The Hybrid Nature of the Eukaryota and a Consilient View of Life on Earth
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Nature Reviews Microbiology | AOP, published online 12 May 2014; doi:10.1038/nrmicro3271 PERSPECTIVES of eukaryogenesis have been proposed. OPINION There is substantial molecular support for endosymbiosis4,14, and the mechanism (that The hybrid nature of the Eukaryota is, selective advantage) for this model has also been explored6,9,20–22. By contrast, autog- and a consilient view of life on Earth enous models, which imply that eukaryotes arose by stepwise mutations without the external acquisition of genetic material, James O. McInerney, Mary J. O’Connell and Davide Pisani require an excessive amount of ad hoc expla- 23 Abstract | The origin of the eukaryotic cell, which is known as eukaryogenesis, has nation . In addition, as it has been found that amitochondriate eukaryotes, such as puzzled scientists for more than 100 years, and many hypotheses have been microsporidia24 and Giardia spp.25, are not proposed. Recent analyses of new data enable the safe elimination of some of primitively amitochondriate but are instead these hypotheses, whereas support for other hypotheses has increased. In this derived from mitochondrion-bearing ances- Opinion article, we evaluate the available theories for their compatibility with tors, the evidence suggests that acquisition empirical observations and conclude that cellular life consists of two primary, of the mitochondrion occurred early in eukaryotic evolution and certainly predates paraphyletic prokaryotic groups and one secondary, monophyletic group that has the origin of all known extant eukaryotes. symbiogenic origins — the eukaryotes. The details of the process of mitochon- drial acquisition are still debated. Much of In 1905, Konstantin Mereschkowski pos- bioenergetics, and modern cell biology and our understanding of the nature of life on tulated a symbiotic origin of plastids and biochemistry — each of which has contrib- Earth and the deepest philosophical rami- animal cells1, and in 1923, Ivan Wallin argued uted important and surprisingly congruent fications of this knowledge depend almost for a bacterial origin of the mitochondrion2. insights relating to this argument. It is the entirely on a precise understanding of the Since then, dozens of scenarios have been put consilience of these lines of evidence that origin of the mitochondrion4,14,22,26. One sce- forward to explain eukaryogenesis3–10. How leads us to conclude that eukaryotes are nario that is commonly seen in textbooks27 then should the different lines of evidence be not a primary lineage of life; rather, they describes Eukaryota as a lineage that sepa- viewed and how should their contributions are a relatively late innovation, are perhaps rated from the Archaebacteria before the to the arguments be weighted? younger than any of the two prokaryotic diversification of the Archaebacteria. In this Although many readers will be familiar groups and emerged from both of them. scenario, mitochondrial origins merely cor- with Karl Popper11, who advocated falsifi- Indeed, the ‘eukaryotes-late’ hypotheses respond to the introgression28 of a symbiont ability — that is, generating, testing and imply that there was a merger between an into an otherwise well-defined eukaryotic rejecting hypotheses — as the framework for archaebacterium and a eubacterium. lineage. This is known as the three‑domains generating knowledge, the framework by A recent report focusing on the evidence hypothesis27 (FIG. 1a). The three‑domains tree which we understand evolution to be a that supports a paraphyletic organization of recognizes Eubacteria, Archaebacteria and strong theory is that of consilience12. Con- the Archaebacteria13 has indicated that life is Eukaryota as three primary, monophyletic silience is said to be the ‘jumping together’ divided into two domains. In this Opinion lineages of ancient origins. The rooting of of facts or, in other words, the analysis of article, we explore the evidence for eukaryotic this tree, which was achieved using deeply whether there is agreement across different origins for all parts of the eukaryotic cell. diverging paralogues29, identified Eukaryota classes of evidence, thereby amounting to as the sister lineage to the Archaebacteria. a single unifying theory12. For example, Background: the proposed models An alternative rooting of the three‑domains evolution is a strong theory because there is The origin of eukaryotes is intimately inter- tree places the Eukaryota as the sister line- consilience between empirical observations twined with the study of endosymbiosis, age to a monophyletic prokaryotic group from genetics, palaeontology, chemistry, particularly with the origin of the mitochon- (which consists of the Archaebacteria and physics and behaviour, and together, these drion. Various endosymbiotic hypotheses the Eubacteria)5,30. This is known as the observations support an overall theory of for eukaryogenesis have been suggested, ‘eukaryotes-early’ hypothesis (FIG. 1b). In this evolution. and specific prokaryotic groups have scenario, an ancient complex eukaryotic cell In this Opinion article, we argue that been proposed as the sister groups of the underwent various reduction events to give hypothesis testing and inductive reasoning mitochondrion and the plastid4,7,8,14–17. The rise to prokaryotes5; no recent phylogenetic are consilient with a symbiogenic hypothesis origin of the mitochondrion is key to dis- analysis has provided convincing support for the origin of the Eukaryota. We address tinguishing between alternative hypotheses for this hypothesis. Other alternatives to the eukaryogenesis from four perspectives — regarding the origins of eukaryotes. Both three‑domains tree include a phagotrophic molecular phylogenetics, palaeontology, endosymbiotic4,14 and autogenous18,19 models hypothesis18, hypotheses that suggest an NATURE REVIEWS | MICROBIOLOGY ADVANCE ONLINE PUBLICATION | 1 © 2014 Macmillan Publishers Limited. All rights reserved PERSPECTIVES a Three-domains Eubacteria Other autogenous theories include the the mitochondrion or identical to it. In its hypothesis gradual evolution of eukaryotes from within original definition36, Eocyte simply referred the Archaebacteria32 or from the Eubacteria, to those organisms that are a sister group to Archaebacteria with some lateral gene transfer (LGT) from the Eukaryota within the Archaebacteria. the Archaebacteria33. The ring of life hypothesis argues that the Eukaryota Current, viable alternatives to autoge- Eukaryota emerged from within the Archae- neous models are represented by a set of bacteria8,9,34,37 at the same time as from hypotheses in which the eukaryotic lineage within the Eubacteria and that the Eocytes b Eukaryotes-early was established as a consequence of a are the archaebacterial sister group of the hypothesis Eukaryota merger in which two (or more) prokaryotes Eukaryota. either fused or entered a process of sym- Regardless of the placement of the root biosis7–9,15,20,21,34,35. These hypotheses differ of life, whether it is within the Eubacteria38 Archaebacteria in the number of mergers they assume, the or between the Eubacteria and Archaebacte- phylogenetic affinities of the mergers and ria29,39, the ring of life and the three‑domains Eubacteria the order in which the mergers occurred. tree are mutually incompatible. Indeed, the Nevertheless, they all imply that the Eukary ring of life type of model has a profound ota are not a primary lineage of life, and implication for how we view life, as it sug- c Eocyte hypothesis hence — in contrast to the three‑domains gests that the Eukaryota are not a primary Eubacteria hypothesis — they do not entail the existence lineage but are a secondary lineage of life of a proto-eukaryotic lineage as old as the and that the Archaebacteria and Eubacteria Archaebacteria. are not monophyletic (FIG. 2). The first step Other Archaebacteria It is important to note that not all towards understanding the origins of eukary Eukaryota hypotheses that propose the existence of otes is therefore to clarify whether the cur- Eocytes only two primary lineages of life are equally rent evidence supports the Eocyte–eukaryote well supported. Although many homologues grouping, which is compatible with the ring are shared by Eukaryota and Archaebacteria, of life, or the three‑domains grouping, which d Ring of life hypothesis Eubacteria the observed contribution to eukaryotic is not. genomes from specifically hydrogen- dependent archaebacteria is limited, which Evidence from phylogenetic analyses Eukaryota weakens support for the hydrogen hypoth- The phylogenetic relationships of eukaryotes esis20 and for sulphur-syntrophy hypotheses21. have been analysed using both genome-scale Eocytes 3,8,39 Other Furthermore, the contributions from Delta data sets and smaller sets of genes (vary- 7 15,35 Archaebacteria proteobacteria and Spirochaetes are not ing from one to approximately 85 genes, significant in number17 and are probably and often encoding ribosomal proteins) Figure 1 | Competing scenarios for the origin limited to individual LGTs. This effectively that are assumed to be ‘genealogy-defining’ of the eukaryotesNature and the Reviews highest-level | Microbiology struc- argues against the serial endosymbiotic (REFS 27,37,40,41). Woese originally pro- ture for describing the diversity of cellular 15,35 life. a | The ‘three‑domains’ phylogenetic tree, theory (SET) of Margulis and the syn- posed ribosomal RNA genes to be the ideal 27 which is also known as the three‑domains tree of trophy hypothesis of López–García and