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Origin and Diversification of Eukaryotes MI66CH20-Katz ARI 21 June 2012 17:22 V I E E W R S Review in Advance first posted online on July 9, 2012. (Changes may still occur before final publication E online and in print.) I N C N A D V A Origin and Diversification of Eukaryotes 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 eukaryotic diversity, protists, tree of life, nucleus, cytoskeleton, micro.annualreviews.org mitochondria This article’s doi: by SMITH COLLEGE on 08/12/12. For personal use only. 10.1146/annurev-micro-090110-102808 Abstract Copyright c 2012 by Annual Reviews. The bulk of the diversity of eukaryotic life is microbial. Although the larger All rights reserved Annu. Rev. Microbiol. 2012.66. Downloaded from www.annualreviews.org eukaryotes—namely plants, animals, and fungi—dominate our visual land- 0066-4227/12/1013-0411$20.00 scapes, microbial lineages compose the greater part of both genetic diversity and biomass, and contain many evolutionary innovations. Our understand- ing of the origin and diversification of eukaryotes has improved substan- tially with analyses of molecular data from diverse lineages. These data have provided insight into the nature of the genome of the last eukaryotic com- mon ancestor (LECA). Yet, the origin of key eukaryotic features, namely the nucleus and cytoskeleton, remains poorly understood. In contrast, the past decades have seen considerable refinement in hypotheses on the major branching events in the evolution of eukaryotic diversity. New insights have also emerged, including evidence for the acquisition of mitochondria at the time of the origin of eukaryotes and data supporting the dynamic nature of genomes in LECA. 411 Changes may still occur before final publication online and in print MI66CH20-Katz ARI 21 June 2012 17:22 Contents INTRODUCTION............................................................... 412 PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST EUKARYOTICCOMMONANCESTOR..................................... 414 Origin of Eukaryotic Genomes . 414 Origin of the Nucleus. 416 Origin of the Cytoskeleton . 417 Origin of Mitochondria . 417 PART II: EVOLUTION OF PHOTOSYNTHESIS WITH EUKARYOTES. 418 PART III: RELATIONSHIPS AMONG MAJOR LINEAGES . 418 RootoftheEukaryoticTreeofLife............................................. 419 MajorEukaryoticClades........................................................ 420 CONCLUSION.................................................................. 422 INTRODUCTION We live on a microbial planet. Microbes have dominated Earth’s history and continue to represent Eukaryote: a cell with the majority of both biodiversity and biomass on our planet. Two of the three domains of life, the a nucleus Bacteria and Archaea, are virtually exclusively microbial, and microbial forms dominate among Last eukaryotic the third domain, Eukaryota, which is the focus of this review. Yet despite their importance, much common ancestor remains to be learned about microbial life in terms of discovering of new forms, understanding (LECA): lineage that major innovations, and incorporating the biology of microorganisms into theories and models gave rise to extant eukaryotes across disciplines within biology. Eukaryotes are named for one of their defining features—the presence of a nucleus (eu, “true,” Cytoskeleton: complex structure in and karyo, “kernel” or “seed”). A defining feature is one that is found in every eukaryote and eukaryotes that that was present in the last eukaryotic common ancestor (LECA). A second defining feature is provides for shape and the presence of a cytoskeleton, which is a complex set of structures underlain by a tremendous motility diversity of proteins (e.g., actins, tubulins, dyneins). The cytoskeleton gives eukaryotes their diverse morphologies (Figure 1), variable motility, and ability to engulf other organisms. by SMITH COLLEGE on 08/12/12. For personal use only. Early attempts to reconstruct the tree of life focused on macroscopic organisms, first di- viding living things between Plantae and Animalia, and then adding Protista as a grab bag of Annu. Rev. Microbiol. 2012.66. Downloaded from www.annualreviews.org −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ 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,atestate amoeba in Tubulinea. (t–w) Opisthokonta. (t) Homo sapiens, animal. (u) Campyloacantha sp., a choanoflagellate. (v) Amanita flavoconia,a ∗ basidiomycete fungus. (w) Chytriomyces sp., a chytrid. All images are provided by micro scope (http://starcentral.mbl.edu/ microscope/portal.php) except panel t, which is provided by the author. Redrawn from Reference 116, BioScience 59(6), Copyright 2009, American Institute of Biological Sciences. 412 Katz Changes may still occur before final publication online and in print MI66CH20-Katz ARI 21 June 2012 17:22 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. aabcb c ded e 10 µm 100 µm 10 µm 10 µm 10 µm fgf g h i j 10 µm 10 µm 10 µm 10 µm 10 µm klllmm n o by SMITH COLLEGE on 08/12/12. For personal use only. 100 µm 10 µm 10 µm 10 µm Annu. Rev. Microbiol. 2012.66. Downloaded from www.annualreviews.org ppqq r s 10 µm 10 µm 5 mm 10 µm t u v w 10 µm 10 µm www.annualreviews.org • Origin and Diversification of Eukaryotes 413 Changes may still occur before final publication online and in print MI66CH20-Katz ARI 21 June 2012 17:22 PART I: ORIGIN OF EUKARYOTES AND FEATURES OF THE LAST EUKARYOTIC COMMON ANCESTOR LGT: lateral gene Beyond the ubiquitous nucleus and cytoskeleton, we can infer that LECA was complex in terms transfer, also called of its morphology and genome. Insights into LECA emerge from a long history of study of horizontal gene diverse eukaryotic organisms coupled with more recent inferences from molecular data. These transfer data reveal that LECA had complex morphology, with a nucleus, mitochondria, and a cytoskeleton Chimerism: the plus associated features (e.g., flagella). As argued in detail below, LECA also had a genome that presence of genes of was both chimeric, with respect to bacteria and archaea, and dynamic, with epigenetic phenomena varying ancestries within eukaryotic playing key roles during life cycles. genomes Homologs: shared characteristics present Origin of Eukaryotic Genomes in last common ancestor of a group of Evidence of the evolutionary history of eukaryotic genomes provides a backdrop for interpretation organisms 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
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