Abstract
The symbiosis between rhizobial bacteria and legume plants has served as a model for investigating the genetics of nitrogen fixation and the evolution of facultative mutualism. We used deep sequence coverage (>100×) to characterize genomic diversity at the nucleotide level among 12 Sinorhizobium medicae and 32 S. meliloti strains. Although these species are closely related and share host plants, based on the ratio of shared polymorphisms to fixed differences we found that horizontal gene transfer (HGT) between these species was confined almost exclusively to plasmid genes. Three multi-genic regions that show the strongest evidence of HGT harbor genes directly involved in establishing or maintaining the mutualism with host plants. In both species, nucleotide diversity is 1.5–2.5 times greater on the plasmids than chromosomes. Interestingly, nucleotide diversity in S. meliloti but not S. medicae is highly structured along the chromosome – with mean diversity (θπ) on one half of the chromosome five times greater than mean diversity on the other half. Based on the ratio of plasmid to chromosome diversity, this appears to be due to severely reduced diversity on the chromosome half with less diversity, which is consistent with extensive hitchhiking along with a selective sweep. Frequency-spectrum based tests identified 82 genes with a signature of adaptive evolution in one species or another but none of the genes were identified in both species. Based upon available functional information, several genes identified as targets of selection are likely to alter the symbiosis with the host plant, making them attractive targets for further functional characterization.
Highlights
Analyses of genome sequences can provide a nearly complete description of the nature and extent of nucleotide diversity segregating within and among species
These data provide one of the most complete examinations of genomic diversity segregating within microbial species that are not causative agents of human illness
Our analyses reveal that horizontal gene transfer, a common source of new genes in microbial species, disproportionately affects genes with direct roles in the rhizobia-plant symbiosis
Summary
Analyses of genome sequences can provide a nearly complete description of the nature and extent of nucleotide diversity segregating within and among species. Prokaryotic species are often studied because they are either pathogens, of environmental or industrial importance, or because they form mutualistic associations with eukaryotes The latter group includes members of the genera Rhizobium, Sinorhizobium ( Ensifer), Bradyrhizobium, Azorhizobium, and Mesorhizobium, collectively referred to as the rhizobia, a group of gram-negative bacteria that form symbiotic associations with legume plants. When growing in symbiosis with legumes, rhizobia convert atmospheric nitrogen (N2), which is unavailable to plants, into ammonia, which plants can use for the synthesis of amino acids This symbiosis is estimated to contribute nearly half of all current biological nitrogen fixation [11] and is a key component of agricultural systems that are not dependent on synthetic fertilizers [12]
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