Skip to main content
Log in

Endosymbiosis, cell evolution, and speciation

  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Abstract

In 1905, the Russian biologist C. Mereschkowsky postulated that plastids (e.g., chloroplasts) are the evolutionary descendants of endosymbiotic cyanobacteria-like organisms. In 1927, I. Wallin explicitly postulated that mitochondria likewise evolved from once free-living bacteria. Here, we summarize the history of these endosymbiotic concepts to their modern-day derivative, the “serial endosymbiosis theory”, which collectively expound on the origin of eukaryotic cell organelles (plastids, mitochondria) and subsequent endosymbiotic events. Additionally, we review recent hypotheses about the origin of the nucleus. Model systems for the study of “endosymbiosis in action” are also described, and the hypothesis that symbiogenesis may contribute to the generation of new species is critically assessed with special reference to the secondary and tertiary endosymbiosis (macroevolution) of unicellular eukaryotic algae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altmann, R., 1890. Die Elementarorganismen und ihre Beziehungen zu den Zellen. Verlag von Veit & Comp., Leipzig.

    Google Scholar 

  • Armbrust, E.V., Berges, J.A., Bowler, C., et al., 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79–86.

    Article  PubMed  CAS  Google Scholar 

  • Baldauf, S.L., Palmer, J.D., 1990. Evolutionary transfer of the chloroplast TufA gene to the nucleus. Nature 344, 262–265.

    Article  PubMed  CAS  Google Scholar 

  • Baluska, F., Volkmann, D., Barlow, P.W., 2004. Eucaryotic cells and their cell bodies: cell theory revised Ann. Bot. 94, 9–32.

    Article  PubMed  CAS  Google Scholar 

  • de Bary, A.H., 1878. Vortrag: Über Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp. 121–126.

    Google Scholar 

  • Bekker, A., Holland, H.D., Wang, P.-L., Rumble, D., Stein, H.J., Hanna, J.L., Coetzee, L.L., Beukes, N.J., 2004. Dating the rise of atmospheric oxygen. Nature 427, 117–120.

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shem, A., Frolow, F., Nelson, N., 2003. Crystal structure of plant photosystem I. Nature 426, 530–635.

    Article  CAS  Google Scholar 

  • Bhattacharya, D., Yoon, H.S., Hackett, J.D., 2003. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26, 50–60.

    Article  Google Scholar 

  • Cavalier-Smith, T., 1975. The origin of nuclei and of eukaryotic cells. Nature 256, 463–468.

    Article  Google Scholar 

  • Cavalier-Smith, T., 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5, 174–182.

    Article  PubMed  CAS  Google Scholar 

  • Cowen, R., 2000. History of Life, third ed. Blackwell Science, Oxford.

    Google Scholar 

  • Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer, Sunderland, MA.

    Google Scholar 

  • de Duve, C., 1996. The birth of complex cells. Sci. Am. 274 (4), 38–45.

    Article  Google Scholar 

  • Douglas, S., 1998. Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Dev. 8, 655–661.

    Article  PubMed  CAS  Google Scholar 

  • Douglas, A.E., Raven, J.A., 2003. Genomes at the interface between bacteria and organelles. Phil. Trans. R. Soc. Lond. B 358, 5–18.

    Article  CAS  Google Scholar 

  • Douglas, S., Zauner, S., Fraunholz, M., et al., 2001. The highly reduced genome of an enslaved algal nucleus. Nature 410, 1091–1096.

    Article  PubMed  CAS  Google Scholar 

  • Dyall, S.D., Brown, M.T., Johnson, P.J., 2004. Ancient invasions: from endosymbionts to organelles. Science 304, 253–257.

    Article  PubMed  CAS  Google Scholar 

  • Falkowski, P.G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O., Taylor, F.J.R., 2004. The evolution of modern eukaryotic phytoplankton. Science 305, 354–360.

    Article  PubMed  CAS  Google Scholar 

  • Famintzin, A., 1907. Die Symbiose als Mittel der Synthese von Organismen. Biol. Centralbl. 27, 353–363.

    Google Scholar 

  • Friedl, T., Bhattacharya, D., 2001. Origin and evolution of green lichen algae. Symbiosis 27, 341–357.

    Google Scholar 

  • Fröhlich, M., Kutschera, U., 1994. Chloroplast development in rye coleoptiles. Bot. Acta 107, 12–17.

    Google Scholar 

  • Graham, L.E., Wilcox, L.W., 2000. Algae. Prentice Hall, New Jersey.

    Google Scholar 

  • Gray, M.W., 1992. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141, 233–357.

    PubMed  CAS  Google Scholar 

  • Gray, M.W., Burger, G., Lang, B.F., 1999. Mitochondrial evolution. Science 283, 1476–1481.

    Article  PubMed  CAS  Google Scholar 

  • Hartman, H., Fedorov, A., 2002. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl. Acad. Sci. USA 99, 1420–1425.

    Article  PubMed  CAS  Google Scholar 

  • Hentschel, U., Steinert, M., Hacker, J., 2000. Common molecular mechanisms of symbiosis and pathenogenesis. Trends Microbiol. 8, 226–231.

    Article  PubMed  CAS  Google Scholar 

  • Hornschuh, M., Grotha, R., Kutschera, U., 2002. Epiphytic bacteria associated with the bryophyte Funaria hygrometrica: effects of Methylobacterium strains and protonema development. Plant Biol. 4, 682–687.

    Article  Google Scholar 

  • Höxtermann, E., 1998. Konstantin S. Merezkovskij und die Symbiogenesetheorie der Zellevolution. In: Geus, A. (Ed.), Bakterienlicht & Wurzelpilz. Endosymbiosen in Forschung und Geschichte. Basiliskenpresse, Marburg, pp. 11–29.

    Google Scholar 

  • Hurtado, L.A., Mateos, M., Lutz, R.A., Vrijenhoek, R.C., 2003. Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl. Environ. Microbiol. 69, 2058–2064.

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann, A.J., Xiao, S., 2003. High CO2 levels in the Proterozoic atmosphere estimated from analyses of individual microfossils. Nature 425, 279–282.

    Article  CAS  Google Scholar 

  • Keeling, P.J., 2004. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91, 1481–1493.

    Google Scholar 

  • Knoll, A.H., 2003. Life on a Young Planet: The First Billion Years of Evolution on Earth. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Koositra, W.H.C.F., De Stefano, M., Mann, D.G., Medlin, L., 2002. The phylogeny of diatoms. Progr. Mol. Subcell. Biol. 33, 59–97.

    Google Scholar 

  • Kühlbrandt, W., 2003. Dual approach to a light problem. Nature 426, 399–400.

    Article  PubMed  CAS  Google Scholar 

  • Kutschera, U., 2001. Evolutionsbiologie. Eine allgemeine Einführung. Parey Buchverlag, Berlin.

    Google Scholar 

  • Kutschera, U., 2002. Bacterial colonization of sunflower cotyledons during seed germination. J. Appl. Bot. 76, 96–98.

    Google Scholar 

  • Kutschera, U., 2003. A comparative analysis of the Darwin-Wallace papers and the development of the concept of natural selection. Theory Biosci. 122, 343–359.

    Google Scholar 

  • Kutschera, U., Hoss, R., 1995. Mobilization of starch after submergence of air-grown rice coleoptiles. Implications for growth and gravitropism. Bot. Acta 108, 266–269.

    CAS  Google Scholar 

  • Kutschera, U., Niklas, K.J., 2004. The modern theory of biological evolution: an expanded synthesis. Naturwissenschaften 91, 255–276.

    Article  PubMed  CAS  Google Scholar 

  • Kutschera, U., Siebert, C., Masuda, Y., Sievers, A., 1990. Effects of submergence on development and gravitropism in the coleoptile of Oryza sativa L. Planta 183, 112–119.

    Google Scholar 

  • Kuznetsov, A.P., Lebkova, N.P., 2002. On bacterial origin of mitochondria in Eukaryotes in light of current ideas of evolution of the organic world. Biol. Bull. 29, 501–507.

    Google Scholar 

  • Lang, B.F., Gray, M.W., Burger, G., 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33, 351–397.

    Article  PubMed  CAS  Google Scholar 

  • Lesser, M.P., Mazel, C.H., Gorbunov, M.Y., Falkowski, P.G., 2004. Discovery of symbiotic nitrogren-fixing cyanobacteria in corals. Science 305, 997–1000.

    Article  PubMed  CAS  Google Scholar 

  • Lloyd, D., 1974. The Mitochondria of Microorganisms. Academic Press, London.

    Google Scholar 

  • Logan, D.C., 2003. Mitochondrial dynamics. New Phytol. 160, 463–478.

    Article  CAS  Google Scholar 

  • Lopez-Garcia, P., Moreira, D., 1999. Metabolic symbiosis and the origin of eukaryotes. Trends Biochem. Sci. 24, 88–93.

    Article  PubMed  CAS  Google Scholar 

  • Mahner, M., Bunge, M., 1997. Foundations of Biophilosophy. Springer, Berlin, Heidelberg, New York.

    Google Scholar 

  • Maier, U.-G., Douglas, S.E., Cavalier-Smith, T., 2000. The nucleomorph genomes of Cryptophytes and Chlorarachinophytes. Protist 151, 103–109.

    Article  PubMed  CAS  Google Scholar 

  • Margulis, L., 1970. Origin of Eukaryotic Cells. Yale University Press, New Haven.

    Google Scholar 

  • Margulis, L., 1990. Words as battle cries—symbiogenesis and the new field of endocytobiology. BioScience 40, 673–677.

    Article  PubMed  CAS  Google Scholar 

  • Margulis, L., 1993. Symbiosis in Cell Evolution. Microbial Communities in the Archean and Proterozoic Eons, second ed. W. H. Freeman & Co., New York.

    Google Scholar 

  • Margulis, L., Sagan, D., 2002. Acquiring Genomes. A Theory of the Origin of Species. Basic Books. New York.

    Google Scholar 

  • Martin, W., 2003. Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc. Natl. Acad. Sci. USA 100, 8612–8614.

    Article  PubMed  CAS  Google Scholar 

  • Martin, W., Müller, M., 1998. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41.

    Article  PubMed  CAS  Google Scholar 

  • Martin, W., Russel, M.J., 2003. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic procaryotes, and from procaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B 358, 99–85.

    Article  CAS  Google Scholar 

  • Martin, W., Hoffmeister, M., Rotte, C., Henze, K., 2001. An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382, 1521–1539.

    Article  PubMed  CAS  Google Scholar 

  • Martin, W., Rotte, C., Hoffmeister, M., Theissen, U., Gelius-Dietrich, G., Ahr, S., Henze, K., 2003. Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55, 193–204.

    PubMed  CAS  Google Scholar 

  • Mayr, E., 2001. What Evolution Is. Basic Books, New York.

    Google Scholar 

  • McFadden, G., Gilson, P., 1995. Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis. Trends. Ecol. Evol. 10, 12–17.

    Article  Google Scholar 

  • Meeuson, S., McCaffery, J.M., Nunnari, J., 2004. Mitochondrial fusion intermediates revealed in vivo. Science 305, 1747–1752.

    Article  CAS  Google Scholar 

  • Mereschkowsky, C., 1905. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl. 25 593–604, 689–691.

    Google Scholar 

  • Mereschkowsky, C., 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenese, einer neuen Lehre von der Entstehung der Organismen. Biol. Centralbl. 30 278–303, 321–347, 353–367.

    Google Scholar 

  • Mereschkowsky, C., 1920. La plante considerée comme un complexe symbiotique. Bull. Soc. Sci. Nat. France 6, 17–98.

    Google Scholar 

  • Meyer, A., 2002. Viewing life as cooperation. Nature 418, 275–276.

    Article  CAS  Google Scholar 

  • Moran, N.A., Baumann, P., 2000. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3, 270–275.

    Article  PubMed  CAS  Google Scholar 

  • Morden, C.W., Sherwood, A.R., 2002. Continued evolutionary surprises among dinoflagellates. Proc. Natl. Acad Sci. USA 99, 11,558–11,560.

    Article  CAS  Google Scholar 

  • Moreira, D., Philippe, H., 2001. Sure facts and open questions about the origin and evolution of photosynthetic plastids. Res. Microbiol. 152, 771–787.

    Article  PubMed  CAS  Google Scholar 

  • Muscatine, L., Greene, R.W., 1973. Chloroplasts and algae as symbionts in molluscs. Int. Rev. Cytol. 36, 137–169.

    Article  PubMed  CAS  Google Scholar 

  • Niklas, K.J., 1997. The Evolutionary Biology of Plants. The University of Chicago Press, Chicago and London.

    Google Scholar 

  • Niklas, K.J., 2000. The evolution of plant body plans—a biomechanical perspective. Ann. Bot. 85, 411–438.

    Article  Google Scholar 

  • Niklas, K.J., 2004. The walls that bind the tree of life. BioScience 54, 831–841.

    Article  Google Scholar 

  • Nobles, P.R., Romanovicz, D.K., Brown, R.M., 2001. Cellulose in Cyanobacteria. origin of vascular plant cellulose synthase? Plant Physiol. 127, 529–542.

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung, K.W., Nunnari, J., 2003. The division of endosymbiotic organelles. Science 302, 1698–1704.

    Article  PubMed  CAS  Google Scholar 

  • Paschen, S.A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., Hell, R., Rapaport, D., Neupert, W., 2003. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426, 862–866.

    Article  PubMed  CAS  Google Scholar 

  • Pennisi, E., 2004. The birth of the nucleus. Science 305, 766–768.

    Article  PubMed  CAS  Google Scholar 

  • Rumpho, M.E., Summer, E.J., Manhart, J.R., 2000. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 123, 29–38.

    Article  PubMed  CAS  Google Scholar 

  • Sachs, J., 1882. Vorlesungen über Pflanzen-Physiologie. Verlag W. Engelmann, Leipzig.

    Google Scholar 

  • Saffo, M.B., 1992. Invertebrates in endosymbiotic associations. Am. Zool. 32, 557–565.

    Google Scholar 

  • Scherp, P., Grotha, R., Kutschera, U., 2001. Occurrence and phylogenetic significance of cytokinesis-related callose in green algae, bryophytes, ferns and seed plants. Plant Cell Rep. 20, 143–149.

    Article  CAS  Google Scholar 

  • Schilthuizen, M., 2001. Frogs, Flies and Dandelions. The Making of Species. Oxford University Press, Oxford.

    Google Scholar 

  • Schimper, A.F.W., 1885. Untersuchungen über die Chlorophyllkörper und die ihnen homologen Gebilde. Jahrb. f. wiss. Botanik 16, 1–247.

    Google Scholar 

  • Schopf, J.W., 1999. Cradle of Life. The Discovery of Earth’s Earliest Fossils. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Schwemmler, W., Schenk, H.E.A. (Eds.), 1980. Endocytobiology. Endosymbiosis and Cell Biology. Walter de Gruyter & Co., Berlin, New York.

    Google Scholar 

  • Sitte P., 1989. Phylogenetische Aspekte der Zellevolution. Biol. Rundsch. 28, 1–18.

    Google Scholar 

  • Sitte, P., 1991. Die Zelle in der Evolution des Lebens. Biol. in unserer Zeit 21, 85–92.

    Article  Google Scholar 

  • Sitte, P., 1994. Die Evolution von Zellen: Innovation durch Symbiogenese. In: Wieser, W. (Ed.), Die Evolution der Evolutionstheorie. Von Darwin zur DNA. Spektrum Akademischer Verlag, Berlin, Heidelberg, pp. 77–108.

    Google Scholar 

  • Sitte, P., 2001. Symbiogenese in der Zell und Lebensevolution. In: Storch, V., Welsch, U., Wink, M. (Eds.), Evolutionsbiologie. Springer, Berlin, Heidelberg, pp. 196–208.

    Google Scholar 

  • Stoebe, B., Maier, U.-G., 2002. One, two, three: nature’s tool box for building plastids. Protoplasma 219, 123–130.

    Article  PubMed  Google Scholar 

  • Taylor, F.J.R., 1979. Symbionticism revisited: a discussion of the evolutionary impact of intracellular symbioses. Proc. R. Soc. Lond. B. 204, 267–286.

    PubMed  CAS  Google Scholar 

  • Thompson, J.N., 1987. Symbiont-induced speciation. Biol. J. Linn. Soc. 32, 385–393.

    Article  Google Scholar 

  • Tice, M.M., Lowe, D.R., 2004. Photosynthetic microbial mats in the 3416-Myr-old ocean. Nature 431, 549–552.

    Article  PubMed  CAS  Google Scholar 

  • Timmis, J.N., Ayliffe, M.A., Huang, C.Y., Martin, W., 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123–135.

    Article  PubMed  CAS  Google Scholar 

  • Vargas, W., Cumino, A., Salerno, G.L., 2003. Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol? Planta 216, 951–960.

    PubMed  CAS  Google Scholar 

  • Walden, W.E., 2002. From bacteria to mitochondria: aconitase yields surprises. Proc. Natl. Acad. Sci. USA 99, 4138–4140.

    Article  PubMed  CAS  Google Scholar 

  • Wallin, I.E., 1927. Symbionticism and the Origin of Species Bailliere, Tindall & Cox, London.

    Google Scholar 

  • Whitefield, J., 2004. News feature: time lords. Nature 429, 124–125.

    Article  PubMed  CAS  Google Scholar 

  • Whitehead, L.F., Day, D.A., 1997. The peribacteroid membrane. Physiol. Plant 100, 30–44.

    Article  CAS  Google Scholar 

  • Wilkinson, D.M., 2001. At cross purposes. Nature 412, 485.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, E.B., 1925. The Cell in Development and Heredity, third ed. McMillan Co., New York.

    Google Scholar 

  • Woese, C.R., 2002. On the evolution of cells. Proc. Natl. Acad. Sci. USA 99, 8742–8747.

    Article  PubMed  CAS  Google Scholar 

  • Xu, M.-Q., Kathe, S.D., Coodrich-Blair, H., Nierzwicki-Bauer, S.A., Shub, D.A., 1990. Bacterial origin of a chloroplast intron: conserved self-splicing Group I introns in cyanobacteria. Science 250, 1566–1572.

    Article  PubMed  CAS  Google Scholar 

  • Yaffe, M.P., 1999. The machinery of mitochondrial inheritance and behavior. Science 283, 1493–1497.

    Article  PubMed  CAS  Google Scholar 

  • Yang, J., Cheng, Q., 2004. Origin and evolution of the light-dependent Protochlorophyllide Oxidoreductase (LPOR) genes. Plant Biol. 6, 537–544.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, M., Mileykovskaya, W., Dowhan, X., 2002. Glueing the respiratory chain together. J. Biol. Chem. 277, 43553–43556.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to U. Kutschera.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kutschera, U., Niklas, K.J. Endosymbiosis, cell evolution, and speciation. Theory Biosci. 124, 1–24 (2005). https://doi.org/10.1016/j.thbio.2005.04.001

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.thbio.2005.04.001

Keywords

Navigation