Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-03T14:08:19.376Z Has data issue: false hasContentIssue false
  • English
  • Français

“Imperfections and oddities” in the origin of the nucleus

Published online by Cambridge University Press:  08 April 2016

Lynn Margulis ,
Michael F. Dolan  and
Jessica H. Whiteside
Lynn Margulis
Affiliation:
Department of Geosciences, University of Massachusetts, Amherst, Massachusetts 01003. E-mail: mdolan@geo.umass.edu
Michael F. Dolan
Affiliation:
Department of Geosciences, University of Massachusetts, Amherst, Massachusetts 01003. E-mail: mdolan@geo.umass.edu
Jessica H. Whiteside
Affiliation:
Department of Earth and Environmental Sciences. Lamont-Doherty Earth Observatory of Columbia University. Palisades, New York 10964. E-mail: jhw@ldeo.columbia.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

We outline a plausible evolutionary sequence that led from prokaryotes to the origin of the first nucleated cell. The nucleus is postulated to evolve after the archaebacterium and eubacterium merged to form the symbiotic ancestor of amitochondriate protists. Descendants of these amitochondriate cells (archaeprotists) today thrive in organic-rich anoxic habitats where they are amenable to study. Eukaryosis, the origin of nucleated cells, occurred by the middle Proterozoic Eon prior to the deposition in sediments of well-preserved microfossils such as Vandalosphaeridium and the spiny spheres in the Doushantou cherts of China.

Type
Macroevolutionary Patterns within and among Clades
Information
Paleobiology , Volume 31 , Issue S2 , 2005 , pp. 175 - 191
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Belgareh, N., Rabut, G., Bai, S. W., van Overbee, M., Beaudouin, J., Daigle, N., Zatsepina, O. V., Pasteau, F., Labas, V., Fromont-Racine, M., Ellenberg, J., and Doyle, V. 2001. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. Journal of Cell Biology 154:1147–1160.Google Scholar
Bermudes, D., Margulis, L., and Tzertzinis, G. 1987. Prokaryotic origin of undulipodia: application of the panda principle to the centriole enigma. Annals of the New York Academy of Sciences 503:187–197.Google Scholar
Bermudes, D., Hinkle, G., and Margulis, L. 1994. Do prokaryotes contain microtubules? Microbiology Reviews 58:387–400.Google Scholar
Breznak, J. A. 2000. Phylogenetic diversity and physiology of termite gut spirochetes. American Zoology 40:954–955.Google Scholar
Chapman, M. J., Dolan, M. F., and Margulis, L. 2000. Centrioles and kinetosomes: form, function, and evolution. Quarterly Review of Biology 75:409–429.Google Scholar
Cleveland, L. R. 1934. The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach, in collaboration withHall, S. R., Sanders, Elizabeth P., and Collier, JaneMemoirs of the American Academy of Arts and Sciences 17:185–342.Google Scholar
Cleveland, L. R. 1947. The origin and evolution of meiosis. Science 105:287–288.Google Scholar
Cleveland, L. R. 1963. Functions of flagellate and other centrioles in cell reproduction. Pp. 3–53in Levine, L., ed. The cell in mitosis. Academic Press, New York.Google Scholar
Cleveland, L. R., and Grimstone, A. V. 1964. The fine structure of the flagellate Mixotricha paradoxa and its associated microorganisms. Proceedings of the Royal Society of London B 159:668–686.Google Scholar
Cole, D. G., Diener, D. R., Himelblau, A., Beech, P. L., Fuster, J. C., and Rosenbaum, J. L. 1998. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. Journal of Cell Biology 141:993–1008.Google Scholar
Corliss, J. O. 1998. Oral communication discussion of his 1987 paper at American Society for Microbiology, Washington, D.C.Google Scholar
Corliss, J. O. 1987. Protistan phylogeny and eukaryogenesis. International Review of Cytology 100:319–370.Google Scholar
d'Ambrosio, U., Dolan, M. F., Wier, A. M., and Margulis, L. 1999. Devescovinid trichomonad with axostyle-based rotary motor (“Rubberneckia”): taxonomic assignment as Caduceia versatilis sp. nov. European Journal of Protistology 35:327–337.Google Scholar
Daniels, E. W., and Breyer, E. P. 1967. Ultrastructure of the giant amoeba, Pelomyxa palustris. Journal of Protozoology 14:167–179.Google Scholar
Darwin, C. 1859. On the origin of species. John Murray, London.Google Scholar
Dobzhansky, T. 1972. Nothing in biology makes sense except in the light of evolution. American Biology Teacher 35:125–129.Google Scholar
Dolan, M. F. 2005. The missing piece: the microtubule cytoskeleton and the origin of eukaryotes. Pp. 281–289in Sapp, J. ed. Microbial phylogeny and evolution: concepts and controversies. Oxford University Press, New York.Google Scholar
Dolan, M. F., Wier, A. M., and Margulis, L. 2000. Budding and asymmetric reproduction of a trichomonad with as many as 1000 nuclei in karyomastigonts: Metacoronympha from Incisitermes. Acta Protozoologica 33:275–280.Google Scholar
Dolan, M. F., Melnitsky, H., Margulis, L., and Kolnicki, R. 2002. Motility proteins and the origin of the nucleus. Anatomical Record 268:290–301.Google Scholar
Doxsey, S. J., Stein, P., Evans, L., Calarco, P., and Kirschner, M. 1994. Pericentrin, a highly conserved protein of centrosomes involved in microtubule organization. Cell 76:639–650.Google Scholar
Dubinina, G. A., Grabovich, M. Y., and Leshcheva, N. V. 1993a. Occurrence, structure, and metabolic-activity of Thiodendron sulfur mats in various saltwater environments. Microbiology 62:450–456.Google Scholar
Dubinina, G. A., Leshcheva, N. V., and Grabovich, M. Y. 1993b. The colorless sulfur bacterium Thiodendron is actually a symbiotic association of spirochetes and sulfidogens. Microbiology 62:432–444.Google Scholar
Dutcher, S. K. 2001. The tubulin fraternity: alpha to eta. Current Opinion in Cell Biology 13:49–54.Google Scholar
Dyson, F. 1985. Origins of life. Cambridge University Press, Cambridge.Google Scholar
Echeverri, C. J., Paschal, B. M., Vaughan, K. T., and Vallee, R. B. 1996. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. Journal of Cell Biology 132:617–633.Google Scholar
Erickson, H. P. 1997. FtsZ, a tubulin homologue in prokaryote cell division. Trends in Cell Biology 7:362–367.Google Scholar
Fraser, C. M., Norris, S. J., Weinstock, G. M., White, O., Sutton, G. G., Dodson, R., et al. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:375–388.Google Scholar
Fuerst, J. A., and Webb, R. I. 1991. Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proceedings of the National Academy of Sciences USA 88:8184–8188.Google Scholar
Gaglio, T., Dionne, M. A., and Compton, D. A. 1997. Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. Journal of Cell Biology 138:1055–1066.Google Scholar
Gould, S. J. 1986. Evolution and the triumph of homology, or why history matters. American Scientist 74:60–69Google Scholar
Gupta, R. S. 1998. Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiology and Molecular Biology Reviews 62:1435–1491.Google Scholar
Gupta, R. S. 2000. The natural evolutionary relationships among prokaryotes. Critical Reviews in Microbiology 26:111–131.Google Scholar
Hall, J. L., and Luck, D. J. L. 1995. Basal body-associated DNA: in situ studies in Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences USA 92:5129–5133.Google Scholar
Hardwick, K. G., and Murray, A. W. 1995. Madlp, a phosphoprotein component of the spindle assembly in budding yeast. Journal of Cell Biology 131:709–720.Google Scholar
Haren, L., and Merdes, A. 2002. Direct binding of NuMA to tubulin is mediated by a novel sequence motif in the tail domain that bundles and stabilizes microtubules. Journal of Cell Science 115:1815–1824.Google Scholar
Helenius, A., and Aebi, M. 2001. Intracellular functions of N-linked glycans. Science 291:2364–2369.Google Scholar
Janicki, C. 1915. Untersuchungen an parasitischen Flagellaten. Zeitschrift für Wissenschftliche Zoologie 112:573–691.Google Scholar
Jenkins, C., Samudrala, R., Anderson, I., Hedlund, B. P., Petroni, G., Michailova, N., Pinel, N., Overbeek, R., Rosati, G., and Staley, J. T. 2002. Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proceedings of the National Academy of Sciences USA 99:17049–17054.Google Scholar
Khodjakov, A., Cole, R. W., Oakley, B. R., and Rieder, C. L. 2000. Centrosome-independent mitotic spindle formation in vertebrates. Current Biology 10:59–67.Google Scholar
Khodjakov, A., and Rieder, C. L. 1999. The sudden recruitment of gamma-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle do not require microtubules. Journal of Cell Biology 146:585–596.Google Scholar
Kirby, H., annotated byMargulis, L. 1994. Harold Kirby's symbionts of termites: Karyomastigont reproduction and calonymphid taxonomy. Symbiosis 16:7–63.Google Scholar
Knoll, A. H. 2003. Life on a young planet: the first three billion years of evolution on Earth. Princeton University Press, Princeton, N.J.Google Scholar
Kolnicki, R. 2000. Kinetochore reproduction in animal evolution: cell biological explanation of karyotypic fission theory. Proceedings of the National Academy of Sciences USA 97:9493–9497.Google Scholar
Kumar, J., Yu, H., and Sheetz, M. P. 1995. Kinectin, an essential anchor for kinesin-driven vesicle motility. Science 267:1834–1837.Google Scholar
Lange, B. M. H., and Gull, K. 1995. A molecular marker for centriole maturation in the mammalian cell cycle. Journal of Cell Biology 130:919–927.Google Scholar
Leadbetter, J. R., Schmidt, T. M., Graber, J. R., and Breznak, J. A. 1999. Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689.Google Scholar
Leidy, J. 1850. On the existence of endophyta in healthy animals as a natural condition. Proceedings of the Academy of Natural Sciences of Philadelphia 4:225–229.Google Scholar
Leidy, J. 1881. The parasites of termites. Journal of the Academy of Natural Sciences of Philadelphia 8:425–447.Google Scholar
Lindsay, M. R., Webb, R. I., Strous, M., Jetter, M. S., Butler, M. K., Forde, R. J., and Fuerst, J. A. 2001. Cell compartmentalization in planctomycetes: novel types of structural organization for the bacterial cell. Archives of Microbiology 175:413–429.Google Scholar
Mack, G. J., and Compton, D. A. 2001. Analysis of mitotic microtubule-associated proteins using mass spectrometry identifies astrin, a spindle-associated protein. Proceedings of the National Academy of Sciences USA 98:14434–14439.Google Scholar
Maney, T., Hunter, A. W., Wagenbach, M., and Wordeman, L. 1998. Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. Journal of Cell Biology 142:787–801.Google Scholar
Margulis, L. 1991. Symbiosis in evolution: Origins of cell motility. Pp. 305–324in Honjo, T. and Osawa, S., eds. Evolution of life: fossils, molecules, and culture. Springer, Tokyo.Google Scholar
Margulis, L. 1993. Symbiosis in cell evolution, 2d ed. W. H. Freeman, New York.Google Scholar
Margulis, L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proceedings of the National Academy of Sciences USA 93:1071–1076.Google Scholar
Margulis, L. 2000. Spirochetes. Pp. 353–363in Lederberg, J., ed. Encyclopedia of Microbiology, Vol. 4, 2d ed.Academic Press, New York.Google Scholar
Margulis, L., and Dolan, M. F. 2004. Eukaryosis: origin of eukaryotic cells. Sony U-matic video. 16 minutes. Color. [Unpublished.]Google Scholar
Margulis, L., and Sagan, D. 1991. Origins of sex: three billion years of genetic recombination. Yale University Press, New Haven, Conn.Google Scholar
Margulis, L., Corliss, J. O., Melkonian, M., and Chapman, D. J., eds. 1990. Handbook of Protoctista: the structure, cultivation, habitats and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett, Boston.Google Scholar
Margulis, L., Dolan, M. F., and Guerrero, R. 2000. The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proceedings of the National Academy of Sciences USA 97:6954–6959.Google Scholar
Martin, W. 2005. Woe is the tree of life. Pp. 134–153in Sapp, J., ed. Microbial phylogeny and evolution: concepts and controversies. Oxford University Press, New York.Google Scholar
Melnitsky, H., and Margulis, L. 2004. Centrosomal proteins in termite symbionts: gamma–tubulin and a scleroderma antigen localize to the bacteria-free cell-rotation zone of the parabasalid Caduceia versatilis. Symbiosis 37:323–333.Google Scholar
Melnitsky, H., Rainey, F., and Margulis, L. 2005. The karyomastigont model of eukaryosis. Pp. 261–280in Sapp, J. ed. Microbial phylogeny and evolution: concepts and controversies. Oxford University Press, New York(in press).Google Scholar
Mignot, J. P. 1996. The centrosomal big bang: from a unique central organelle towards a constellation of MTOC's. Biology of the Cell 86:81–91.Google Scholar
Moritz, M., Braunfeld, M. B., Sedat, J. W., Alberts, B., and Agard, D. A. 1995. Microtubule nucleation by gamma-tubulin-containing rings in the centrosome. Nature 378:638–640.Google Scholar
Nicklas, R. B., Ward, S. C., and Gorbsky, G. J. 1995. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. Journal of Cell Biology 130:929–939.Google Scholar
Robson, S. K. 1987. Review of “Origin of sex: three billion years of genetic recombination” by L. Margulis and D. Sagan. Symbiosis 3:207–212.Google Scholar
Schopf, J. W. 1999. Cradle of life. Princeton University Press, Princeton, N.J.Google Scholar
Searcy, D. G., and Lee, S. H. 1998. Sulfur reduction by human erythrocytes. Journal of Experimental Zoology 282:310–322Google Scholar
Searcy, D. G., and Stein, D. B. 1980. Nucleoprotein subunit structure in an unusual prokaryotic organism: Thermoplasma acidophilum. Biochimica et Biophysica Acta 609:180–195.Google Scholar
Suh, M. R., Han, J. W., No, Y. R., and Lee, J. 2002. Transient concentration of a gamma-tubulin-related protein with a pericentrin-related protein in the formation of basal bodies and flagella during the differentiation of Naegleria gruberi. Cell Motility and the Cytoskeleton 52:66–81.Google Scholar
Surkov, A. V., Dubinina, G. A., Lynesko, A. M., Glöckner, F. O., and Kuever, J. 2001. Dethiosulfovibrio russensis sp. nov., Dethiosulfovibrio marinus sp. nov. and Dethiosulfovibrio acidaminovorans sp. nov., novel anaerobic, thiosulfate- and sulfur-reducing bacteria isolated from “Thiodendron” sulfur mats in different saline environments. International Journal of Systematic and Evolutionary Microbiology 51:327–337.Google Scholar
Toyoshima, I., Yu, H., Steuer, E. R., and Sheetz, M. P. 1992. Kinectin, a major kinesin-binding protein on ER. Journal of Cell Biology 118:1121–1131.Google Scholar
Vidal, G. 1998. Proterozoic and Cambrian bioevents. Revista Española de Paleontología, No. extr. Homenaje al Prof. Gonzalo Vidal, pp. 11–16.Google Scholar
Vidal, G., and Moczydłowska-Vidal, M. 1997. Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology 23:230–246.Google Scholar
Viscogliosi, E., Edgcomb, V. P., Gerbod, D., et al. 1999. Molecular evolution inferred from small subunit rRNA sequences: what does it tell us about phylogenetic relationships and taxonomy of the parabasalids? Parasite 6:279–291.Google Scholar
von Dohlen, C. D., Kohler, S., Alsop, S. T., and McManus, W. R. 2001. Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412:433–436.Google Scholar
Wang, J., Jenkins, C., Webb, R. I., Fuerst, J. A. 2002. Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Applied and Environmental Microbiology 68:417–422.Google Scholar
Wheatley, D. N. 1982. The centriole: a central enigma of cell biology. Elsevier, Amsterdam.Google Scholar
Wier, A., Ashen, J., and Margulis, L. 2000. Canaleparolina darzwiniensis, gen. nov. sp. nov., and other pillotinaceous spirochetes from insects. International Microbiology 3:213–223.Google Scholar
Wilson, E. B. 1925. The cell in development and heredity. Macmillan, New York.Google Scholar
Young, A., Dictenberg, J. B., Purohit, A., Tuft, R., and Doxsey, S. J. 2000. Cytoplasmic dynein-mediated assembly of pericentrin and gamma tubulin onto centrosomes. American Society for Cell Biology 11:2047–2056.Google Scholar
Zimmerman, W., and Doxsey, S. J. 2000. Construction of centrosomes and spindle poles by molecular motor-driven assembly of protein particles. Traffic 1:927–934.Google Scholar