Abstract
BackgroundPhaseolus vulgaris (common bean) microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe. Individual symbiosis genes (e.g., nodC) of these rhizobia can be different within each genus and among distinct genera. Little information is available about the symbiotic structure of indigenous Rhizobium strains nodulating introduced bean plants or the emergence of a symbiotic ability to associate with bean plants in Bradyrhizobium and Ensifer strains. Here, we sequenced the genomes of 29 representative bean microsymbionts (21 Rhizobium, four Ensifer, and four Bradyrhizobium) and compared them with closely related reference strains to estimate the origins of symbiosis genes among these Chinese bean microsymbionts.ResultsComparative genomics demonstrated horizontal gene transfer exclusively at the plasmid level, leading to expanded diversity of bean-nodulating Rhizobium strains. Analysis of vertically transferred genes uncovered 191 (out of the 2654) single-copy core genes with phylogenies strictly consistent with the taxonomic status of bacterial species, but none were found on symbiosis plasmids. A common symbiotic region was wholly conserved within the Rhizobium genus yet different from those of the other two genera. A single strain of Ensifer and two Bradyrhizobium strains shared similar gene content with soybean microsymbionts in both chromosomes and symbiotic regions.ConclusionsThe 19 native bean Rhizobium microsymbionts were assigned to four defined species and six putative novel species. The symbiosis genes of R. phaseoli, R. sophoriradicis, and R. esperanzae strains that originated from Mexican bean-nodulating strains were possibly introduced alongside bean seeds. R. anhuiense strains displayed distinct host ranges, indicating transition into bean microsymbionts. Among the six putative novel species exclusive to China, horizontal transfer of symbiosis genes suggested symbiosis with other indigenous legumes and loss of originally symbiotic regions or non-symbionts before the introduction of common bean into China. Genome data for Ensifer and Bradyrhizobium strains indicated symbiotic compatibility between microsymbionts of common bean and other hosts such as soybean.
Highlights
Phaseolus vulgaris microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe
The 50 Rhizobium strains were classified into 19 clusters or species at the 95% average nucleotide identity (ANI) threshold for species delineation; this is consistent with the grouping results of digital DNA:DNA hybridization estimation and multilocus sequence analysis of housekeeping genes [15]
The 29 rhizobial genomes were used to investigate the evolution of symbiotic genes among indigenous Rhizobium strains nodulating introduced bean plants, and to assess the emergence of an ability to engage in symbiotic relationships with bean plants in Bradyrhizobium and Ensifer strains
Summary
Phaseolus vulgaris (common bean) microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe. (common bean) is an important leguminous food crop cultivated worldwide in a broad range of cropping systems and environments This species was domesticated from a wild-growing vine around 7000 years ago, in two primary centers of origin located in Mexico/Central America and the southern Andes (Ecuador, Peru, Chile, and Argentina) [3, 4]. The symbiovar (sv.) mediterranense in Ensifer (Sinorhizobium) meliloti [8], E. fredii [9], and E. americanum [10] can nodulate common bean plants in alkaline-saline soils. Some of these rhizobia have been detected in both the centers of origin and other areas because they can be introduced with common bean seeds [11]
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