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Lynn Margulis and the Endosymbiont Hypothesis: 50 Years Later

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Lynn Margulis and the Endosymbiont Hypothesis: 50 Years Later MBoC | RETROSPECTIVE Lynn Margulis and the endosymbiont hypothesis: 50 years later Michael W. Gray* Department of Biochemistry and Molecular Biology and Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, NS B3H 4R2, Canada ABSTRACT The 1967 article “On the Origin of Mitosing Cells” in the Journal of Theoretical Monitoring Editor Biology by Lynn Margulis (then Lynn Sagan) is widely regarded as stimulating renewed inter- Keith G. Kozminski est in the long-dormant endosymbiont hypothesis of organelle origins. In her article, not only University of Virginia did Margulis champion an endosymbiotic origin of mitochondria and plastids from bacterial Received: Feb 21, 2017 ancestors, but she also posited that the eukaryotic flagellum (undulipodium in her usage) and Revised: Mar 16, 2017 mitotic apparatus originated from an endosymbiotic, spirochete-like organism. In essence, Accepted: Mar 21, 2017 she presented a comprehensive symbiotic view of eukaryotic cell evolution (eukaryogenesis). Not all of the ideas in her article have been accepted, for want of compelling evidence, but her vigorous promotion of the role of symbiosis in cell evolution unquestionably had a major influence on how subsequent investigators have viewed the origin and evolution of mito- chondria and plastids and the eukaryotic cell per se. In 1967, Lynn Margulis (then Lynn Sagan) published an article enti- proposition that a third subcellular structure, the eukaryotic fla- tled “On the Origin of Mitosing Cells” in the Journal of Theoretical gellum (“undulipodium” in her usage), originated from “ingestion Biology (Sagan, 1967). This publication did not have an auspicious of certain motile prokaryotes,” “perhaps spirochaete-like,” which beginning, reportedly having been rejected by more than a dozen eventually “became symbiotic in their hosts.” This overall scenario journals before eventually finding a home (Archibald, 2014). Now, it was later dubbed the serial endosymbiosis theory (Taylor, 1974). is widely regarded as marking the modern renaissance of the endo- Although a discussion of the origin of mitosis that Margulis symbiotic theory of organelle origins. outlined comprises a substantial portion of her article, there is no evi- In her article, Margulis hypothesized that “three fundamental dence supporting it, in contrast to the proposed endosymbiotic ori- organelles: the mitochondria, the photosynthetic plastids and the gin of mitochondria and plastids. The reason is simple: no genome (9 + 2) basal bodies of flagella were once themselves free-living has been associated with the eukaryotic flagellar apparatus despite (prokaryotic) cells.” That mitochondria and plastids might have orig- efforts to find one (Johnson and Rosenbaum, 1991), and it is through inated endosymbiotically from prokaryotic progenitors was not at the genomes contained in the mitochondrion and the plastid—the the time a new idea, having first emerged in various forms in the genes they harbor and how they are arranged and expressed—that late 19th and early 20th centuries before fading from mainstream we know with a high degree of certainty from whence these organ- biological view (Sapp, 1994). Margulis’ article was notable, how- elles originated: the bacterial clades α-Proteobacteria and Cyano- ever, in that it laid out an all-encompassing view of (endo)symbiosis bacteria, respectively (Gray and Doolittle, 1982; Gray, 1992). as the end-all and be-all of the eukaryotic cell: it was perhaps the Margulis’ vigorous promotion of the role of symbiosis in eukaryotic first unified theory of eukaryogenesis. The article included the novel cell evolution (Margulis, 1970) sparked a spirited debate throughout the 1970s and into the 1980s between proponents of autogenous ori- gin (“origin from within”) and xenogenous origin (“origin from with- out”) theories of organelle evolution. Although various authors re- DOI:10.1091/mbc.E16-07-0509 jected an endosymbiont scenario for both mitochondria and plastids *Address correspondence to: Michael W. Gray ([email protected]). (Uzzell and Spolsky, 1974), controversy during this period focused Abbreviations used: LECA, last eukaryotic common ancestor; PhAT, phagocytos- ing archaeon theory. especially on the mitochondrion (Raff and Mahler, 1972). A particularly © 2017 Gray. This article is distributed by The American Society for Cell Biology troubling issue, noted early by Mahler (1981), was the fact that “the under license from the author(s). Two months after publication it is available to mitochondrial genetic system exhibits unmistakable signs of great in- the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Cre- ative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). ter- and intra-species diversity,” suggesting that “this system is unique “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of and that its features are distinct from both its prokaryotic and eukary- the Cell®” are registered trademarks of The American Society for Cell Biology. otic counterparts.” Subsequent comparative analysis of mitochondrial Volume 28 May 15, 2017 1285 genomes and their expression only reinforced the view that in mito- In her 1967 article, Margulis suggested that “the first step in the chondria, anything goes (Burger et al., 2003). Nevertheless, a conflu- origin of eukaryotes from prokaryotes was related to survival in the ence of data—biochemical, molecular, and cell biological, coupled new oxygen-containing atmosphere: an aerobic prokaryotic mi- with the characterization in a group of eukaryotic microbes (the jako- crobe (i.e., the protomitochondrion) was ingested into the cyto- bid flagellates) of a gene-rich mitochondrial genome that strongly plasm of a heterotrophic anaerobe. This endosymbiosis became resembles a shrunken bacterial genome (Burger et al., 2013)—now obligate and resulted in the evolution of the first aerobic amitotic provides a compelling case for a single, endosymbiotic, α- amoeboid organisms.” It is not certain from this description whether proteobacterial origin of mitochondria (Gray et al., 1999; Gray, 2012). the proposed host was itself a prokaryote or something more “ad- A compelling case for an endosymbiotic origin has always been vanced”: Margulis is not explicit on this point. The allusion to easier to make for the plastid than for the mitochondrion. For one “amoeboid” and “ingestion” does suggest a type of protoeukary- thing, the plastid is evolutionarily younger than the mitochondrion: ote, albeit without many of the defining features of the contempo- whereas the last eukaryotic common ancestor (LECA) already had a rary eukaryotic cell, in particular a nucleus and mitotic apparatus. functional mitochondrion approximating its modern counterpart Later, however, Margulis (1981) made it clear that she favored a pro- (Koumandou et al., 2013), several major eukaryotic lineages (e.g., karyotic host, stating, “it is likely that protomitochondria invaded that containing animals and fungi) are clearly primitively aplastidic, their hosts just as modern predatory bacteria Bdellovibrio invade descending from ancestors that never had plastids. In consequence, prey bacteria”: “an amazing example of prokaryote-prokaryote in most (although not all) plastid-bearing eukaryotes, the resem- ‘emboîtement’ without phagocytosis.” Mind you, given that Bdel- blance between plastid and cyanobacterial structure and biochemis- lovibrio very effectively destroys its “host” bacterium in the process try is considerably more pronounced than in the mitochondrion/ of invading it, this type of scenario does offer a particularly promis- α-proteobacteria comparison. In addition, plastid genomes generally ing route to a stable prokaryote–prokaryote symbiosis. contain substantially more genes on which to base such a compari- The nature of the host is, in fact, central to widely differing sym- son than do mitochondrial genomes, and the plastid translation biogenesis models of mitochondrial origin and evolution, which system displays decidedly more bacterial character than does its fall into roughly two broad categories: mitochondria early (mito- counterpart in most mitochondrial systems (Gray, 1992). early, or mito-first) and mitochondria late (mito-late, or mito-last), Margulis’ treatment of the plastid in her 1967 article is remarkably differing on timing–within the transition from first eukaryotic com- brief: she simply asserted (p. 244) that “eukaryotic plant cells did not mon ancestor to LECA–and having different implications for the evolve oxygen-eliminating photosynthesis”; instead, “they acquired overall origin of the eukaryotic cell (Poole and Gribaldo, 2014). it by symbiosis” (from blue-green algae, i.e., cyanobacteria). She Comparative genomics and other analyses emphasize that the further suggested that “different photosynthetic eukaryotes (proto- LECA was already a complex organism with a fully functioning mi- plastids) were ingested by heterotrophic protozoans at various tochondrion (Koumandou et al., 2013) and that all supposedly ami- times” during evolution, becoming “obligately symbiotic plastids, tochondrial eukaryotic lineages (with one recently described ex- retaining their characteristic photosynthetic pigments and path- ception; Karnkowska et al., 2016) contain mitochondrion-related ways.” This theme of multiple plastid origins was later taken up by organelles and descend from mitochondria-containing ancestors. others (e.g., Raven, 1970). The current consensus,
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