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3 The Chimeric Eukaryote: Origin of the Nucleus from the Karyomastigont in Amitochondriate Protists LYNN MARGULIS*, MICHAEL F. DOLAN*, and RICARDO GUERREROâ¡ We present a testable model for the origin of the nucleus, the membrane-bounded organelle that defines eukaryotes. A chi- meric cell evolved via symbiogenesis by syntrophic merger between an archaebacterium and a eubacterium. The archae- bacterium, a thermoacidophil resembling extant Thermoplasma, generated hydrogen sulfide to protect the eubacterium, a het- erotrophic swimmer comparable to Spirochaeta or Hollandina that oxidized sulfide to sulfur. Selection pressure for speed swimming and oxygen avoidance led to an ancient analogue of the extant cosmopolitan bacterial consortium âThiodendron latens.â By eu- bacterial-archaebacterial genetic integration, the chimera, an ami- tochondriate heterotroph, evolved. This âearliest branching pro- tistâ that formed by permanent DNA recombination generated the nucleus as a component of the karyomastigont, an intracellular complex that assured genetic continuity of the former symbionts. The karyomastigont organellar system, common in extant amito- *Department of Geosciences, Organismic and Evolutionary Biology Graduate Program, University of Massachusetts, Amherst, MA 01003; and â¡Department of Microbiology, and Special Research Center Complex Systems (Microbiology Group), University of Barcelona, 08028 Barcelona, Spain This paper was presented at the National Academy of Sciences colloquium âVariation and Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins,â held January 27â29, 2000, at the Arnold and Mabel Beckman Center in Irvine, CA. 21
22 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero chondriate protists as well as in presumed mitochondriate ances- tors, minimally consists of a single nucleus, a single kinetosome and their protein connector. As predecessor of standard mitosis, the karyomastigont preceded free (unattached) nuclei. The nu- cleus evolved in karyomastigont ancestors by detachment at least five times (archamoebae, calonymphids, chlorophyte green al- gae, ciliates, foraminifera). This specific model of syntrophic chi- meric fusion can be proved by sequence comparison of function- al domains of motility proteins isolated from candidate taxa. Archaeprotists / spirochetes / sulfur syntrophy / Thiodendron / trichomonad TWO DOMAINS, NOT THREE A ll living beings are composed of cells and are unambiguously classifiable into one of two categories: prokaryote (bacteria) or eukaryote (nucleated organisms). Here we outline the origin of the nucleus, the membrane-bounded organelle that defines eukaryotes. The common ancestor of all eukaryotes by genome fusion of two or more different prokaryotes became âchimerasâ via symbiogenesis (Gupta and Golding, 1995). Long term physical association between metabolically dependent consortia bacteria led, by genetic fusion, to this chimera. The chimera originated when an archaebacterium (a thermoacidophil) and a motile eubacterium emerged under selective pressure: oxygen threat and scarcity both of carbon compounds and electron acceptors. The nucleus evolved in the chimera. The earliest descendant of this momentous merger, if alive today, would be recognized as an amitochondriate pro- tist. An advantage of our model includes its simultaneous consistency in the evolutionary scenario across fields of science: cell biology, develop- mental biology, ecology, genetics, microbiology, molecular evolution, paleontology, protistology. Environmentally plausible habitats and mod- ern taxa are easily comprehensible as legacies of the fusion event. The scheme that generates predictions demonstrable by molecular biology, especially motile protein sequence comparisons (Chapman et al., 2000), provides insight into the structure, physiology, and classification of microorganisms. Our analysis requires the two- (Bacteria/Eukarya) not the three- (Archaea/Eubacteria/Eukarya) domain system (Woese et al., 1990). The prokaryote vs. eukaryote that replaced the animal vs. plant dichotomy so far has resisted every challenge. Microbiologistâs molecular biology-based threat to the prokaryote vs. eukaryote evolutionary distinction seems idle (Mayr, 1998). In a history of contradictory classifications of microorgan- isms since 1820, Scamardella (1999) noted that Woeseâs entirely nonmor-
The Chimeric Eukaryote / 23 phological system ignores symbioses. But bacterial consortia and protist endosymbioses irreducibly underlie evolutionary transitions from pro- karyotes to eukaryotes. Although some prokaryotes [certain Gram-posi- tive bacteria (Gupta, 1998a)] are intermediate between eubacteria and archaebacteria, no organisms intermediate between prokaryotes and eu- karyotes exist. These facts render the 16S rRNA and other nonmor- phological taxonomies of Woese and others inadequate. Only all- inclusive taxonomy, based on the work of thousands of investigators over more than 200 years on live organisms (Margulis and Schwartz, 1998), suffices for detailed evolutionary reconstruction (Mayr, 1998). When Woese (1998) insists âthere are actually three, not two, primary phylogenetic groupings of organisms on this planetâ and claims that they, the âArchaebacteriaâ (or, in his term that tries to deny their bacterial nature, the âArchaeaâ) and the âEubacteriaâ are âeach no more like the other than they are like eukaryotes,â he denies intracellular motility, in- cluding that of the mitotic nucleus. He minimizes these and other cell biological data, sexual life histories including cyclical cell fusion, fossil record correlation (Margulis, 1996), and protein-based molecular com- parisons (Gupta, 1998a, b). The tacit, uninformed assumption of Woese and other molecular biologists that all heredity resides in nuclear genes is patently contradicted by embryological, cytological, and cytoplasmic he- redity literature (Sapp, 1999). The tubulin-actin motility systems of feed- ing and sexual cell fusion facilitate frequent viable incorporation of heter- ologous nucleic acid. Many eukaryotes, but no prokaryotes, regularly ingest entire cells, including, of course, their genomes, in a single phago- cytotic event. This invalidates any single measure alone, including ribo- somal RNA gene sequences, to represent the evolutionary history of a lineage. As chimeras, eukaryotes that evolved by integration of more than a single prokaryotic genome (Gupta, 1998b) differ qualitatively from prokaryotes. Because prokaryotes are not directly comparable to symbi- otically generated eukaryotes, we must reject Woeseâs three-domain interpretation. Yet our model greatly appreciates his archaebacterial- eubacterial distinction: the very first anaerobic eukaryotes derived from both of these prokaryotic lineages. The enzymes of protein synthesis in eukaryotes come primarily from archaebacteria whereas in the motility system (microtubules and their organizing centers), many soluble heat- shock and other proteins originated from eubacteria (Margulis, 1996). Here we apply Guptaâs idea (from protein sequences) (1998a) to compara- tive protist data (Dolan et al., 2000) to show how two kinds of prokaryotes made the first chimeric eukaryote. We reconstruct the fusion event that produced the nucleus.
24 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero THE CHIMERA: ARCHAEBACTERIUM\EUBACTERIUM MERGER Study of conserved protein sequences [a far larger data set than that used by Woese et al. (1990)] led Gupta (1998a) to conclude âall eukaryotic cells, including amitochondriate and aplastidic cells received major genetic contributions to the nuclear genome from both an archaebacterium (very probably of the eocyte, i.e., thermoacidophil group and a Gram-negative bacterium . . . [t]he ancestral eukaryotic cell never directly descended from archaebacteria but instead was a chimera formed by fusion and integration of the genomes of an archaebacerium and a Gram-negative bacteriumâ (p. 1487). The eubacterium ancestor has yet to be identified; Gupta rejects our spirochete hypothesis. In answer to which microbe pro- vided the eubacterial contribution, he claims: âthe sequence data . . . . suggest that the archaebacteria are polyphyletic and are close relatives of the Gram-positive bacteriaâ (p. 1485). The archaebacterial sequences, we posit, following Searcy (1992), come from a Thermoplasma acidophilum-like thermoacidophilic (eocyte) prokaryote. This archaebacterial ancestor lived in warm, acidic, and sporadically sulfurous waters, where it used either elemental sulfur (generating H2S) or less than 5% oxygen (generating H2O) as terminal electron acceptor. As does its extant descendant, the ancient archaebacterium survived acid-hydrolysis environmental condi- tions by nucleosome-style histone-like protein coating of its DNA (Searcy, 1992) and actin-like stress-protein synthesis (Searcy and Delange, 1980). The wall-less archaebacterium was remarkably pleiomorphic; it tended into tight physical association with globules of elemental sulfur by use of its rudimentary cytoskeletal system (Searcy and Hixon, 1994). The second member of the consortium, an obligate anaerobe, required for growth the highly reduced conditions provided by sulfur and sulfate reduction to hydrogen sulfide. Degradation of carbohydrate (e.g., starch, sugars such as cellobiose) and oxidation of the sulfide to elemental sulfur by the eubacterium generated carbon-rich fermentation products and electron acceptors for the archaebacterium. When swimming eubacteria attached to the archaebacterium, the likelihood that the consortium efficiently reached its carbon sources was enhanced. This hypothetical consortium, before the integration to form a chimera (Fig. 1), differs little from the widespread and geochemically important âThiodendronâ (Dubinina et al., 1993a, b). THE âTHIODENDRONâ STAGE The âThiodendronâ stage refers to an extant bacterial consortium that models our idea of an archaebacteria-eubacteria sulfur syntrophic motility symbiosis. The partners in our view merged to become the chimeric pre- decessor to archaeprotists. The membrane-bounded nucleus, by hypoth-
Prokaryotes Amitochondriate Eukaryotes archaebacteria protoeukaryote Thermoplasma-like "Thiodendron" stage eubacteria nucleated cell Spirochaeta- like with karyomastigont anoxic sulfuretum motility symbioses first archamoebas, DNA, membrane and protein fusion archaebacterial proteins and lipids DNA/genes in formation of elemental sulfur globules eubacterial proteins and lipids the nucleus FIGURE 1. Origin of the chimeric eukaryote with karyomastigonts from a motile sulfur-bacteria consortium. The Chimeric Eukaryote / 25
26 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero esis, is the morphological manifestation of the chimera genetic system that evolved from a Thiodendron-type consortium. Each phenomenon we suggest, from free-living bacteria to integrated association, enjoys extant natural analogues. Study of marine microbial mats revealed relevant bacterial consortia in more than six geographically separate locations. Isolations from Staraya Russa mineral spring 8, mineral spring Serebryani, Lake Nizhnee, mud- baths; littoral zone at the White Sea strait near Veliky Island, Gulf of Nilma; Pacific Ocean hydrothermal habitats at the Kurile Islands and Kraternaya Bay; Matupi Harbor Bay, Papua New Guinea, etc. (Dubinina et al., 1993a) all yielded âThiodendron latensâ or very similar bacteria. Samples were taken from just below oxygen-sulfide interface in anoxic waters (Dubinina et al., 1993a, b). Laboratory work showed it necessary to abolish the genus Thiodendron because it is a sulfur syntrophy. A stable ectosymbiotic associa- tion of two bacterial types grows as an anaerobic consortium between 4 and 32Â°C at marine pH values and salinities. Starch, cellobiose, and other carbo- hydrates (not cellulose, amino acids, organic acids, or alcohol) supple- mented by heterotrophic CO2 fixation provide it carbon. Thiodendron ap- pears as bluish-white spherical gelatinous colonies, concentric in structure within a slimy matrix produced by the consortium bacteria. The dominant partner invariably is a distinctive strain of pleiomorphic spirochetes: they vary from the typical walled Spirochaeta 1:2:1 morphology to large membra- nous spheres, sulfur-studded threads, gliding or nonmotile cells of variable width (0.09â0.45 Âµm) and lengths to millimeters. The other partner, a small, morphologically stable vibrioid, Desulfobacter sp., requires organic carbon, primarily acetate, from spirochetal carbohydrate degradation. The spiro- chetal Escherichia coli-like formic acid fermentation generates energy and food. Desulfobacter sp. cells that reduce both sulfate and sulfur to sulfide are always present in the natural consortium but in far less abundance than the spirochetes. We envision the Thiodendron consortium of âfree-living spiro- chetes in geochemical sulfur cycleâ (Dubinina et al., 1993b, p. 456) and spirochete motility symbioses (Margulis, 1993) as preadaptations for chi- mera evolution. Thiodendron differs from the archaebacterium-eubacterium association we hypothesize; the marine Desulfobacter would have been re- placed with a pleiomorphic wall-less, sulfuric-acid tolerant soil Thermo- plasma-like archaebacterium. New thermoplasmas are under study. We predict strains that participate in spirochete consortia in less saline, more acidic, and higher temperature sulfurous habitats than Thiodendron will be found. When âpure culturesâ that survived low oxygen were first described [by B. V. Perfilâev in 1969, in Russian (see Dubinina et al., 1993a, b)] a complex life history of vibrioids, spheroids, threads and helices was at- tributed to âThiodendron latens.â We now know these morphologies are
The Chimeric Eukaryote / 27 artifacts of environmental selection pressure: Dubinina et al. (1993a, p. 435), reported that âthe pattern of bacterial growth changes drastically when the redox potential of the medium is brought down by addition of 500 mg/l of sodium sulfide.â The differential growth of the two tightly associated partners in the consortium imitates the purported Thiodendron bacterial developmental patterns. The syntrophy is maintained by lower- ing the level of oxygen enough for spirochete growth. The processes of sulfur oxidation-reduction and oxygen removal from oxygen-sensitive enzymes, we suggest, were internalized by the chimera and retained by their protist descendants as developmental cues. Metabolic interaction, in particular syntrophy under anoxia, retained the integrated prokaryotes as emphasized by Martin and MÃ¼ller (1998). However, we reject their concept, for which no evidence exists, that the archaebacterial partner was a methanogen. Our sulfur syntrophy idea, by contrast, is bolstered by observations that hydrogen sulfide is still gener- ated in amitochondriate, anucleate eukaryotic cells (mammalian erythro- cytes) (Searcy and Lee, 1998). T. acidophilum in pure culture attach to suspended elemental sulfur. When sulfur is available, they generate hydrogen sulfide (Searcy and Hixon, 1994). Although severely hindered by ambient oxygen, they are microaero- philic in the presence of small quantities (<5%) of oxygen. The Thermoplasma partner thus would be expected to produce sulfide and scrub small quanti- ties of oxygen to maintain low redox potential in the spirochete association. The syntrophic predecessors to the chimera is metabolically analogous to Thiodendron where Desulfobacter reduces sulfur and sulfate producing sul- fide at levels that permit the spirochetes to grow. We simply suggest the replacement of the marine sulfidogen with Thermoplasma. In both the theo- retical and actual case, the spirochetes would supply oxidized sulfur as terminal electron acceptor to the sulfidogen. The DNA of the Thermoplasma-like archaebacterium permanently re- combined with that of the eubacterial swimmer. A precedent exists for our suggestion that membrane hypertrophies around DNA to form a stable vesicle in some prokaryotes: the membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus (Fuerst and Webb, 1991). The joint Thermoplasma-like archaebacterial DNA package that began as the consor- tium nucleoid became the chimeraâs nucleus. The two unlike prokaryotes together produced a persistent protein exudate package. This step in the origin of the nucleusâthe genetic inte- gration of the two-membered consortium to form the chimeraâis trace- able by its morphological legacy: the karyomastigont. The attached swim- mer partner, precursor to mitotic microtubule system, belonged to genera like the nearly ubiquitous consortium-former Spirochaeta or the cytoplas- mic tubule-maker Hollandina (Margulis, 1993). The swimmerâs attachment
28 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero structures hypertrophied as typically they do in extant motility symbio- ses (Margulis, 1993). The archaebacterium-eubacterium swimmer attach- ment system became the karyomastigont. The proteinaceous karyo- mastigont that united partner DNA in a membrane-bounded, jointly produced package, assured stability to the chimera. All of the DNA of the former prokaryotes recombined inside the membrane to become nuclear DNA while the protein-based motility system of the eubacterium, from the moment of fusion until the present, segregated the chimeric DNA. During the lower Proterozoic eon (2,500â1,800 million years ago), many interactions inside the chimera generated protists in which mitosis and eventually meiotic sexuality evolved. The key concept here is that the karyomastigont, retained by amitochondriate protists and later by their mitochondriate descendants, is the morphological manifestation of the original archaebacterial-eubacterial fused genetic system. Free (unat- tached) nuclei evolved many times by disassociation from the rest of the karyomastigont. The karyomastigont, therefore, was the first microtu- bule-organizing center. KARYOMASTIGONTS PRECEDED NUCLEI The term âkaryomastigontâ was coined by Janicki (1915) to refer to a conspicuous organellar system he observed in certain protists: the mas- tigont (âcell whip,â eukaryotic flagellum, or undulipodium, the [9 (2) + (2)] microtubular axoneme underlain by its [9 (3) + 0)] kinetosome) at- tached by a ânuclear connectorâ or ârhizoplastâ to a nucleus. The need for a term came from Janickiâs work on highly motile trichomonad symbionts in the intestines of termites where karyomastigonts dominate the cells. When kinetosomes, nuclear connector, and other components were pres- ent but the nucleus was absent from its predictable position, Janicki called the organelle system an âakaryomastigont.â In the Calonymphidae, one family of entirely multinucleate trichomonads, numerous karyomasti- gonts, and akaryomastigonts are simultaneously present in the same cell (e.g., Calonympha grassii) (Kirby and Margulis, 1994). The karyomastigont, an ancestral feature of eukaryotes, is present in âearly branching protistsâ (Dacks and Redfield, 1998; Delgado-Viscogliosi et al., 2000; Edgcomb et al., 1998). Archaeprotists, a large inclusive taxon (phylum of Kingdom Protoctista) (Margulis and Schwartz, 1998) are het- erotrophic unicells that inhabit anoxic environments. All lack mitochon- dria. At least 28 families are placed in the phylum Archaeprotista. Ex- amples include archaemoebae (Pelomyxa and Mastigamoeba), metamonads (Retortamonas), diplomonads (Giardia), oxymonads (Pyrsonympha), and the two orders of Parabasalia: Trichomonadida [Devescovina, Mixotricha, Monocercomonas, Trichomonas, and calonymphids (Coronympha, Snyderella)]
The Chimeric Eukaryote / 29 and Hypermastigida (Lophomonas, Staurojoenina, and Trichonympha). These cells either bear karyomastigonts or derive by differential organelle re- production (simple morphological steps) from those that do (Table 1). When, during evolution of these protists, nuclei were severed from their karyomastigonts, akaryomastigonts were generated (Kirby, 1949). Nu- clei, unattached, at least temporarily, to undulipodia were freed to prolif- erate and occupy central positions in cells. Undulipodia, also freed to proliferate, generated larger, faster-swimming cells in the same evolu- tionary step. The karyomastigont is the conspicuous central cytoskeleton in basal members of virtually all archaeprotist lineages [three classes: Arch- amoeba, Metamonads, and Parabasalia (Brugerolle, 1991)] (Fig. 2). In tri- chomonads, the karyomastigont, which includes a parabasal body (Golgi complex), coordinates the placement of hydrogenosomes (membrane- bounded bacterial-sized cell inclusions that generate hydrogen). The karyomastigont reproduces as a unit structure. Typically, four attached kinetosomes with rolled sheets of microtubules (the axostyle and its ex- tension the pelta) reproduce as their morphological relationships are re- tained. Kinetosomes reproduce first, the nucleus divides, and the two groups of kinetosomes separate at the poles of a thin microtubule spindle called the paradesmose. Kinetosomes and associated structures are parti- tioned to one of the two new karyomastigonts. The other produces com- ponents it lacks such as the Golgi complex and axostyle. Nuclear Î±-proteobacterial genes were interpreted to have originated from lost or degenerate mitochondria in at least two archaeprotist species [Giardia lamblia (Roger et al., 1998); Trichomonas vaginalis (Roger et al., 1996; Germont et al., 1996)] and in a microsporidian (Sogin, 1997). Hydrogeno- somes, at least some types, share common origin with mitochondria. In the hydrogen hypothesis (Martin and MÃ¼ller, 1998), hydrogenosomes are claimed to be the source of eubacterial genes in amitochondriates. That mitochondria were never acquired in the ancestors we consider more likely than that they were lost in every species of these anaerobic protists. Eubacterial genes in the nucleus that are not from the original spirochete probably were acquired in amitochondriate protists from proteobacterial symbionts other than those of the mitochondrial lineage. Gram-negative bacteria, some of which may be related to ancestors of hydrogenosomes, are rampant as epibionts, endobionts, and even endonuclear symbiontsâ for example, in Caduceia versatilis (dâAmbrosio et al., 1999). Karyomastigonts freed (detached from) nuclei independently in many lineages both before and after the acquisition of mitochondria. Calo- nymphid ancestors of Snyderella released free nuclei before the mitochon- drial symbiosis (Dolan et al., 2000), and Chlamydomonas-like ancestors of other chlorophytes such as Acetabularia released the nuclei after the lin-
30 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero eage was fully aerobic (Hall and Luck, 1995). In trophic forms of protists that lack mastigote stages, the karyomastigont is generally absent. An exception is Histomonas, an amoeboid trichomonad cell that lacks an ax- oneme but bears enough of the remnant karyomastigont structure to per- mit its classification with parabasalids rather than with rhizopod amoe- bae (Dyer, 1990). This organellar system appears in the zoospores, motile trophic forms, or sperm of many organisms, suggesting the relative ease of karyomastigont development. The karyomastigont, apparently in some cells, is easily lost, suppressed, and regained. In many taxa of multinucle- ate or multicellular protists (foraminifera, green algae) and even in plants, the karyomastigont persists only in the zoospores or gametes. In yeast, nematode, insect, and mammalian cells, nonkaryomastigont microtubule-organizing centers are ârequired to position nuclei at spe- cific locations in the cytoplasmâ (Raff, 1999). The link between the micro- tubule organizing center and the nuclei âis mysteriousâ (Raff, 1999). To TABLE 1. Karyomastigont distribution in unicellular protoctists Archaeprotista* Class Karyomastigont Kinetosome Nucleus Pelobiontids +â â + Metamonads + + +/â Parabasalids + + + Trichomonads + + +/â Hypermastigids â + â Chlorophyta Genus Karyomastigont Kinetosome Nucleus Chlamydomonas + + â Chlorella Acetabularia + + + Ciliophora Subphyla Karyomastigont Kinetosome Nucleus Postciliodesmatophora â + + Rabdophora â + + Cyrtophora â + + Discomitochondria Class Karyomastigont Kinetosome Nucleus Amoebomastigotes + â +/â Kinetoplastids â â â Euglenids â/? + â Pseudociliates â + â Granuloreticulosa Class Karyomastigont Kinetosome Nucleus Reticulomixids â/+ â + Foraminiferans + â +
The Chimeric Eukaryote / 31 us, the link is an evolutionary legacy, a remnant of the original arch- aebacterial-eubacterial connector. The modern organelles (i.e., centriole- kinetosomes, untethered nuclei, Golgi, and axostyles) derive from what first ensured genetic continuity of the chimeraâs components: the karyo- mastigont, a structure that would have been much more conspicuous to Proterozoic investigators than to us. We thank our colleagues Ray Bradley, Michael Chapman, Floyd Craft, Kathryn Delisle (for figures), Ugo dâAmbrosio, Donna Reppard, Dennis Searcy, and Andrew Wier. We acknowledge research assistance from the University of Massachusetts Graduate School via Linda Slakey, Dean of Natural Science and Mathematics, from the Richard Lounsbery Founda- tion, and from the American Museum of Natural History Department of Invertebrates (New York). Our research is supported by National Aero- nautics and Space Administration Space Sciences and Comision Inter- ministerial de Ciencia y Tecnologia Project No. AMB98-0338 (to R.G.). Hemimastigophora Genus Karyomastigont Kinetosome Nucleus Stereonema â + +/â Spironema â + â Hemimastix â + â Zoomastigota Class Karyomastigont Kinetosome Nucleus Jakobids ? â â Bicosoecids +/? + â Proteromonads + _ _ Opalinids â + + Choanomastigotes + â â *Bold entries are protoctist phyla. All species of Archaeprotists lack mitochondria. âKaryo- mastigont,â âkinetosome,â and ânucleus,â refer to relative proliferation of these organelles. Members of the phylum Archaeprotista group into one of three classes: Pelobiontid giant amoebae; Metamonads, which include three subclasses: Diplomonads (Giardia), Retorta- monads (Retortamonas), and Oxymonads (such as Pyrsonympha and Saccinobaculus); and Parabasalia. The Class Parabasalia unites trichomonads, devescovinids, calonymphids, and hypermastigotes such as Trichonympha. The phylum Discomitochondria includes amoebo- mastigotes, kinetoplastids (Trypanosoma), euglenids, and pseudociliates (Stephanopogon). The Hemimastigophora comprise a new southern-hemisphere phylum of free-living mitochon- driate protists (Foissner et al. 1988). Hemimastigophorans probably evolved from members of the kinetoplastid-euglenid taxon (Foissner and Foissner, 1993). If so, they represent a seventh example of release of the nucleus from the karyomastigont and subsequent kineto- some proliferation. The phylum Granuloreticulosa includes the shelled (Class Foramin- ifera) and unshelled (Class Reticulomyxa) foraminiferans. The phylum Zoomastigota in- cludes five classes of single-celled, free-living and symbiotrophic mitochondriate protists; Jakobids, Bicosoecids, Proteromonads, Opalinids, and Choanomastigotes. Details of the bi- ology are in the work by Margulis et al. (1993). A current phylogeny is depicted in Figure 2. â Structure known but not demonstrated for all species at the electron microscopic level.
Metamonads Giardia Archamoebae DIPLOMONADS Mastigamoeba-like RETORTAMONADS (ancestor) Retortamonas OXYMONADS Pyrsonympha Pelomyxa Parabasalids Metacoronympha MONOCERCOMONADS TRICHOMONADS TRICHOMONADIDS Coronympha nucleus Trichomonas CALONYMPHIDS DEVESCOVINIDS archaebacterial lipids, proteins karymastigont akarymastigont Devescovina 32 / Lynn Margulis, Michael F. Dolan, and Ricardo Guerrero FAMILIES Trichonympha ORDERS Calonymha Class- Stephanonympha HYPERMASTIGIDS Snyderella FIGURE 2. Biological phylogeny of chimeric eukaryotes taken to be primitively amitochondriate.
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