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The alphaproteobacterial genus Bradyrhizobium has been best known as N 2 -fixing members that nodulate legumes, supported by the nif and nod gene clusters. Recent environmental surveys show that Bradyrhizobium represents one of the most abundant free-living bacterial lineages in the world's soils. However, our understanding of Bradyrhizobium comes largely from symbiotic members, biasing the current knowledge of their ecology and evolution. Here, we report the genomes of 88 Bradyrhizobium strains derived from diverse soil samples, including both nif-carrying and non-nif-carrying free-living (nod free) members. Phylogenomic analyses of these and 252 publicly available Bradyrhizobium genomes indicate that nif-carrying free-living members independently evolved from symbiotic ancestors (carrying both nif and nod) multiple times. Intriguingly, the nif phylogeny shows that the vast majority of nif-carrying free-living members comprise an independent cluster, indicating that horizontal gene transfer promotes nif expansion among the free-living Bradyrhizobium. Comparative genomics analysis identifies that the nif genes found in free-living Bradyrhizobium are located on a unique genomic island of ~50 kb equipped with genes potentially involved in coping with oxygen tension. We further analyze amplicon sequencing data to show that Bradyrhizobium members presumably carrying this nif island are widespread in a variety of environments. Given the dominance of Bradyrhizobium in world's soils, our findings have implications for global nitrogen cycles and agricultural research.

Evolutionary origin and ecological implication of a unique nif island in free-living Bradyrhizobium lineages