Evolution of root nodule bacteria: Reconstruction of the speciation processes resulting from genomic rearrangements in a symbiotic system


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Abstract

The processes of speciation and macroevolution of root nodule bacteria (rhizobia), based on deep rearrangements of their genomes and occurring in the N2-fixing symbiotic system, are reconstructed. At the first stage of rhizobial evolution, transformation of free-living diazotrophs (related to Rhodopseudomonas) to symbiotic N2-fixers (Bradyrhizobium) occurred due to the acquisition of the fix gene system, which is responsible for providing nitrogenase with electrons and redox potentials, as well as for oxygen-dependent regulation of nitrogenase synthesis in planta, and then of the nod genes responsible for the synthesis of the lipo-chitooligosaccharide Nod factors, which induce root nodule development. The subsequent rearrangements of bacterial genomes included (1) increased volume of hereditary information supported by species, genera (pangenome), and individual strains; (2) transition from the unitary genome to a multicomponent one; and (3) enhanced levels of bacterial genetic plasticity and horizontal gene transfer, resulting in formation of new genera—of which Mesorhizobium, Rhizobium, and Sinorhizobium are the largest—and of over 100 species. Rhizobial evolution caused by development and diversification of the Nod factor-synthesizing systems may result in either relaxed host specificity range (transition of Bradyrhizobium from autotrophic to symbiotrophic carbon metabolism in interaction with a broad spectrum of legumes) or narrowed host specificity range (transition of Rhizobium and Sinorhizobium to “altruistic” interaction with legumes of the galegoid clade). Reconstruction of the evolutionary pathway from symbiotic N2-fixers to their free-living ancestors makes it possible to initiate the studies based on up-to-date genome screening technologies and aimed at the issues of genetic integration of organisms into supraspecies complexes, ratios of the macro- and microevolutionary mechanisms, and development of cooperative adaptations based on altruistic interaction between the symbiotic partners.

About the authors

N. A. Provorov

All-Russia Research Institute for Agricultural Microbiology

Author for correspondence.
Email: provorov@newmail.ru
Russian Federation, St. Petersburg

E. E. Andronov

All-Russia Research Institute for Agricultural Microbiology

Email: provorov@newmail.ru
Russian Federation, St. Petersburg

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