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Acquisition of Cytoskeletal Motility from Aerotolerant Spirochetes in the Proterozoic Eon

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Acquisition of Cytoskeletal Motility from Aerotolerant Spirochetes in the Proterozoic Eon The last eukaryotic common ancestor (LECA): Acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon Lynn Margulis*†, Michael Chapman‡, Ricardo Guerrero§, and John Hall* *Department of Geosciences, University of Massachusetts, Amherst, MA 01003; §Department of Microbiology, University of Barcelona, 08028 Barcelona, Spain; and ‡Department of Biology, Holy Cross College, Worcester, MA 01610 Contributed by Lynn Margulis, July 10, 2006 We develop a symbiogenetic concept of the origin of eukaryotic associated with myosin-ATPases, intermediate filaments (12–14 intracellular motility systems from anaerobic but aerotolerant spiro- nm in diameter), and microtubules (24 nm) with microtubule- chetes in sulfide-rich environments. The last eukaryotic common associated proteins (MAPs) (dynein, kinesin, and other ATP- or ancestors (LECAs) have extant archaeprotist descendants: motile GTPases). We detail only the microtubular cytoskeleton, but a nucleated cells with Embden-Meyerhof glycolysis and substrate-level complete account of cell evolution must consider other motile phosphorylation that lack the ␣-proteobacterial symbiont that be- proteins. Three possibilities for the origin of the cytoskeleton came the mitochondrion. Swimming and regulated O2-tolerance via include (i) ancient origin from our genetically-not-yet-annealed sulfide oxidation already had been acquired by sulfidogenic wall-less ancestors (3), (ii) direct filiation from a prokaryotic ancestor, or archaebacteria (thermoplasmas) after aerotolerant cytoplasmic- (iii) symbiotic addition to a different eukaryotic ancestor. Lack tubule-containing spirochetes (eubacteria) attached to them. Increas- of precision of ‘‘genetically-not-yet-annealed’’ precludes inves- ing stability of sulfide-oxidizing͞sulfur-reducing consortia analogous tigation of the first. Continuous reevaluation of the assumed to extant sulfur syntrophies (Thiodendron) led to fusion. The eubac- second reveals slim evidence and terminology misused (2). Even teria–archaebacteria symbiosis became permanent as the nucleus the accepted concept of FtsZ (filament temperature-sensitive Z evolved by prokaryotic recombination with membrane hypertrophy, protein) as prokaryotic ancestor of tubulin protein is debatable analogous to Gemmata obscuriglobus and other ␦-proteobacteria (2). Symbiogenetic origin of intracellular motility including with membrane-bounded nucleoids. Histone-coated DNA, protein- mitosis, via addition of Spirochaeta to a Thermoplasma-like synthetic RNAs, amino-acylating, and other enzymes were contrib- archaebacterium (4–7), our concept, unlike other alternatives, uted by the sulfidogen whereas most intracellular motility derives explains superficially unrelated phenomena and generates de- from the spirochete. From this redox syntrophy in anoxic and mi- tails studiable by genomic, proteomic, cytologic, and geologic crooxic Proterozoic habitats LECA evolved. The nucleus originated by methods. recombination of eu- and archaebacterial DNA that remained at- tached to eubacterial motility structures and became the microtubular Results and Discussion cytoskeleton, including the mitotic apparatus. Direct LECA descen- Our evolutionary scenario, developed independently of molec- dants include free-living archaeprotists in anoxic environments: ar- ular sequence data, unlike others (8–10) reconstructs evolution- chamoebae, metamonads, parabasalids, and some mammalian sym- ary history from extant organisms (Fig. 1). Taken as represen- bionts with mitosomes. LECA later acquired the fully aerobic Krebs tative clues, many of the steps have been videographed in live cycle-oxidative phosphorylation-mitochondrial metabolism by inte- microbes. We show how both claims that no eukaryote ‘‘prim- gration of the protomitochondrion, a third ␣-proteobacterial symbi- itively lacked mitochondria’’ and ‘‘the evolutionary gap between ont from which the ancestors to most protoctists, all fungi, plants, and prokaryotes and eukaryotes is now deeper, and the nature of the animals evolved. Secondarily anaerobic eukaryotes descended from host that acquired the mitochondrion more obscure, than ever LECA after integration of this oxygen-respiring eubacterium. Explan- before’’ are based on protistological ignorance but rely on the atory power and experimental predictions for molecular biology of kind of molecular data that will support or disprove our model. the LECA concept are stated. New results mandate that aspects of our putative evolutionary (chronological) karyomastigont model be reconsidered and the karyomastigont ͉ kinetosome-centriole ͉ mitotic apparatus ͉ i nucleus origin ͉ Thiodendron only propositions disputed in scientific literature [( ) symbiotic origin of archaebacterial cytoplasm from sulfidogens, not meth- anogens, and (ii) nucleus-associated microtubule cytoskeleton he cytoskeleton in all eukaryotes comprises the mitotic preceded acquisition of mitochondria] be defended. Tspindle (often its kinetosome-centrioles within the centro- some), protist karyomastigonts (1), and neurotubules; the kin- 1. Hydrogen sulfide (H2S)-oxygen (O2) interface habitats etome of 10,000 species of ciliates; microtubules of foram abounded during the Proterozoic Eon (2,500–541 mya) granuloreticulopodia; submembranous microtubules of red throughout the world ocean as inferred from sedimentary, blood cells, trypanosomes, and many algae; and the undulipo- isotopic, and other geologic observation (11, 12). Worldwide dium (cilium-eukaryotic ‘‘flagellum’’ or intrinsically motile 0.25- localities show preservation of ancient eukaryotes mostly as ␮m-diameter ninefold symmetrical intracellular ‘‘whip’’ gener- microfossils in thin-section of cherty rock; nucleated cells ated from a kinetosome-centriole base). ‘‘This later structure is evolved before 1,000 mya in sulfidic, muddy habitats period- a highly complex organelle, composed of hundreds of proteins. ically well lit, dominated by cyanobacteria and therefore rich It has no bacterial homolog, and undoubtedly evolved into its current form after the evolution of microtubules. However, it is a remarkably standardized organelle across diverse eukaryotic Conflict of interest statement: No conflicts declared. taxa, which indicates that it evolved once in the early evolution Abbreviations: LECA, last eukaryotic common ancestor; MAP, microtubule-associated of eukaryotes’’ (2). protein. Movement inside cells, limited to eukaryotes, involves three †To whom correspondence should be addressed. E-mail: [email protected]. classes of structures: actin filaments (6–8 nm in diameter) © 2006 by The National Academy of Sciences of the USA 13080–13085 ͉ PNAS ͉ August 29, 2006 ͉ vol. 103 ͉ no. 35 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604985103 Downloaded by guest on September 23, 2021 Fig. 1. Karyomastigont model of origin of nucleated cells. The LECA evolved from eubacterial-archaebacterial syntrophies in which sulfide-oxidizing spirochetes attached to sulfidogenic thermoplasmas to form a ‘‘Thiodendron’’-like consortium. Archaeprotist (trichomonad Mixotricha paradoxa, lower right), CELL BIOLOGY LECA analogue in termite Mastotermes darwiniensis, swims via motility symbiosis with 200,000 Treponema sp. surface spirochetes. Four distinctive surface spirochetes are detected by morphological and molecular techniques (36). Chromatin appears first in the karyomastigont (‘‘kymstgnt’’), the precursor cytoskeletal organellar system from which the tethered nucleus (‘‘n’’) was released. in organics. Spirochetes, an ancient cohesive group of helical, tile nucleated cells with low levels of oxygen tolerance and motile chemoheterotrophic eubacteria, had evolved, in re- utilization. sponse to cyanobacterial oxygenesis, from their strictly an- Spirochetes detoxified fluctuating ambient gaseous oxygen EVOLUTION aerobic origin through aerotolerant-facultative aerobes, to by its conversion with sulfide to elemental sulfur usable by microaerophils like Leptospira (13, 14). Spirochetes, active Thermoplasma as terminal electron acceptor. Conferrence chemotactic swimmers, thrived in marine microbial mats, of motility on this redox syntrophy permitted both partners pond scums, and fresh and saline hot springs, where many, as access to organic-rich habitats that augmented survival and now, lived syntrophically. growth. Modern descendants of syntrophic consortia be- 2. The ancestors to which Spirochaeta were added were Thermo- came archaeprotists, motile premitochondriates amenable plasma-like sulfidogenic archaebacteria. This postulate, crit- to study. The Archaeprotista phylum, members riddled with ical to our model, was argued by Searcy (15–21) (Table 1). endo-, epi-, and even nuclear symbionts (22), includes the Thermoplasma acidophilum, heat- and acid-tolerant plei- archamoebae (pelomyxids, mastigoamoebae), metamonads omorphs that lack cell walls, are amenable to study as Retortamonas and Giardia, and parabasalids such as co-descendants of conserved archaebacterial features in eu- trichomonads, devescovinids, hypermastigotes, and cal- karyotes. Thermoplasma are predicted to enter metabolic onymphids (23, 24). Distinctive features of eukaryotic cells associations more easily than walled relatives. Their DNA, (e.g., archaebacterial-like transcription and translation in unlike most prokaryotes, is protected from hot acid by protein synthesis, histone-like proteins of nucleosomes and ‘‘nucleosomes,’’ a coating of arginine- and lysine-rich histone- chromatin, glucose catabolism, sulfide generation, ATP- like proteins (20,
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