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Symbiotic Models for Reconstruction of Organellogenesis

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Abstract

Various groups of proteobacteria and cyanobacteria, as well as unicellular algae capable of endosymbioses with eukaryotes, are addressed as the models for reconstruction of organellogenesis (transformation of symbiotic microbes into cellular organelles) as a major result of symbiogenesis—the evolution based on formation of integral hereditary systems by tightly interacting partners. Organellogenesis includes the following transitions: facultative non-inherited intracellular symbionts → obligatory inherited endocytobionts → genome-containing organelles → genome-free organelles. We have demonstrated that organellogenesis is accompanied by the loss of bacterial genetic individuality—the ability to maintain and express their own genomes, including their complete elimination. Comparative analysis of various groups of endosymbiotic bacteria showed that the major prerequisite for their transformation into organelles (primary organellogenesis) is high genomic plasticity expressed at the early stages of organellogenesis, under facultative or obligatory dependences on hosts. It is manifested as a directed change in genome architecture (transitions of unitary-type genomes to multicomponent- and reduced-type genomes), as well as in the export of functionally active genes into nonrelated organisms. These properties are characteristic for α-proteobacteria and cyanobacteria—the ancestors of mitochondria and plastids, but not for β- and γ-proteobacteria, Bacteroidetes and Firmicutes, which, although they include multiple endosymbiotic forms, have not been transformed into organelles. A convenient model for analyzing the secondary organellogenesis implemented by eukaryotic microorganisms is represented by dinoflagellates Symbiodinium (Alveolata), which (1) harbor chloroplasts derived from red algae and (2) develop intracellular symbioses with invertebrates behaving as their plastids. Reconstruction of organellogenesis allows us to address the early stages of organic evolution including the trade-off between metabolism and heredity, as well as between the RNA- or DNA-based genomes.

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The work was supported by the Russian Science Foundation, project no. 19-16-00081.

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Provorov, N.A. Symbiotic Models for Reconstruction of Organellogenesis. Russ J Genet 57, 10–22 (2021). https://doi.org/10.1134/S1022795421010117

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