Complex evolutionary history of photosynthesis in Bradyrhizobium

Abstract

Bradyrhizobium comprises a diverse group of bacteria with various lifestyles. Although best known for their nodule-based nitrogen-fixation in symbiosis with legumes, a select group of bradyrhizobia are also capable of photosynthesis. This ability seems to be rare among rhizobia, and its origin and evolution in these bacteria remain a subject of substantial debate. Therefore, our aim here was to investigate the distribution and evolution of photosynthesis in Bradyrhizobium using comparative genomics and representative genomes from closely related taxa in the families Nitrobacteraceae, Methylobacteriaceae, Boseaceae and Paracoccaceae. We identified photosynthesis gene clusters (PGCs) in 25 genomes belonging to three different Bradyrhizobium lineages, notably the so-called Photosynthetic, B. japonicum and B. elkanii supergroups. Also, two different PGC architectures were observed. One of these, PGC1, was present in genomes from the Photosynthetic supergroup and in three genomes from a species in the B. japonicum supergroup. The second cluster, PGC2, was also present in some strains from the B. japonicum supergroup, as well as in those from the B. elkanii supergroup. PGC2 was largely syntenic to the cluster found in Rhodopseudomonas palustris and Tardiphaga. Bayesian ancestral state reconstruction unambiguously showed that the ancestor of Bradyrhizobium lacked a PGC and that it was acquired horizontally by various lineages. Maximum-likelihood phylogenetic analyses of individual photosynthesis genes also suggested multiple acquisitions through horizontal gene transfer, followed by vertical inheritance and gene losses within the different lineages. Overall, our findings add to the existing body of knowledge on Bradyrhizobium’s evolution and provide a meaningful basis from which to explore how these PGCs and the photosynthesis itself impact the physiology and ecology of these bacteria.