Genomic Evolution of α-Proteobacteria in the Symbiotic System

Formation of symbioses with eukaryotic organisms is one of the major strategies for evolution of bacteria, accompanied by pronounced changes in their genetic organization. Eukaryotes provide their micropartners with nutrients and ecological niches, while bacteria perform trophic or protective functions useful for their hosts. Acquisition of the ability for symbiosis is associated with formation of specialized sym gene systems, which is often accompanied by structural modifications of the bacterial genome. Nodule bacteria (rhizobia) are N2-fixing symbionts of leguminous plants; most of them are α-proteobacteria of order Hyphomicrobiales. In this group, symbiogenic genome modifications vary depending on the taxonomic position. In the evolutionarily primary rhizobia of family Bradyrhizobiaceae, which emerged directly from free-living N2 fixers, transition to symbiosis was accompanied by a significant (by 1.5–2 times) increase in the genome size. However, their genomes have retained a unitary structure: most Bradyrhizobium strains carry more than 95% of genes in their chromosomes. Secondary rhizobia of the family Phyllobacteriaceae (Mesorhizobium, Phyllobacterium), which emerged by transfer of sym genes into soil bacteria, demonstrate various stages of multipartite genome formation where a significant part of genes is located in extrachromosomal elements (ECEs): plasmids and chromids. The multipartite genome structure is the most pronounced in members the family Rhizobiaceae (Rhizobium, Sinorhizobium, Neorhizobium): the total size of ECEs containing sym genes can exceed the size of the chromosome. In these bacteria, the transfer from tropical to temperate ecosystems was accompanied by a narrowing of the host specificity. However, modification of the genome structure was revealed only in members of Sinorhizobium, with proportion of ECEs reaching up to 52% of the total genome. Similar genome structure is observed in associative (rhizospheric or endophytic) N2 fixers of the genus Azospirillum, in which ECEs comprise up to 60% of a genome. Rhizobia can also form bacteroids: irreversibly differentiated N2-fixing cellular forms included into symbiosomes, temporary organelles that can be considered as precursors of N2-fixing organelles found in some protists. Construction of such organelles in crop plants represents a promising direction in plant bioengineering research.