2012. Ag- gregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22: 1123– REFERENCES 1127. Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang F, Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson Simpson AG, Roger AJ. 2013. Phylogenomics demon- OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, strates that breviate flagellates are related to opishokonts Fredericq S, et al. 2005. The new higher level classification and apusomonads. Proc Biol Sci 280: 20131755. of eukaryotes with emphasis on the of protists. Brugerolle G, Bricheux G, Philippe HH, Coffe G. 2002. J Eukaryot Microbiol 52: 399–451. Collodictyon triciliatum and (¼ Adl SM, Simpson AG, Lane CE, Lukes J, Bass D, Bowser SS, Aulacomonas submarina) form a new familyof flagellates Brown MW, Burki F, Dunthorn M, Hampl V, et al. 2012. () with tubular mitochondrial cristae The revised classification of eukaryotes. J Eukaryot Micro- that is phylogenetically distant from other flagellate biol 59: 429–514. groups. Protist 153: 59–70. Archibald JM. 2009. The puzzle of plastid evolution. Curr Bui ET,Bradley PJ, Johnson PJ. 1996. A common evolution- Biol 19: R81–R88. ary origin for mitochondria and hydrogenosomes. Proc Archibald JM, Longet D, Pawlowski J, Keeling PJ. 2003. A Natl Acad Sci 93: 9651–9656. novel polyubiquitin structure in and Forami- Burki F, Pawlowski J. 2006. Monophyly of Rhizaria and nifera: Evidence for a new eukaryotic supergroup. Mol multigene phylogeny of unicellular bikonts. Mol Biol Biol Evol 20: 62–66. Evol 23: 1922–1930. Baldauf SL. 1999. A search for the origins of animals and Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Ni- fungi: Comparing and combining molecular data. Am kolaev SI, Jakobsen KS, Pawlowski J. 2007. Phylogenom- Nat 154: S178–S188. ics reshuffles the eukaryotic supergroups. PLoS ONE 2: Baldauf SL. 2003. The deep of eukaryotes. Science 300: e790. 1703–1706. Burki F, Shalchian-Tabrizi K, Pawlowski J. 2008. Phyloge- Baldauf SL, Palmer JD. 1993. Animals and fungi are each nomics reveals a new “megagroup” including most pho- other’s closest relatives: Congruent evidence from multi- tosynthetic eukaryotes. Biol Lett 4: 366–369. ple proteins. Proc Natl Acad Sci 90: 11558–11562. Burki F, Inagaki Y, Bra˚te J, Archibald JM, Keeling PJ, Cava- Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle W. 2000. A lier-Smith TT, Sakaguchi M, Hashimoto T, Horak A, Ku- kingdom-level phylogeny of eukaryotes based on com- mar S, et al. 2009. Large-scale phylogenomic analyses bined protein data. Science 290: 972–977. reveal that two enigmatic protist lineages, Bapteste E, Brinkmann H, Lee JA, Moore DV, Sensen CW, and centroheliozoa, are related to photosynthetic chro- Gordon P,Durufle´ L, Gaasterland T,Lopez P,Mu¨ller M, et malveolates. Genome Biol Evol 1: 231–238. al. 2002. The analysis of 100 genes supports the grouping Burki F,Kudryavtsev A, Matz MV,Aglyamova GV,Bulman S, of three highly divergent amoebae: Dictyostelium, Ent- Fiers M, Keeling PJ, Pawlowski J. 2010. Evolution of Rhi- amoeba, and . Proc Natl Acad Sci 99: zaria: New insights from phylogenomic analysis of un- 1414–1419. cultivated protists. BMC Evol Biol 10: 377. Bass D, Moreira D, Lo´pez-Garcı´a P,Polet S, Chao EE, von der Burki F, Flegontov P, Obornik M, Cihlar J, Pain A, Lukes J, Heyden S, Pawlowski J, Cavalier-Smith T. 2005. Poly- Keeling PJ. 2012a. Reevaluating the green versus red sig- insertions and the phylogeny of Cercozoa and nal in eukaryotes with secondary plastid of red algal or- Rhizaria. Protist 156: 149–161. igin. Genome Biol Evol 4: 626–635. Baurain D, Brinkmann H, Petersen J, Rodriguez-Ezpeleta N, Burki F, Okamoto N, Pombert J-FF, Keeling PJ. 2012b. The Stechmann A, Demoulin V,Roger AJ, Burger G, Lang BF, evolutionary history of haptophytes and cryptophytes:

12 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

Phylogenomic evidence for separate origins. Proc R Soc clear genome from the microsporidian Encephalitozoon Lond B Biol Sci 279: 2246–2254. intestinalis. Nat Commun 1: 77. Burki F, Corradi NN, Sierra R, Pawlowski J, Meyer GR, Ab- del Campo J, Ruiz-Trillo I. 2013. Environmental survey bott CL, Keeling PJ. 2013. Phylogenomics of the intracel- meta-analysis reveals hidden diversity among unicellular lular parasite Mikrocytos mackini reveals evidence for a opisthokonts. Mol Biol Evol 30: 802–805. in rhizaria. Curr Biol 23: 1541–1547. Delsuc F,Brinkmann H, Philippe HH. 2005. Phylogenomics Cavalier-Smith T. 1983. A 6 kingdom classification and a and the reconstruction of the tree of life. Nat Rev Genet 6: unified phylogeny (ed. Schwemmler W, Schenk HEA). 361–375. De Gruyter, Berlin. Derelle R, Lang BF. 2012. Rooting the eukaryotic tree with Cavalier-Smith T.1986. The Kingdom : Origin and mitochondrial and bacterial proteins. Mol Biol Evol 29: systematics (ed. Round FE, Chapman DJ). Biopress, Bris- 1277–1289. tol, UK. Deschamps P,Moreira D. 2012. Reevaluating the green con- Cavalier-Smith T. 1987. Eukaryotes with no mitochondria. tribution to genomes. Genome Biol Evol 4: 795– Nature 326: 332–333. 800. Cavalier-Smith T. 1989. Molecular phylogeny. Archaebacte- Dorrell RG, Smith AG. 2011. Do red and green make ria and Archezoa. Nature 339: l00–l01. brown?: Perspectives on plastid acquisitions within chro- Cavalier-Smith T. 1991. Cell diversification in heterotrophic malveolates. Eukaryot Cell 10: 856–868. flagellates (ed. Patterson DJ, Larsen D). Clarendon, Douglas SE, Zauner S, Fraunholz M, Beaton M, Penny S, Oxford. Deng LT, Wu X, Reith M, Cavalier-Smith T, Maier UG. 2001. The highly reduced genome of an enslaved algal Cavalier-Smith T. 1999. Principles of protein and tar- nucleus. Nature 410: 1091–1096. geting in secondary : Euglenoid, dinofla- gellate, and sporozoan plastid origins and the eukaryote Eisen JA. 1998. Phylogenomics: Improving functional pre- family tree. J Eukaryot Microbiol 46: 347–366. dictions for uncharacterized genes by evolutionary anal- ysis. Genome Res 8: 163–167. Cavalier-Smith T.2002. The phagotrophic origin of eukary- otes and phylogenetic classification of . Int J Syst Elias M, Patron NJ, Keeling PJ. 2009. The RAB family Evol Micr 52: 297–354. GTPase Rab1A from defines a unique paralog shared by chromalveolates and rhizaria. J Cavalier-Smith T. 2010a. Deep phylogeny, ancestral groups Eukaryot Microbiol 56: 348–356. and the four ages of life. Philos Trans R Soc Lond B Biol Sci 365: 111–132. Embley TM, Hirt RP. 1998. Early branching eukaryotes? Curr Opin Genet Dev 8: 624–629. Cavalier-Smith T. 2010b. Kingdoms Protozoa and Chro- mista and the eozoan root of the eukaryotic tree. Biol Embley TM, Martin WF.2006. Eukaryotic evolution, chang- Lett 6: 342–345. es and challenges. Nature 440: 623–630. Cavalier-Smith T, Chao EE. 1995. The Opalozoan Apuso- Fahrni JF, Bolivar I, Berney C, Nassonova E, Smirnov A, monas is related to the common ancestor of animals, Pawlowski J. 2003. Phylogeny of lobose amoebae based on actin and small-subunit ribosomal RNA genes. Mol fungi, and choanoflagellates. Proc R Soc Lond B Biol Sci Biol Evol 20: 1881–1886. 261: 1–6. Fast NM, Logsdon JM, Doolittle W. 1999. Phylogenetic Cavalier-Smith T, Chao EE. 2006. Phylogeny and megasys- analysis of the TATA box binding protein (TBP) gene tematics of phagotrophic heterokonts (kingdom Chro- from Nosema locustae: Evidence for a microsporidia- mista). J Mol Biol 62: 388–420. fungi relationship and spliceosomal loss. Mol Chan CX, Soares MB, Bonaldo MF, Wisecaver JH, Hackett Biol Evol 16: 1415–1419. JD, Anderson DM, Erdner DL, Bhattacharya D. 2012. Fast NM, Xue L, Bingham S, Keeling PJ. 2002. Re-examining Analysis of Alexamdrium tamarense () alveolate evolution using multiple protein molecular genes reveals the complex evolutionary history of a mi- phylogenies. J Eukaryot Microbiol 49: 30–37. crobial eukaryote. J Phycol 48: 1130–1142. Felsenstein J. 1981. Evolutionary trees from DNA sequences: Chu KH, Qi J, Yu Z, Anh V. 2004. Origin and phylogeny of A maximum likelihood approach. J Mol Biol 17: 368– chloroplasts revealed by a simple correlation analysis of 376. complete genomes. Mol Biol Evol 21: 200–206. Foster PG. 2004. Modeling compositional heterogeneity. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Syst Biol 53: 485–495. Bork P.2006. Toward automatic reconstruction of a high- ly resolved tree of life. Science 311: 1283–1287. Friedman S, Debrunner-Vossbrinck B, Woese CR. 1987. Ri- bosomal RNA sequence suggests microsporidia are ex- Clark CG, Cross GA. 1988. Small-subunit ribosomal RNA tremely ancient eukaryotes. Nature 326: 411–414. sequence from gruberi supports the polyphy- Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, Mc- letic origin of . Mol Biol Evol 5: 512–518. Fadden GI. 2006. Complete nucleotide sequence of the Clark CG, Roger AJ. 1995. Direct evidence for secondary : Nature’s smallest nu- loss of mitochondria in . Proc cleus. Proc Natl Acad Sci 103: 9566. Natl Acad Sci 92: 6518–6521. Goldberg AV,Molik S, Tsaousis AD, Neumann K, Kuhnke G, Copeland H. 1938. The kingdoms of organisms. Q Rev Biol Delbac F, Vivare`s CP, Hirt RP, Lill R, Embley TM. 13: 383–420. 2008. Localization and functionality of microsporidian Corradi NN, Pombert J-FF,Farinelli L, Didier ES, Keeling PJ. iron-sulphur cluster assembly proteins. Nature 452: 624– 2010. The complete sequence of the smallest known nu- 628.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 13 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

Green BR. 2004. The genome of dinoflagel- forms redefines the fungal tree of life. Nature 474: 200– lates—A reduced instruction set? Protist 155: 23–31. 203. Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Ru¨mmele SE, Jones MD, Richards TA, Hawksworth DL, Bass D. 2011b. Bhattacharya D. 2007. Phylogenomic analysis supports Validation and justification of the name Crypto- the monophyly of cryptophytes and haptophytes and mycota phyl. nov. IMA 2: 173–175. the association of rhizaria with chromalveolates. Mol Kamaishi T, Hashimoto T, Nakamura Y, Nakamura F, Mu- Biol Evol 24: 1702–1713. rata S, Okada N, Okamoto K, Shimizu M, Hasegawa M. Haeckel E. 1866. Generelle Morphologie der Organismen. 1996. Protein phylogeny of translation elongation factor Reimer, Berlin. EF-1a suggests microsporidians are extremely ancient Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oli- eukaryotes. J Mol Biol 42: 257–263. veira MC. 2004. Comparative analysis of the complete Karpov SA, Mikhailov KV, Mirzaeva GS, Mirabdullaev IM, plastid genome sequence of the red alga Gracilaria ten- Mamkaeva KA, Titova NN, Aleoshin VV.2013. Obligate- uistipitata var. liui provides insights into the evolution of ly phagotrophic aphelids turned out to branch with the rhodoplasts and their relationship to other plastids. J Mol earliest-diverging fungi. Protist 164: 195–205. Biol 59: 464–477. Katz LA, Grant J, Parfrey LW, Gant A, O’Kelly CJ, Anderson Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson OR, Molestina RE, Nerad T. 2011. Subulatomonas tetra- AGB, Roger AJ. 2009. Phylogenomic analyses support spora nov. gen. nov. sp. is a member of a previously the monophyly of Excavata and resolve relationships unrecognized major clade of eukaryotes. Protist 162: among eukaryotic “supergroups.” Proc Natl Acad Sci 762–773. 106: 3859–3864. Katz LA, Grant JR, Parfrey LW, Burleigh JG. 2012. Turning Harper JT,WaandersE, Keeling PJ. 2005. On the monophyly the crown upside down: Gene tree parsimony roots the of chromalveolates using a six-protein phylogeny of eu- eukaryotic tree of life. Syst Biol 61: 653–660. karyotes. Int J Syst Evol Micr 55: 487–496. Keeling PJ. 1998. A kingdom’s progress: Archezoa and the He D, Fiz-Palacios O, Fu C-J, Fehling J, Tsai C-C, Baldauf SL. origin of eukaryotes. Bioessays 20: 87–95. 2014. An alternative root for the eukaryote tree of life. Keeling PJ. 2001. Foraminifera and Cercozoa are related in Curr Biol 24: 465–470. actin phylogeny: Two orphans find a home? Mol Biol Evol Heiss AA, Walker G, Simpson AGB. 2011. The ultrastructure 18: 1551–1557. of , a eukaryote without supergroup affin- ities. Protist 162: 373–393. Keeling PJ. 2004. Diversity and evolutionary history of plas- tids and their hosts. Am J Bot 91: 1481–1493. Hirt RP, Logsdon JM, Healy B, Dorey MW, Doolittle W, Embley TM. 1999. Microsporidia are related to Fungi: Keeling PJ. 2009. Chromalveolates and the evolution of plas- Evidence from the largest subunit of RNA polymerase tids by secondary endosymbiosis. J Eukaryot Microbiol II and other proteins. Proc Natl Acad Sci 96: 580–585. 56: 1–8. Hjort K, Goldberg AV, Tsaousis AD, Hirt RP, Embley TM. Keeling PJ. 2013. The number, speed, and impact of plastid 2010. Diversity and reductive evolution of mitochondria endosymbioses in eukaryotic evolution. Annu Rev among microbial eukaryotes. Philos Trans R Soc Lond B Biol 64: 27.1–27.25. Biol Sci 365: 713–727. Keeling PJ, Doolittle WF. 1996. A non-canonical genetic Ho SY, Jermiin L. 2004. Tracing the decay of the historical code in an early diverging eukaryotic lineage. EMBO J signal in biological sequence data. Syst Biol 53: 623–637. 15: 2285–2290. Iwamoto M, Pi M, Kurihara M, Morio T, Tanaka Y. 1998. A Keeling PJ, Slamovits CH. 2005. Causes and effects of nu- gene cluster is encoded in the mito- clear genome reduction. Curr Opin Genet Dev 15: 601– chondrial DNA of : UGA ter- 608. mination codons and similarity of gene order to Acan- Keeling PJ, Burger G, Durnford DG, Lang BF,Lee RW,Pearl- thamoeba castellanii. Curr Genet 33: 304–310. man RE, Roger AJ, Gray MW. 2005. The tree of eukary- James TY, Pelin A, Bonen L, Ahrendt S, Sain D, Corradi N, otes. Trends Ecol Evol 20: 670–676. Stajich JE. 2013. Shared signatures of and phy- Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, Bowman logenomics unite Cryptomycota and Microsporidia. S, Archibald JM. 2007. Plastid genome sequence of the Curr Biol 23: 1–6. cryptophyte alga salina CCMP1319: Later- Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ. al transfer of putative DNA replication machinery and a 2010. A common red algal origin of the apicomplexan, of chromist plastid phylogeny. Mol Biol Evol 24: dinoflagellate, and heterokont plastids. Proc Natl Acad Sci 1832–1842. 107: 10949–10954. Kim E, Simpson AG, Graham LE. 2006. Evolutionary rela- Jeffroy O, Brinkmann H, Delsuc F, Philippe H. 2006. Phy- tionships of apusomonads inferred from taxon-rich anal- logenomics: The beginning of incongruence? Trends Ge- yses of 6 nuclear encoded genes. Mol Biol Evol 23: 2455– net 22: 225–231. 2466. Jermiin L, Ho SY,Ababneh F,Robinson J, Larkum AW.2004. Kim E, Harrison JW, Sudek S, Jones MD, Wilcox HM, Ri- The biasing effect of compositional heterogeneity on chards TA, WordenAZ, Archibald JM. 2011. Newly iden- phylogenetic estimates may be underestimated. Syst Biol tified and diverse plastid-bearing branch on the eukary- 53: 638–643. otic tree of life. Proc Natl Acad Sci 108: 1496–1500. Jones MD, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, Klaveness D. 1995. Collodictyon triciliatum H.J. Carter Richards TA. 2011a. Discovery of novel intermediate (1865)—A common but fixation-sensitive algivorous fla-

14 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

gellate from the limnopelagial. Nord J Freshw Res 70: Moreira D, Le Guyader H, Philippe H. 2000. The origin of 3–11. red algae and the evolution of chloroplasts. Nature 405: Klenk H-P, Zilllg W, Lanzendorfer M, Grampp B, Palm P. 69–72. 1995. Location of protist lineages in a phylogenetic tree Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, inferred from sequences of DNA-dependent RNA poly- Bhattacharya D. 2009. Genomic footprints of a cryptic merases. Archiv fu¨r Protistenkunde 145: 221–230. plastid endosymbiosis in diatoms. Science 324: 1724– 1726. Knoll AH. 1992. The early evolution of eukaryotes: A geo- logical perspective. Science 256: 622–627. Nikolaev SI, Berney C, Fahrni JF, Bolivar I. 2004. The twi- light of and rise of Rhizaria, an emerging super- ¨ Kohler S, Delwiche CF, Denny PW, Tilney LG, Webster P, group of amoeboid eukaryotes. Proc Natl Acad Sci 101: Wilson RJ, Palmer JD, Roos DS. 1997. A plastid of prob- 8066–8071. able green algal origin in Apicomplexan parasites. Science Not FF, Valentin K, Romari K, Lovejoy C, Massana R, To¨be 275: 1485–1489. K, Vaulot D, Medlin LK. 2007. Picobiliphytes: A marine Kolisko M, Cepicka I, Hampl V, Leigh J, Roger AJ, Kulda J, picoplanktonic algal group with unknown affinities to Simpson AG, Flegr J. 2008. Molecular phylogeny of dip- other eukaryotes. Science 315: 253–255. a lomonads and enteromonads based on SSU rRNA, - Nozaki H, Iseki M, Hasegawa M, Misawa K, Nakada T, Sa- and genes: Implications for the evolu- saki N, Watanabe M. 2007. Phylogeny of primary photo- tionary history of the double karyomastigont of diplo- synthetic eukaryotes as deduced from slowly evolving monads. BMC Evol Biol 8: 205. nuclear genes. Mol Biol Evol 24: 1592–1595. Lane CE, Archibald JM. 2008. The eukaryotic tree of life: Nozaki H, Maruyama S, Matsuzaki M, Nakada T, Kato S, Endosymbiosis takes its TOL. Trends Ecol Evol 23: 268– Misawa K. 2009. Phylogenetic positions of Glaucophyta, 275. green plants (Archaeplastida) and Haptophyta (Chro- Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, malveolata) as deduced from slowly evolving nuclear Bowman S, Archibald JM. 2007. Nucleomorph genome genes. Mol Phylogenet Evol 53: 872–880. of andersenii reveals complete intron loss Okamoto N, Inouye I. 2005. The katablepharids are a distant and compaction as a driver of and func- sister group of the Cryptophyta: A proposal for Katable- tion. Proc Natl Acad Sci 104: 19908–19913. pharidophyta divisio nova/Kathablepharida phylum no- Lara E, Moreira D, Lo´pez-Garcı´a P.2010. The environmental vum based on SSU rDNA and b-tubulin phylogeny. Pro- clade LKM11 and Rozella form the deepest branching tist 156: 163–179. clade of fungi. Protist 161: 116–121. Okamoto N, Chantangsi C, Horak A, Leander BS, Keeling Liu Y, Steenkamp E, Brinkmann H, Forget L, Philippe HH, PJ. 2009. Molecular phylogeny and description of the novel gen. et sp. nov., Lang BF. 2009. Phylogenomic analyses predict sis- and establishment of the Hacrobia taxon nov. PLoS ONE tergroup relationship of nucleariids and fungi and para- 4: e7080. phyly of zygomycetes with significant support. BMC Evol Biol 9: 272. Palmer JD. 2003. The symbiotic birth and spread of plastids: How many times and whodunit? J Phycol 39: 4–11. Lonergan KM, Gray MW. 1996. Expression of a continuous Parfrey LW, Barbero E, Lasser E, Dunthorn M, Bhattacharya encoding subunits 1 and 2 of cyto- D, Patterson DJ, Katz LA. 2006. Evaluating support for chrome c oxidase in the mitochondrial DNA of Acantha- the current classification of eukaryotic diversity. PLoS moeba castellanii. J Mol Biol 257: 1019–1030. Genet 2: e220. Lopez P, Casane D, Philippe H. 2002. Heterotachy, an Patron NJ, Inagaki Y, Keeling PJ. 2007. Multiple gene phy- important process of protein evolution. MolBiolEvol19: logenies support the monophyly of cryptomonad and 1–7. host lineages. Curr Biol 17: 887–891. Lynch M, Conery JS. 2003. The origins of genome complex- Pawlowski J. 2013. The new micro-kingdoms of eukaryotes. ity. Science 302: 1401–1404. BMC Biol 11: 40. Margulis L. 1971. Whittaker’s five kingdoms of organisms: Pawlowski J, Burki F. 2009. Untangling the phylogeny of Minor revisions suggested by considerations of the origin amoeboid protists. J Eukaryot Microbiol 56: 16–25. of . Evolution 25: 242–245. Pawlowski J, Bolivar I, Fahrni JF,Cavalier-Smith T,Gouy M. McFadden GI, van Dooren GG. 2004. Evolution: Red algal 1996. Early origin of foraminifera suggested by SSU genome affirms a common origin of all plastids. Curr Biol rRNA gene sequences. Mol Biol Evol 13: 445–450. 14: R514–R516. Philippe H. 2000. Opinion: Long branch attraction and Minge MA, Silberman JD, Orr RJS, Cavalier-Smith T, Shal- protist phylogeny. Protist 151: 307–316. chian-Tabrizi K, Burki F, Skjaeveland A, Jakobsen KS. Philippe H, Germot A, Moreira D. 2000a. The new phylog- 2009. Evolutionary position of breviate amoebae and eny of eukaryotes. Curr Opin Genet Dev 10: 596–601. the primary eukaryote divergence. Proc R Soc Lond B Philippe H, Lopez P, Brinkmann H, Budin K, Germot A, Biol Sci 276: 597–604. Laurent J, Moreira D, Mu¨ller M, Le Guyader H. 2000b. Moore RB, Obornik M, Janouskovec J, Chrudimsky´ T, Van- Early-branching or fast-evolving eukaryotes? An answer cova´ M, Green DH, Wright SW, Davies NW, Bolch CJ, based on slowly evolving positions. Proc R Soc Lond B Biol Heimann K, et al. 2008. A photosynthetic alveolate close- Sci 267: 1213–1221. ly related to apicomplexan parasites. Nature 451: 959– Philippe H, Delsuc F, Brinkmann H, Lartillot N. 2005. Phy- 963. logenomics. Annu Rev Ecol Evol Syst 36: 541–562.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 15 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

F. Burki

Philippe H, Brinkmann H, Lavrov DV, Littlewood DT, Ma- Shalchian-TabriziK, Minge MA, Espelund M, Orr R, Ruden nuel M, Wo¨rheide G, Baurain D. 2011. Resolving difficult T, Jakobsen KS, Cavalier-Smith T. 2008. Multigene phy- phylogenetic questions: Why more sequences are not logeny of and the origin of animals. PLoS enough. PLoS Biol 9: e1000602. ONE 3: e2098. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber AP, Sierra R, Matz MV,Aglyamova G, Pillet L, Decelle J, Not F,de Schwacke R, Gross J, Blouin NA, Lane C, et al. 2012. Vargas C, Pawlowski J. 2013. Deep relationships of Rhi- genome elucidates origin of pho- zaria revealed by phylogenomics: A farewell to Haeckel’s tosynthesis in algae and plants. Science 335: 843–847. . Mol Phylogenet Evol 67: 53–59. Reyes-Prieto A, WeberAP,Bhattacharya D. 2007. The origin Simpson AG. 2003. Cytoskeletal organization, phylogenetic and establishment of the plastid in algae and plants. Annu affinities and systematics in the contentious taxon Exca- Rev Genet 41: 147–168. vata (Eukaryota). Int J Syst Evol Micr 53: 1759–1777. Rice DW, Palmer JD. 2006. An exceptional horizontal gene Simpson AG, Roger AJ. 2004. The real “kingdoms” of eu- transfer in plastids: Gene replacement by a distant bacte- karyotes. Curr Biol 14: R693–R696. rial paralog and evidence that haptophyte and crypto- phyte plastids are sisters. BMC Biol 4: 31. Smirnov A, Nassonova E, Berney C, Fahrni J, Bolivar I, Pawlowski J. 2005. Molecular phylogeny and classifica- Richards TA, Cavalier-Smith T. 2005. Myosin domain evo- tion of the lobose amoebae. Protist 156: 129–142. lution and the primary divergence of eukaryotes. Nature 436: 1113–1118. Sogin ML. 1991. Early evolution and the origin of eukary- otes. Curr Opin Genet Dev 1: 457–463. Riisberg I, Orr RJ, Kluge R, Shalchian-TabriziK, Bowers HA, Patil V,Edvardsen B, Jakobsen KS. 2009. Seven gene phy- Sogin ML, Elwood HJ, Gunderson JH. 1986. Evolutionary logeny of heterokonts. Protist 160: 191–204. diversity of eukaryotic small-subunit rRNA genes. Proc Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Natl Acad Sci 83: 1383–1387. Burger G, Lo¨ffelhardt W, Bohnert HJ, Philippe H, Lang Sogin ML, Gunderson JH, Elwood HJ, Alonso R. 1989. Phy- BF. 2005. Monophyly of primary photosynthetic eukary- logenetic meaning of the kingdom concept: An unusual otes: Green plants, red algae, and glaucophytes. Curr Biol ribosomal RNA from Giardia lamblia. Science 243: 15: 1325–1330. 75–77. Rodriguez-Ezpeleta N, Brinkmann H, Burger G, Roger AJ, Stechmann A, Cavalier-Smith T. 2002. Rooting the eukary- Gray MW, Philippe H, Lang BF. 2007a. Toward resolving ote tree by using a derived gene fusion. Science 297: the eukaryotic tree: The phylogenetic positions of jako- 89–91. bids and cercozoans. Curr Biol 17: 1420–1425. Stechmann A, Cavalier-Smith T. 2003. The root of the eu- Rodriguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, karyote tree pinpointed. Curr Biol 13: R665–R666. Lang BF, Philippe H. 2007b. Detecting and overcoming Steenkamp ET, Wright J, Baldauf SL. 2006. The protistan systematic errors in genome-scale phylogenies. Syst Biol origins of animals and fungi. Mol Biol Evol 23: 93–106. 56: 389–399. Stiller JW. 2011. Experimental design and statistical rigor in Roger A. 1999. Reconstructing early events in eukaryotic phylogenomics of horizontal and endosymbiotic gene evolution. Am Nat 154: S146–S163. transfer. BMC Evol Biol 11: 259. Roger AJ, Simpson AG. 2009. Evolution: Revisiting the root TakishitaK, Kolisko M, Komatsuzaki H, YabukiA, Inagaki Y, of the eukaryote tree. Curr Biol 19: R165–R167. Cepicka I, Smejkalova´ P, Silberman JD, Hashimoto T, Roger AJ, Sandblom O, Doolittle W, Philippe H. 1999. An Roger AJ, et al. 2012. Multigene phylogenies of diverse evaluation of elongation factor 1a as a phylogenetic -like organisms identify the closest rela- marker for eukaryotes. Mol Biol Evol 16: 218–233. tives of “amitochondriate” diplomonads and retortamo- Rogozin IB, Basu MK, Csu¨ro¨s M, Koonin EV.2009. Analysis nads. Protist 163: 344–355. of rare genomic changes does not support the unikont- Tovar J, Fischer A, Clark CG. 1999. The mitosome, a novel bikont phylogeny and suggests cyanobacterial organelle related to mitochondria in the amitochondrial as the point of primary of eukaryotes. Genome parasite Entamoeba histolytica. Mol Microbiol 32: 1013– Biol Evol 1: 99–113. 1021. Ruiz-Trillo I, Roger AJ, Burger G, Gray MW, Lang BF. 2008. ´ ´ A phylogenomic investigation into the origin of metazoa. Tovar J, Leon-Avila G, Sanchez LB, Sutak R, Tachezy J, van Mol Biol Evol 25: 664–672. der Giezen M, Herna´ndez M, Mu¨ller M, Lucocq JM. 2003. Mitochondrial remnant organelles of Giardia func- Sanchez Puerta MV, Delwiche CF. 2008. A hypothesis for tion in iron-sulphur protein maturation. Nature 426: plastid evolution in chromalveolates. J Phycol 44: 1097. 172–176. Seenivasan R, Sausen N, Medlin LK, Melkonian M. 2013. Van de Peer Y, Van der Auwera G, De Wachter R. 1996. The Picomonas judraskeda gen. et sp nov.: The first identified member of the Picozoa phylum nov., a widespread group evolution of stramenopiles and alveolates as derived by of , formerly known as “picobiliphytes.” “substitution rate calibration” of small ribosomal subunit PLoS ONE 8: e59565. RNA. J Mol Biol 42: 201–210. Shalchian-Tabrizi K, Eikrem W, Klaveness D, Vaulot D, WainrightPO, Hinkle G, Sogin ML, Stickel SK. 1993. Mono- Minge MA, Le Gall F, Romari K, Throndsen J, Botnen phyletic origins of the metazoa: An evolutionary link A, Massana R, et al. 2006. Telonemia, a new protist phy- with fungi. Science 260: 340–342. lum with affinity to chromist lineages. Proc R Soc Lond B Whittaker H. 1969. New concepts of kingdoms of organ- Biol Sci 273: 1833–1842. isms. Science 163: 150–160.

16 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Tree of Eukaryotes

Wideman JG, Gawryluk RM, Gray MW,Dacks JB. 2013. The Yamamoto A, Hashimoto T, Asaga E, Hasegawa M, Goto N. ancient and widespread nature of the ER-mitochondria 1997. Phylogenetic position of the mitochondrion-lack- encounter structure. Mol Biol Evol 30: 2044–2049. ing protozoan , based on amino acid Williams BA, Hirt RP, Lucocq JM, Embley TM. 2002. A sequences of elongation factors 1a and 2. J Mol Evol 44: mitochondrial remnant in the microsporidian Trachi- 98–105. pleistophora hominis. Nature 418: 865–869. Yoon HS, Hackett JD, Pinto G, Bhattacharya D. 2002. The Williams TA,Foster PG, Nye TM, Cox CJ, Embley TM. 2012. single, ancient origin of chromist plastids. Proc Natl Acad Acongruent phylogenomic signal places eukaryotes with- Sci 99: 15507–15512. in the . Proc R Soc Lond B Biol Sci 279: 4870–4879. Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki WoeseCR, Kandler O, Wheelis ML. 1990. Towards a natural ME, Wilson WH, Yang EC, Duffy S, Bhattacharya D. system of organisms: Proposal for the domains Archaea, 2011. Single-cell genomics reveals organismal interac- , and Eucarya. Proc Natl Acad Sci 87: 4576–4579. tions in uncultivated . Science 332: 714– Yabuki A, Inagaki Y, Ishida K-I. 2010. 717. gen. et sp. nov.: A novel deep-branching Zhao S, Burki F, Brate J, Keeling PJ, Klaveness D, Shalchian- possibly related to Archaeplastida or Hacrobia. Protist Tabrizi K. 2012. Collodictyon—An ancient lineage in the 161: 523–538. tree of eukaryotes. Mol Biol Evol 29: 1557–1568.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016147 17 Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Eukaryotic Tree of Life from a Global Phylogenomic Perspective

Fabien Burki

Cold Spring Harb Perspect Biol 2014; doi: 10.1101/cshperspect.a016147

Subject Collection The Origin and Evolution of Eukaryotes

The Persistent Contributions of RNA to Eukaryotic Origins: How and When Was the Eukaryotic Gen(om)e Architecture and Cellular Mitochondrion Acquired? Function Anthony M. Poole and Simonetta Gribaldo Jürgen Brosius Green Algae and the Origins of Multicellularity in Bacterial Influences on Origins the Plant Kingdom Rosanna A. Alegado and Nicole King James G. Umen The Archaeal Legacy of Eukaryotes: A Missing Pieces of an Ancient Puzzle: Evolution of Phylogenomic Perspective the Eukaryotic Membrane-Trafficking System Lionel Guy, Jimmy H. Saw and Thijs J.G. Ettema Alexander Schlacht, Emily K. Herman, Mary J. Klute, et al. Origin and Evolution of the Self-Organizing The Neomuran Revolution and Phagotrophic in the Network of Eukaryotic Origin of Eukaryotes and Cilia in the Light of Organelles Intracellular Coevolution and a Revised Tree of Gáspár Jékely Life Thomas Cavalier-Smith On the Age of Eukaryotes: Evaluating Evidence and Transport as a Necessary from and Molecular Clocks Consequence of Increased Cellular Complexity Laura Eme, Susan C. Sharpe, Matthew W. Brown, Maik S. Sommer and Enrico Schleiff et al. Origin of Spliceosomal and Alternative How Natural a Kind Is ''Eukaryote?'' Splicing W. Manuel Irimia and Scott William Roy Protein and DNA Modifications: Evolutionary What Was the Real Contribution of Imprints of Bacterial Biochemical Diversification to the Eukaryotic Nucleus? and Geochemistry on the of Insights from Photosynthetic Eukaryotes Eukaryotic David Moreira and Philippe Deschamps L. Aravind, A. Maxwell Burroughs, Dapeng Zhang, et al.

For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved Downloaded from http://cshperspectives.cshlp.org/ on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press

The Eukaryotic Tree of Life from a Global Bioenergetic Constraints on the Evolution of Phylogenomic Perspective Complex Life Fabien Burki Nick Lane

For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved