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Proc. Natl. Accad. Sci. USA Vol. 93, pp. 1071-1076, February 1996 Evolution Archaeal- eubacterial mergers in the origin of Eukarya: Phylogenetic classification of life (centriole-kinetosome DNA/Protoctista/kingdom classification/symbiogenesis/archaeprotist) LYNN MARGULIS Department of Biology, University of Massachusetts, Amherst, MA 01003-5810 Conitribluted by Lynnl Marglulis, September 15, 1995 ABSTRACT A symbiosis-based phylogeny leads to a con- these features evolved in their ancestors by inferable steps (4, sistent, useful classification system for all life. "Kingdoms" 20). rRNA gene sequences (Trichomonas, Coronympha, Giar- and "Domains" are replaced by biological names for the most dia; ref. 11) confirm these as descendants of anaerobic eu- inclusive taxa: Prokarya (bacteria) and Eukarya (symbiosis- karyotes that evolved prior to the "crown group" (12)-e.g., derived nucleated organisms). The earliest Eukarya, anaero- animals, fungi, or plants. bic mastigotes, hypothetically originated from permanent If eukaryotes began as motility symbioses between Ar- whole-cell fusion between members of Archaea (e.g., Thermo- chaea-e.g., Thermoplasma acidophilum-like and Eubacteria plasma-like organisms) and of Eubacteria (e.g., Spirochaeta- (Spirochaeta-, Spirosymplokos-, or Diplocalyx-like microbes; like organisms). Molecular biology, life-history, and fossil ref. 4) where cell-genetic integration led to the nucleus- record evidence support the reunification of bacteria as cytoskeletal system that defines eukaryotes (21)-then an Prokarya while subdividing Eukarya into uniquely defined optimal explanation for Table I's large quantity of otherwise subtaxa: Protoctista, Animalia, Fungi, and Plantae. baffling sequence data ensues (Table 2). Nucleoid membranes are known in at least one prokaryote, Gemmata obscuriglobus (24), and membrane hypertrophy is Bacterial Symbioses Form Cells of Eukarya common in invasive associations implying nuclear-endomem- brane systems originated as defensive response in bacterial Here I detail implications of serial endosymbiotic theory (SET; mergers (4). Centriole-kinetosomes are thought derived from ref. 1) of origins of nucleated organisms for interpretation of attached eubacteria (Fig. 1) such that centriole-kinetosome molecular data and classification of all life. Eukaryotes evolved DNA (c-kDNA; refs. 25 and 26) is their vestige (4, 21). when archaeal (2) (=archaebacterial) and eubacterial cells A great distinction is made between prokaryotic genomes no merged in ahaerobic symbiosis. Nucleocytoplasm (from Ar- matter their recombinant source or number per cell (e.g., chaea) acquired swimming motility (from fermenting Eubac- Escherichia coli's same-genome multiple nucleoids when fis- teria) becoming mastigotes prior to acquisition of mitochon- sion is retarded) and composite genomes derived from genetic dria or plastids (3, 4). Some mastigotes then incorporated integration of symbionts. Archaea and eubacteria, no matter purple Eubacteria (mitochondria precursors) to become oxy- their vast RNA, protein, and metabolic differences, are nev- gen-respiring aerobes from which most protoctists, animals, ertheless prokaryotes. They lack the system that underlies and fungi evolved. Aerobes in later permanent association with mendelian genetics (composite heterospecific genomes, intra- plastid-precursor cyanobacteria became algae-i.e., phototro- cellular motility, and cell fusion) and therefore are united into phic protoctists (5). one most inclusive taxon: Prokarya. Nucleated organisms, Individuality reappears as former symbionts integrate and products of symbiont integration of two or more former branches on bifurcating phylogenies anastomose to generate prokaryotes, are placed in the second taxon: Eukarya. new name-requiring taxa. The necessary and sufficient expla- nation of simultaneous archaeal and eubacterial protein and Protoctista nucleic acid sequences (refs. 2, 5-13; Table 1) even in amito- chondriate eukaryotes is their origin as genetically integrated The Eukarya taxon (equivalent to "Superkingdom" or "Do- bacterial symbionts. The consequences of the SET phylogeny main") includes amitochondriate mastigotes [Archeozoa (27), for systematics (evolutionary classification) includes replace- Hypochondria (13), here Archaeprotista], organisms derived ment of ad hoc gene transfer hypotheses (10), social-political from symbioses between as few as two prokaryote types. terms like Kingdom or Domain (2), and other confusion with Meiosis and fertilization are known in some: parabasalids a consistent taxonomy for identifying, naming, and classifying (Barbulanympha) and pyrsonymphids (Notila; ref. 28). Meio- all life. tic-sexual cycles did not evolve in all Archaeprotista as Kirby Comparable to extant prokaryotic consortia-e.g., Thioden- showed for large Calonymphidae trichomonads (29). These dron (15), Methanobacillus omelianski (16), and Daptobacter- amitochondriate multikinetosome mastigotes are multinucle- infected chromatia (17)-the earliest symbioses that became ated. They bear numerous akaryomastigonts (four-kinetosome eukaryotic cells lacked mitosis and meiosis. Abiding in anoxic structures that lack their connected nucleus) and karyomas- environments today are free-living amitochondriate motile tigonts (four-kinetosome organelles attached to a nucleus) heterotrophs, mastigotes, related to animal intestinal symbi- peculiar to the family. Akaryomastigont kinesis outpaced onts (18, 19). They vary in number of nuclei, organization of karyomastigont kinesis such that the akaryomastigonts out- chromatin, kinetochores, Golgi-parabasal bodies, rhizoplast number the nuclei in the genera Calonympha, Stephanoniym- nucleus-kinetosome connectors, [9(2)+21 microtubule-based pha, and Snyderella (29). From DNA staining in Calonympha intracellular motility organelles (undulipodia), centriole- grassii akarymastigonts (*) we infer that certain centriole- kinetosome-mitotic spindles, and meiotic sexuality, suggesting kinetosomes retained their genes. The nuclear internalization of c-kDNA (i.e., in Chlamydomonas; ref. 26) probably oc- The publication costs of this article were defrayed in part by page charge payment. This articlc must therefore be hereby marked "advertisement" in *Dolan, M., Second European Congress of Protistology, July 24-28, accordance with 18 U.S.C. §1734 solely to indicate this fact. 1995, Clermont-Ferrand, France, p. 42 (abstr.). 1071 Downloaded by guest on September 26, 2021 1072 Evolution: Margulis Proc. Natl. Acad. Sci. USA 93 (1996) Table 1. Prokarya origins of Eukarya components: Eubacterial Table 2. Hypothetical source of eukaryotic features and archacal protein contributions to the nucleocytoplasm of eukaryotes Spirochaeta sp. Thermoplasnma sp. (or related eubacterium) (or related archae) Eubacteria Archaea Undulipodium: undulating Acid, heat resistance Aminto acid metabolism/proteini synthesis swimming motility Aspartate aminotransferase Arginosuccinate synthetase Centriole-kinetosomes Membrane ATPases and lipids, Glutamine synthetase Elongation factor 2 (centrosomes, centroplasts) H +-ATPase Glutamate dehydrogenase Elongation factor Tu Spindle tubules, axonemes Chromatin with nucleosomal Aminoacyl tRNA synthetase organization, histones, (isoleucyl-, leucyl-, valyl-) (8) lamins Ubiquitin; proteosomes* Eubacterial genes, proteins* Archaebacterial polymerases Modified rRNA3, 5' ppp on 5SrRNA* and protein-synthetic Methionine initiation apparatus; other Fermentation/energy metabolism archaebacterial enzymes* Ferredoxin Cytoplasmic a-chain, /3-chain HI 02 hypersensitivity 02 microaerophilia vacuolar-type ATPase Retractiont Pleiomorphism (absence of cell Glyceraldehyde-3- Phosphoglycerol kinase wall) phosphate H2 productiont Sulfur respiration§ dchydrogenase (9) Resistant propagule formationt Cytoskeletal fibers$ Nutcleotide/lnlcleic acid metabolisnm Emergent after fusion and integration: amitochondriate mastigotes Formylglycinylmide Carbamoyl-phosphate synthaset (Phylum Archaeprotista of Table 4), nuclear envelope with 8-fold ribonucleotide symmetrical pores, mitosis, Ca2+-sensitive physiologies, actin- and synthetaset myosin-based phagocytosis, fluid (reversibly fusing) membranes, mo- Pyrroline-5-carboxylate Indole-3-glycerol phosphate tility-based morphogenesis, programmed cell hybrid formation. reductase DNA-directed RNA polymerase *See Table 1 (6, 7). DNA polymerase tSpirosynmplokos deltaeiberi provides an example of a spirochete pre- DNA topoisomeraset adaptation of undulipodial withdrawal into the cell and perhaps even Histone-DNA binding proteins resistant propagule formation (22). Histidine pathwayt tFermentation product. Fibrillamina of nucleolus §Thermoplasma grows anaerobically if in contact with elemental sulfur particles as electron acceptors. Most membranes SThese structures reported in mycoplasms (23); their presence in Ester-linked lipids, Amino acid-Na+ cotransport protein Thermoplasma requires investigation. phospholipids Isoprenoid membrane lipids (ethers) Striess proteinl mitochondriate aerobes (nucleocytoplasm/centriole-kineto- hsp7O (DnaK) hsp6() chaperonin, cocytes (TCP-1) some/mitochondria). These include malarial parasites, cili- Vitaninl antd storage metabolism ates, and amoebae, whereas those of at least four genomes Dihydrofolate reductase (nucleocytoplasm/centriole- kinetosome/mitochondria/ Glycogen or cytoplasmic "floridean" plastids) include euglenids, diatoms, chrysophytes, coccolith- starch ophorids, and brown and red algae (Table 3). Protoctists in Carbolhydrate
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