Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2016, Vol. 51, № 5, p. 746-758.

doi: 10.15389/agrobiology.2016.5.746eng

UDC 573.22:581.55

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

 

K.S. MEREZHKOVSKY AND THE ORIGIN OF THE EUKARYOTIC CELL:
111 YEARS OF SYMBIOGENESIS THEORY

N.A. Provorov

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

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.

 

Full article (Rus)

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