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Eukaryogenesis, How Special Really? Eukaryogenesis, how special really? Austin Bootha,b and W. Ford Doolittlea,1 Departments of aBiochemistry and Molecular Biology and bPhilosophy, Dalhousie University, Halifax, NS, Canada B3H 4R2 Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved March 19, 2015 (received for review January 12, 2015) Eukaryogenesis is widely viewed as an improbable evolutionary Hydrogen Hypothesis (6)] entailed unique cellular mechanisms transition uniquely affecting the evolution of life on this planet. and had uniquely important, radical consequences for both the However, scientific and popular rhetoric extolling this event as a subsequent evolution of organismal complexity and the articulation singularity lacks rigorous evidential and statistical support. Here, of evolutionary theory, it is believed. The biochemist Nick Lane has we question several of the usual claims about the specialness of written, for instance, eukaryogenesis, focusing on both eukaryogenesis as a process and If the origin of the eukaryotic cell was not a bottleneck, then it was its outcome, the eukaryotic cell. We argue in favor of four ideas. probably a genuinely unlikely sequence of events, for it happened First, the criteria by which we judge eukaryogenesis to have only once. Speaking as a multicellular eukaryote, I might be biased, required a genuinely unlikely series of events 2 billion years in the but I do not believe that bacteria will ever ascend the smooth ramp to making are being eroded by discoveries that fill in the gaps of the sentience, or anywhere much beyond slime, here or anywhere else in prokaryote:eukaryote “discontinuity.” Second, eukaryogenesis the universe. No, the secret of complex life lies in the chimeric nature confronts evolutionary theory in ways not different from other of the eukaryotic cell—a hopeful monster, born in an improbable evolutionary transitions in individuality; parallel systems can be merger 2000 million years ago, an event still frozen in our innermost found at several hierarchical levels. Third, identifying which of sev- constitution and dominating our lives today (2). eral complex cellular features confer on eukaryotes a putative richer Writing for public audiences, and often even for themselves, evolutionary potential remains an area of speculation: various keys biologists are not loath to make simplifying claims about to success have been proposed and rejected over the five-decade uniqueness and importance that are rhetoric disguised as fact. history of research in this area. Fourth, and perhaps most impor- Such generalizations serve purposes in the doing of science, but tantly, it is difficult and may be impossible to eliminate eukaryocen- are often not themselves testable scientific claims and are subject tric bias from the measures by which eukaryotes as a whole are to biases. Evolutionary biology may be especially vulnerable to judged to have achieved greater success than prokaryotes as a hype, as suggested by the frequency with which revolutionary whole. Overall, we question whether premises of existing theories evolutionary claims in top-notch journals are debunked (7, 8). about the uniqueness of eukaryogenesis and the greater evolution- Additionally, anthropocentrism, as it grades into “zoocentrism” ary potential of eukaryotes have been objectively formulated and (9) and then “eukaryocentrism,” surely remains a subtle distorter whether, despite widespread acceptance that eukaryogenesis was “ ” of objectivity. special, any such notion has more than rhetorical value. Our aim here is to critique general claims about the unique- ness and special importance of eukaryogenesis, with an aim to eukaryogenesis | endosymbiosis | evolutionary theory | major transitions making them more open to question and conceptual and em- pirical analysis. We ask (i) whether eukaryogenesis entailed such “ ” The eukaryotic cell originated by the most complex set of evolu- a genuinely unlikely sequence of events (2) as to justify belief tionary changes since life began: eukaryogenesis. Their complexity in its uniqueness as a process, (ii) if, as is often claimed, eukaryo- and mechanistic difficulty explain why eukaryotes evolved two billion genesis has a problematic or unique theoretical status in evolu- years or more after prokaryotes. To understand these changes, we tionary biology, (iii) what intrinsic features might have conferred must consider the cell biology of all five major kinds of cells; deter- on eukaryotes their presumed “richer evolutionary potential” (3), mine their correct phylogenetic relationships; and explain the causes, and (iv) if this greater potential might be just a presumption, an steps, and detailed mechanisms of the radical transitions between illusion reflecting eukaryocentric bias. them. [Cavalier-Smith (1)] The acquisition of mitochondria was the pivotal moment in the his- Was Eukaryogenesis Unique as a Process? tory of life. [Lane (2)] It is often said that eukaryotes arose only once. What must really be meant by this is that there was but one last eukaryotic Compared to prokaryotes, eukaryotic cells represent not only an al- ternative mode of cellular organization but one endowed with far common ancestor (LECA) from which all contemporary living richer evolutionary potential: only among Eukarya do we find in- things that we call eukaryotes descend, and that if other lineages tegrated multicellular creatures that bear embryos, respond to music, with similar features arose independently, they are now extinct or and reflect on their own nature. Whatever meaning one assigns to the have not been found. Often, LECA is conceptualized as a single history of life, the advent of eukaryotic cells marked a radical and cell, but unless it was obligately asexual [which comparative ge- fateful transition. [Harold (3)] nomics suggests that it was not (10)], single species seems a better bet. Also, unless eukaryogenesis was a once-in-a-universe cataclysmic miracle, in which all eukaryote-specific features n the early 1960s, Stanier et al. famously wrote that the “basic Idivergence in cellular structure, which separates the bacteria and blue-green algae from all other cellular organisms, repre- This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of sents the greatest single evolutionary discontinuity to be found in Organelles,” held October 15–17, 2014, at the Arnold and Mabel Beckman Center of the the present-day world” (4). Nowadays, a tripartite division of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and living world is more popular—prokaryotes comprising Bac- video recordings of most presentations are available on the NAS website at www.nasonline. teria (including “blue-green algae”) and Archaea. However, the org/Symbioses. sentiment remains strong that the transition between prokaryotic Author contributions: A.B. and W.F.D. wrote the paper. and eukaryotic cell types, whether by symbiogenic or archezoan The authors declare no conflict of interest. schemes (5), was the single most important step in cellular evolu- This article is a PNAS Direct Submission. tion. The founding endosymbiosis [or syntrophic merger a la the 1To whom correspondence should be addressed. Email: [email protected]. 10278–10285 | PNAS | August 18, 2015 | vol. 112 | no. 33 www.pnas.org/cgi/doi/10.1073/pnas.1421376112 Downloaded by guest on September 28, 2021 PAPER appeared simultaneously and full-blown, there were very likely independent origins in different lineages, even from endosymbionts COLLOQUIUM many contemporaneous lineages with all or some of those fea- so closely related as to be indistinguishable in phylogenies (19). tures. It need not be that eukaryogenesis was so onerous that it In just the last few years, however, at least one endosymbiont took 2 billion years to accomplish, as Cavalier-Smith (1) main- not genealogically related to mitochondria and plastids has been tains. As likely, we think, is that only one of many near- shown to (likely) have independently evolved protein transport eukaryotic lineages survived. Notwithstanding claims about its machinery. Nowack and Grossman (20) reported that three genes enormous evolutionary potential, perhaps that lineage was encoding components of photosystem I that have been transferred just lucky! to the nucleus of the (eukaryotic) amoeba Paulinella chromato- Along the lineage leading to LECA, what we might choose to phora produce cytosol-synthesized proteins that are imported back designate as the first eukaryotic common ancestor (FECA) into chromatophores. These latter are cyanobacterial descendants (11) depends (barring that miraculous cataclysm) on which with highly reduced genomes, which apparently first entered into eukaryote-defining feature we take as necessary and sufficient endosymbiosis only some 60 Mya, long after and completely in- for eukaryoteness. Nowadays, many theorists would nominate dependently from (other) plastids. Whether there is some key the mitochondrion as that feature. Here again we should be difference between a highly dependent endosymbiont and an or- thinking not only of multiple contemporaneous but also re- ganelle is a definitional matter and not a scientific question an- ticulating lineages leading from FECA to LECA. It seems cer- swerable by experiment (21). Indeed, McCutcheon and Keeling, tain, for instance, that endosymbiotic gene transfer (EGT) prefiguring our title, recently
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