The Eukaryotic Tree of Life from a Global Phylogenomic Perspective
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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 Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada Correspondence: [email protected] Molecular phylogenetics has revolutionized our knowledge of the eukaryotic tree of life. With the advent of genomics, a new discipline of phylogenetics has emerged: phylogenom- ics. This method uses large alignments of tens to hundreds of genes to reconstruct evolution- 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 protist lineages for understanding eukaryote evolution. Here, I discuss the pros and cons of phylogenomics 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 root. 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 eukaryotes are di- ticellular organisms. Eukaryotes have occupied Iverse. Plants, animals, and fungi are the char- just about every ecological niche on Earth. 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 plastids (chloroplasts) to de- justice to the eukaryotic diversity. Microscop- rive energy from the light; many can adapt to ic eukaryotes, often unicellular and known as variable conditions by switching between auto- the protists, 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 genomes—more than organelles), an infinite variation of forms and 200 times larger than that of humans (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 oceans. 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 algae. At around 500,000 nucleotides 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 genome 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, biologists 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 phylogenetic tree marker. including all organisms is not only the ultimate The pioneering molecular phylogenies con- goal of systematics, it would also provide the sistently recovered a handful of deeply diverging foundation to infer the acquisition and evolu- protist lineages (e.g., diplomonads, parabasal- tion of countless characters through the history ids, microsporidians, Archamoebae), progres- of long-dead species. 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, biology text- cause these early diverging species were seem- books assigned the eukaryotes to evolutionary ingly morphologically simple single-cell 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 biologist ignored protists, and also consistent with the archezoa hypothesis, they have been in fact recognized as a kingdom 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 mitochondrion-containing mental paraphyletic and complex nature 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 clades of eukaryotes, through some profound rearrangements in the appearing tightly bunched together as if they past 20 years. Comparing nucleotide 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 alveolates and stramenopiles (see tation of their morphological characters alone below). The branching pattern 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 protein 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 prokaryote-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 time, 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 gene fusions, or the systematic analysis the eukaryotic tree showing the archezoan- of light and electron microscopy 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 Euglenozoa and Foraminifera 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