doi: 10.15389/agrobiology.2016.5.746eng

UDC 573.22:581.55

Supported by Russian Science Foundation (project 14-26-00094).



N.A. Provorov

All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations,3, sh. Podbel’skogo, St. Petersburg, 196608 Russia,

Received June 13, 2016


Theory of symbiogenesis proposed 111 years ago by K.S. Mereschkowsky, postulated the emergence of plants through the integration of phototrophic microbes into heterotrophic host cells. To date, it has become apparent that this theory can be used to describe an extremely wide range of evolutionary processes induced in the systems of cooperative adaptation. We have proposed a new definition of symbiogenesis as of a multi-stage process converting the symbiotic system into the entire organism (holobiont), based on the formation of an integral partners’ system of heredity. This system emerges in the course of transition of partners from facultative to obligatory symbiosis and evolves from the functional integrity, based on the signaling partners’ interactions (symbiogenome) to the structural integrity, based on the exchange of partners’ genes (hologenome). Trade-off between the proposed approach with the symbiogenesis theory of K.S. Mereschkowsky is shown using the material of paper «The nature and origin of chromatophores in the plant kingdom» (C. Mereschkowsky 1905. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biologisches Centralblatt 25: 593-604). We analyzed the relationship of traditional argumentation of symbiogenesis (genetic continuity of the cellular organelles based on their transmission in the host reproduction) with its current argumentation, used by the Theory of Serial Endosymbioses (TSE) proposed by L. Margulis: a) the presence of rudimental organelle genomes; b) phylogenetic kinship of organelles with the free-living and symbiotic microorganisms; c) identification of the transitional cellular forms linking the free-living bacteria and organelles. Modern versions of TSE suggest that the introduction of aerobic a-proteobacteria into anaerobic archaea gave rise to eukaryotes, which further evolved through the recruiting into their cellular structures of additional endosymbionts, including phototrophic cyanobacteria and viruses. The forms of archaea, close to the common ancestor of eukaryotes, are represented by the newly discovered chemotrophic Lokiarchaeota which cells are characterized by a number of eukaryotic features, including the actin cytoskeleton and the ability for endocytosis. Convincing evidence in favor of TSE was obtained in the study of cyanelles (phototrophic symbionts of protozoa, combining the properties of free-living cyanobacteria and plastids), as well as insects’ endocytobionts with the deeply reduced genome (less than 200 kb), which, in contrast to mitochondria and plastids, retained the ability to implement independently the basic template processes — replication, transcription, translation. One of the intriguing destinations of modern TSE is the analysis of the emergence of the nucleus and chromosomes, which may be associated with the introduction of highly organized «giant» DNA-viruses into ancestral cellular forms having RNA genomes (the hypothesis of viral eukaryogenesis).

Keywords: symbiogenesis theory, evolution of bacterial genome, plastids and mitochondria, origin of eukaryotic cell, holobiont, hologenome and symbiogenome, theory of serial endosymbiosis.


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  1. Mereschkowsky C. Uber Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl., 1905, 25: 593-604 (addendum in 25: 689-691).
  2. Martin W., Kowallik K.V. Annotated English translation of Mereschkowsky's 1905 paper «Uber Natur und Ursprung der Chromatophoren im Pflanzenreiche». Eur. J. Phycol., 1999, 34: 287-295.
  3. Famintzin A.S., Baranetzky O.V. Zur Entwickelungsgeschichte der Gonidien und Zoosporenbildung der Flechten. Mémoires de l’Académie imp. des sciences de St.-Pétersbourg, 7 serié, 1867, 11: 1-35.
  4. Famintsyn A.S. Zapiski Imperatorskoi akademii nauk, fiz.-mat. otd., seriya 8, 1907, 20: 1-14 (in Russ.).
  5. Read C.R. Parasitism and symbiology. 1st edition. NY, 1970.
  6. de Bary A. Uber Symbiose. Versammlung deutscher Naturforscher und Aerzte in Cassel, 1878, 51: 121-126.
  7. Provorov N.A. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2014, 3: 113-126 CrossRef (in Russ.).
  8. Tikhonovich I.A., Provorov N.A. Genetika, 2012, 48: 437-450 (in Russ.).
  9. Merezhkovskii K.S. Teoriya dvukh plazm kak osnova simbiogenezisa, novogo ucheniya o proiskhozhdenii organizmov [The theory of two plasmas as a basis of symbiogenesis, the new doctrine of the origin of organisms]. Kazan', 1909 (in Russ.).
  10. Mereschkowsky C. Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol. Centralbl., 1910, 30: 278-288.
  11. Nageli C. Blaschenformige Gebilde im Inhalte der Pflanzenzelle. Z. Wiss. Bot., 1846, 3/4: 94-128.
  12. Schimper A.F.W. Uber die Entwickelung der Chlorophyllkorner und Farbkorper. Bot. Zeit., 1883, 41: 105-113.
  13. Schimper A.F.W. Untersuchungen uber die Chlorophyllkorner und die ihnen homologen Gebilde. Jahrb. Wiss. Bot., 1885, 16: 1-247.
  14. Schmitz F. Die Chromatophoren der Algen. Vergleichende Untersuchungen uber Bau und Entwicklung der Chlorophyllkorper und analogen Farbstoffkorper der Algen. Verhandlungen des Naturwissenschaftlichen Vereins der Preussischen Rheinlande und Westfalen, 1883, 40: 1-180.
  15. Rumpho M.E., Worful J.M., Lee J. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. PNAS USA, 2008, 105: 17867-17871 CrossRef
  16. Hoxtermann E. Konstantin S. Merezkovskij und die Symbiogenesetheorie der Zellevolution. In: Bakterienlicht und Wurzelpilz. A. Geus (ed.). Marburg, 1998: 11-29.
  17. Gross J., Bhattacharya D. Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective. Nat. Rev. Genet., 2009, 10: 495-505 CrossRef
  18. Wallin I.E. Symbionticism and the origin of species. London, 1927.
  19. Wilson E.B. The Cell in development and heredity, 3d edition. NY, 1928.
  20. Chatton E. Pansporella perplexa. Réflexions sur la biologie et la phylogenie des protozoaires. Ann. Sci. Nat. Zool. 10èserie, 1923, 7: 1-84.
  21. Zakharov-Gezekhus I.A. Vavilovskii zhurnal genetiki i selektsii, 2014, 18: 93-102 (in Russ.).
  22. Sagan L. On the origin of mitosing cells. J. Theor. Biol., 1967, 14: 225-274.
  23. Margulis L. Rol' simbioza v evolyutsii kletki [The role of symbiosis in cell evolution]. Moscow, 1983 (in Russ.).
  24. Kozo-Polyanskii B.M. Novyi printsip biologii. Ocherk teorii simbiogeneza [The new principle of biology. Essay on symbiogenesis theory]. Leningrad-Moscow, 1924 (in Russ.).
  25. Smith D.R., Lee R.W. A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol., 2014, 164: 1812-1819 CrossRef
  26. Rizotti M. Non-symbiotic origin of locomotory organelles. In: Symbiosis: mechanisms and model systems. J. Seckbach (ed.). Dordrecht, Boston, London, 2002: 99-110.
  27. Gabaldón T., Snel B., van Zimmeren F., Hemrika W., Tabak H., Huyn-
    en M.A. Origin and evolution of the peroxisomal proteome. Biol. Direct., 2006, 1: 8 CrossRef
  28. Rogers M.B., Patron N.J., Keeling P.J. Horizontal transfer of a eukaryotic plastid-targeted protein gene to cyanobacteria. BMC Biol., 2007, 5: 26 CrossRef
  29. Price D.C., Chan C.X., Yoon H.S., Yang E.C., Qiu H., Weber A.P., Schwacke R., Gross J., Blouin N.A., Lane C., Reyes-Prieto A., Durnford D.G., Neilson J.A., Lang B.F., Burger G., Steiner J.M., Löffelhardt W., Meuser J.E., Posewitz M.C., Ball S., Arias M.C., Henrissat B., Coutinho P.M., Rensing S.A., Symeonidi A., Doddapaneni H., Green B.R., Rajah V.D., Boore J., Bhattacharya D. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science, 2012, 335: 843-847 CrossRef
  30. Douglas A.E. The molecular basis of bacterial—insect symbiosis. J. Mol. Biol., 2014, 426: 3830-3837 CrossRef
  31. Spang A., Saw J.H., Jørgensen S.L., Zaremba-Niedzwiedzka K., Martijn J., Lind A.E., van Eijk R., Schleper C., Guy L., Ettema T.J. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature, 2015, 521: 173-179 CrossRef
  32. Guy L., Ettema T.J. The archaeal TACK superphylum and the origin of eukaryotes. Trends in Microbiol., 2011, 19: 580-587 CrossRef
  33. Margulis L., Sagan D. Acquiring genomes. A theory of the origins of species. NY, 2002.
  34. Zilber-Rosenberg I., Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev., 2008, 32: 723-735 CrossRef
  35. Provorov N.A., Tikhonovich I.A. Zhurnal obshchei biologii, 2014, 75: 247-260 (in Russ.).
  36. Forterre P. Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. PNAS USA, 2006, 103: 3669-3674 CrossRef
  37. Witzany G. The viral origins of telomeres and telomerases and their important role in eukaryogenesis and genome maintenance. Biosemiotics, 2008, 1: 191-206 CrossRef
  38. Di Giulio M. The universal ancestor and the ancestors of Archaea and Bacteria were anaerobes whereas the ancestor of the Eukarya domain was an aerobe. J. Evol. Biol., 2007, 20: 543-548 CrossRef