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.

Bradyrhizobium ontarionense sp. nov., a novel bacterial symbiont isolated from Aeschynomene indica (Indian jointvetch), harbours photosynthesis, nitrogen fixation and nitrous oxide (N2O) reductase genes

“…BTAi1 and novel strain A19 T ). It is notable that the phylogenetic division of symbiotic and nonsymbiotic bradyrhizobia on the basis of puf gene analysis corresponds to the two types of photosynthetic gene clusters (PGC1 and PGC2, respectively) defined by Avontuur et al ( 2023 ). The organization of genes in the PGC of strain A19 T is similar to close relative B. oligotrophicum possessing a type 1 PGC but differs from non-symbiotic bacteria such as B. amphicarpaea carrying type 2 PGCs (Fig.…”

“…nov . strain A19 T and reference taxa showing division of Bradyrhizobium strains into two clades corresponding to photosynthetic gene cluster type 1 (PGC1) and type 2 (PGC2) as defined by Avontuur et al ( 2023 ). B Comparative arrangement of the photosynthesis gene cluster of Bradyrhizobium ontarionense sp.…”

“…Bacterial species possessing photosynthesis genes are distributed across the genus Bradyrhizobium (Avontuur et al 2023 ). These include apparently free-living (non-symbiotic) species such as B. betae (Rivas et al 2004 ; Cloutier and Bromfield 2019 ), B. amphicarpaeae (Bromfield et al 2019 ) and B. cosmicum (Wasai-Hara et al 2020b ).…”

“…These include apparently free-living (non-symbiotic) species such as B. betae (Rivas et al 2004 ; Cloutier and Bromfield 2019 ), B. amphicarpaeae (Bromfield et al 2019 ) and B. cosmicum (Wasai-Hara et al 2020b ). Others are represented by the species, B. oligotrophicum (Okubo et al 2013 ; Ramirez-Bahena et al 2013 ), ‘ B. aeschynomenes’ (Sun et al 2022 ), and, B. denitrificans (van Berkum et al 2006 ) that are symbionts of tropical plant species of the genus Aeschynomene , and based on core gene analyses, are placed exclusively in the so called “photosynthetic clade” (Avontuur et al 2023 ) of the genus Bradyrhizobium . These bacterial species lack the Type III Secretion System (T3SS) and nodulation ( nod ) genes needed for symbiosis by most rhizobia and yet are still capable of eliciting root- and stem-nodules on Aeschynomene species in a nodulation (nod) factor -T3SS independent manner (Giraud et al 2007 ; Camuel et al 2023 ).…”

Bradyrhizobium ontarionense sp. nov. isolated from Aeschynomene indica (Indian jointvetch) harbours photosynthesis, nitrogen fixation and nitrous oxide reductase genes.

“…Bacterial species possessing photosynthesis genes are distributed across the genus Bradyrhizobium (Avontuur et al 2023). These include apparently freeliving (non-symbiotic) species such as B. betae (Rivas et al 2004 ) that lack the Type III Secretion System (T3SS) and nodulation (nod) genes needed for symbiosis by most rhizobia and yet are still capable of eliciting root-and stem-nodules on tropical plant species of the genus Aeschynomene in a nodulation (nod) factor -T3SS independent manner (Giraud et al 2007;Camuel et al 2023).…”