Symbiosis in Evolution: Origins of Cell Motility

Origins of Cell Motility
  • Lynn Margulis


Summary. Using symbiosis in the DeBary sense of “living together of unlike organisms,” K.S. Mereschkowsky (1855–1921), on the basis of his original work, rejected Darwinian natural selection as source of evolutionary innovation [1]; he invented the term “symbiogenesis” referring to the appearance of new organisms emerging from prolonged symbiotic associations. A.S. Famintzyn (1835–1918) taught B.M. Kozo-Polyanski (1890–1957) who, in his 1924 text on new concepts in biology, attempted to unite Darwinian natural selection with symbiogenesis [2]. Kozo-Polyanski even claimed that cell motility was derived symbiotically from “flagellated cytodes” by which he meant “primitive flagellated bacteria.” The American I.E. Wallin (1883–1969) developed his theory of “symbionticism and the origin of species” [3] in the absence of direct communication with these Russian scientists, and he also elucidated the importance of symbiosis as the source of novelty in evolution.

Molecular biology and ultrastructural analysis has increased greatly the probability that these early biologists were correct in asserting the importance of symbiosis in evolution. The bacterial ancestry of plastids (from cyanobacteria) and mitochondria (from respiring bacteria) is now well established. Our independently- derived version of Kozo-Polyanski’s prophetic suggestion requires more rigorous proof; the status of the symbiotic origin of undulipodia is reviewed here.


Mitotic Spindle Evolutionary Innovation Darwinian Natural Selection Motile Bacterium Bacterial Flagellum 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Merschkowsky KS (1909) The theory of two plasms as the foundation of symbiogenesis: New knowledge concerning the origins of organisms (in Russian). KazanGoogle Scholar
  2. 2.
    Kozo-Polyanski BM (1924) New principles of biology (in Russian). Puchina, MoscowGoogle Scholar
  3. 3.
    Wallin IE (1927) Symbionticism and the origin of species. Williams and Wilkins, BaltimoreCrossRefGoogle Scholar
  4. 4.
    Shmagina AP (1948) Ciliary movement (in Russian). State Publishing house for medical Literature, MEDGIZ, MoscowGoogle Scholar
  5. 5.
    Seravin LN (1967) Advanced systems of protozoa: Structure, mechanochemistry and physiology. USSR Academy of Sciences Scientific Council on Problems of Cytology. “Science” Publishing House, LeningradGoogle Scholar
  6. 6.
    Hall JL, Ramanis Z, Luck DJL (1989) Basal body/centriolar DNA: Molecular genetic studies inChlamydomonas. Cell 59:121–132PubMedCrossRefGoogle Scholar
  7. 7.
    Khakhina LN (1979) Concepts of symbiogenesis (in Russian). Akademie NAUK, ( Soviet Academy of Sciences ), LeningradGoogle Scholar
  8. 8.
    Wilson EB (1928) The cell in development and heredity, 3rd edn. Macmillan, New YorkGoogle Scholar
  9. 9.
    Mehos D (1983) The symbionticism principle of Ivan E. Wallin. Master’s thesis, Boston University Graduate SchoolGoogle Scholar
  10. 10.
    Pierantoni (1948) Trattato di biologia e zoologia generale. Humus, NaplesGoogle Scholar
  11. 11.
    Buchner P (1965) Endosymbiosis of animals with plant–like microorganisms. Intersci– ence Publishers ( Wiley ), New YorkGoogle Scholar
  12. 12.
    Portier P (1918) Les symbiotes. Masson et Cie, ParisGoogle Scholar
  13. 13.
    Lumiere A (1919) Le myth des symbiotes. Masson et Cie, ParisGoogle Scholar
  14. 14.
    Gray MW (1983) Bacterial ancestry of mitochondria and plastids. Bioscience 33:693– 699Google Scholar
  15. 15.
    Margulis L (1981) Symbiosis in cell evolution. W.H. Freeman, San FranciscoGoogle Scholar
  16. 16.
    Margulis L, Sagan D (1986) Microcosmos: Four billion years of evolution from our bacterial ancestors. Summit, New YorkGoogle Scholar
  17. 17.
    Margulis L, Corliss JO, Melkonian M, Chapman D (eds) 1990. Handbook of Protoctis– ta: The structure, cultivation, habitats, and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants, and fungi. Jones and Bartlett, BostonGoogle Scholar
  18. 18.
    Bermudes D, Chase D, Margulis L (1988) Morphology as the basis of taxonomy in large spirochetes symbiotic in termites. Int J Syst Bacteriol 38: 291–302PubMedCrossRefGoogle Scholar
  19. 19.
    Hovind-Hougen K, Birch-Andersen A (1971) Electron microscopy of endoflagella and microtubules inTreponema Retier. Acta Pathol Microbiol Immunol Scand [B] 79: 37–50Google Scholar
  20. 20.
    Stewart KD, Mattox KR (1984) The case for polyphyletic origin of mitochondria: Morphological and molecular comparisons. J Molec Evol 21: 54–57PubMedCrossRefGoogle Scholar
  21. 21.
    Margulis L (1988) Serial Endosymbiotic Theory (SET): Undulipodia, mitosis and their microtubule systems preceded mitochondria. Internalt J of Endocytobiosis and Cell Research 5: 133–162Google Scholar
  22. 22.
    Margulis L, Hinkle G, Stolz JF, Craft F, Esteve I, Guerrero R (1990) Mobilifilum chasei: Morphology and ecology of a spirochete from an intertidal stratified microbial mat community. Arch Microbiol 153: 422–427PubMedCrossRefGoogle Scholar
  23. 23.
    Margulis L, Sagan (1985) Order amidst animalcules: The protoctista kingdom and its undulipodiated cells. Biosystems 18: 141–147PubMedCrossRefGoogle Scholar
  24. 24.
    Margulis L, Sagan D (1990) Origins of sex, Yale University Press, New Haven (Preface to the paperback ed, 2nd printing January 1990 ).Google Scholar
  25. 25.
    Allen RD (1969) The morphogenesis of basal bodies and accessory structures of the ciliated protozoanTetrahymena pyriform.J Protozool 14: 553–565Google Scholar
  26. 26.
    Dyer BD Zoomastigina. Chap. 14. In [17] aboveGoogle Scholar
  27. 27.
    Raikov I (1982) The protozoan nucleus. Springer, Heidelberg New YorkGoogle Scholar
  28. 28.
    Wheatley DN (1982) The centriole: A central enigma of cell biology. Elsevier Biomedical Press, New YorkGoogle Scholar
  29. 29.
    Nicklas RB (1989) The motor for poleward chromosome movement in anaphase is in or near the kinetochore. J Cell Biol 109: 2245–2255PubMedCrossRefGoogle Scholar
  30. 30.
    Ris H, Kubai D (1974) An unusual mitotic mechanism in the protozoanSyndinium sp. J Cell Biol 60: 702–720PubMedCrossRefGoogle Scholar
  31. 31.
    Szathmary E (1987) Early evolution of microtubules and undulipodia. Biosystems 20: 11–131CrossRefGoogle Scholar
  32. 32.
    Margulis L, Chase D, To L (1978) Microtubules in prokaryotes. Science 200:1118– 1123CrossRefGoogle Scholar
  33. 33.
    Bermudes D, Tzertzinis G, Obar R, Bosco G (unpublished manuscript)Google Scholar
  34. 34.
    Little M, Seehaus T (1988) Comp Biochem Physiol [Tubulin homology] 90B: 655–670CrossRefGoogle Scholar
  35. 35.
    Tzertzinis G (1987) Immunochemical characterization and partial amino acid sequence of tubulin-like protein fromSpirochaeta bajacaliforniensis. PhD disertation. Boston University Graduate SchoolGoogle Scholar
  36. 36.
    Bermudes D, Fracek SP Jr, Laursen RA, Margulis L, Obar R, Tzertzinis G (1987) Tubulinlike protein fromSpirochaeta bajacaliforniensis. Ann NY Acad Sci 503: 515–527CrossRefGoogle Scholar
  37. 37.
    Beisson J, TM Sonneborn (1965) Cytoplasmic inheritance of the organization of the cell cortex inParamecium aurelia. Proc Nat Acad Sci USA 53: 275–282PubMedCrossRefGoogle Scholar
  38. 39.
    Bermudes D, Margulis L, Tzertzinis G (1987) Prokaryotic origins of undulipodia: Application of the panda principle to the centriole enigma. Ann NY Acad Sci 503:187– 197PubMedGoogle Scholar
  39. 40.
    Strother PK (1989) Pre-metazoan life. In Allen KC, Briggs DEG (eds): Evolution and the fossil record. Belhaven, LondonGoogle Scholar
  40. 41.
    Law R (1989) New phenotypes from symbiosis. TREE 4: 334–335Google Scholar
  41. 42.
    Margulis L, Fester R, (eds) (to be published) Evolution and speciation: Symbiosis as a source of evolutionary innovation. MIT Press, CambridgeGoogle Scholar
  42. 43.
    Maynard-Smith J (1989) Generating novelty by symbiosis. Nature 341: 284–285CrossRefGoogle Scholar
  43. 44.
    Mereschkowsky KS (Merejkovsky C) (1920) La plante consideree comme un complexe symbiotique. Bull Soc Sci Nat 6: 17–98Google Scholar
  44. 45.
    Sagan L (Margulis L) (1967) On the origin of mitosing cells. J Theor Biol 14: 225–274CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Tokyo 1991

Authors and Affiliations

  • Lynn Margulis
    • 1
  1. 1.Department of BotanyUniversity of MassachusettsAmherstUSA

Personalised recommendations