Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations

Abstract

The rhizobium–legume symbiosis has been widely studied as the model of mutualistic evolution and the essential component of sustainable agriculture. Extensive genetic and recent genomic studies have led to the hypothesis that many distinct strategies, regardless of rhizobial phylogeny, contributed to the varied rhizobium–legume symbiosis. We sequenced 26 genomes of Sinorhizobium and Bradyrhizobium nodulating soybean to test this hypothesis. The Bradyrhizobium core genome is disproportionally enriched in lipid and secondary metabolism, whereas several gene clusters known to be involved in osmoprotection and adaptation to alkaline pH are specific to the Sinorhizobium core genome. These features are consistent with biogeographic patterns of these bacteria. Surprisingly, no genes are specifically shared by these soybean microsymbionts compared with other legume microsymbionts. On the other hand, phyletic patterns of 561 known symbiosis genes of rhizobia reflected the species phylogeny of these soybean microsymbionts and other rhizobia. Similar analyses with 887 known functional genes or the whole pan genome of rhizobia revealed that only the phyletic distribution of functional genes was consistent with the species tree of rhizobia. Further evolutionary genetics revealed that recombination dominated the evolution of core genome. Taken together, our results suggested that faithfully vertical genes were rare compared with those with history of recombination including lateral gene transfer, although rhizobial adaptations to symbiotic interactions and other environmental conditions extensively recruited lineage-specific shell genes under direct or indirect control through the speciation process.

Genetic Diversity and Evolution of Bradyrhizobium Populations Nodulating Erythrophleum fordii, an Evergreen Tree Indigenous to the Southern Subtropical Region of China

“…T indicated the significance of exploitation for microsymbionts associated with the endangered and rare legume trees (19,38).…”

The tRNA arg Gene and engA Are Essential Genes on the 1.7-Mb pSymB Megaplasmid of Sinorhizobium meliloti and Were Translocated Together from the Chromosome in an Ancestral Strain

“…The Sinorhizobium genus is expanding as new root nodule isolates are identified from diverse leguminous plants and geographic regions (14,43,56,(77)(78)(79). It will be interesting to see how the chromosome or megaplasmid location of the engA and tRNA arg genes segregates in these newly identified Sinorhizobium species.…”

“…Furthermore, both the engA and tRNA arg genes were located on the chromosome for Sinorhizobium fredii strains NGR234, USDA257, and HH103 (45)(46)(47) and nine recently sequenced Sinorhizobium strains (seven S. fredii strains, one Sinorhizobium sojae strain, and one Sinorhizobium sp. strain [56]). Since S. meliloti and S. medicae form a monophyletic group, we hypothesized that the engA and tRNA arg genes were chromosomally encoded in an early Rhizobiaceae ancestor and that following the divergence of S. meliloti from S. fredii, but before the split from S. medicae, these genes were transferred to the precursor of the pSymB megaplasmid.…”

Genetic Analysis Reveals the Essential Role of Nitrogen Phosphotransferase System Components in Sinorhizobium fredii CCBAU 45436 Symbioses with Soybean and Pigeonpea Plants

“…S. fredii strains can establish symbiosis with diverse legumes, including the important crops soybean (G. max, with determinate nodules) and pigeonpea (C. cajan, with indeterminate nodules) (34)(35)(36)(37). CCBAU 45436 represents a dominant sublineage of S. fredii that nodulates soybeans in alkaline-saline soils (17,38,39). A mutant forming rough colonies was found in a Tn5 mutant library of CCBAU 45436 constructed previously in our lab (27).…”

“…The GenBank accession number for the S. fredii CCBAU 45436 draft genome assembly is GCA_000261885.1 (17). Sequences of related genes described in this study are available in the supplemental material.…”