Diversity analyses of Aeschynomene symbionts in Tropical Africa and Central America reveal that nod‐independent stem nodulation is not restricted to photosynthetic bradyrhizobia

Abstract

SummaryTropical aquatic legumes of the genus Aeschynomene are unique in that they can be stem-nodulated by photosynthetic bradyrhizobia. Moreover, a recent study demonstrated that two Aeschynomene indica symbionts lack canonical nod genes, thereby raising questions about the distribution of such atypical symbioses among rhizobial-legume interactions. Population structure and genomic diversity were compared among stem-nodulating bradyrhizobia isolated from various Aeschynomene species of Central America and Tropical Africa. Phylogenetic analyses based on the recA gene and whole-genome amplified fragment length polymorphism (AFLP) fingerprints on 110 bacterial strains highlighted that all the photosynthetic strains form a separate cluster among bradyrhizobia, with no obvious structuring according to their geographical or plant origins. Nod-independent symbiosis was present in all sampling areas and seemed to be linked to Aeschynomene host species. However, it was not strictly dependent on photosynthetic ability, as exemplified by a newly identified cluster of strains that lacked canonical nod genes and efficiently stemnodulated A. indica, but were not photosynthetic. Interestingly, the phenotypic properties of this new cluster of bacteria were reflected by their phylogenetical position, as being intermediate in distance between classical root-nodulating Bradyrhizobium spp. and photosynthetic ones. This result opens new prospects about stem-nodulating bradyrhizobial evolution.

Genetic Diversity, Symbiotic Evolution, and Proposed Infection Process of Bradyrhizobium Strains Isolated from Root Nodules of Aeschynomene americana L. in Thailand

“…strains BTAi1 and ORS278, which nodulate A. indica and A. sensitiva belonging to CI group 3, respectively. These strains lack classical nodulation genes, so they are called "nod-independent strains" (27). In addition, a photosynthetic Bradyrhizobium strain, ORS285, from A. afraspera (CI group 2) was found to have coexistence of 2 nodulation mechanisms-a classical nod-dependent one with A. afraspera and a nod-independent one with A. indica (29).…”

“…Bradyrhizobia have been described in the nodules of Aeschynomene (39), and most studies have focused on photosynthetic bradyrhizobial strains nodulating on Aeschynomene that belong to CI group 2 and CI group 3 (27). Extensive studies have been done for photosynthetic Bradyrhizobium sp.…”

“…Members of CI group 2, such as A. afraspera and A. nilotica, and CI group 3, such as A. indica and A. sensitiva, are nodulated on their roots and stems. CI group 2 is nodulated by both nonphotosynthetic and photosynthetic bradyrhizobia, which are also able to nodulate CI group 3 (27). CI group 3 is only nodulated by photosynthetic bradyrhizobia, such as Bradyrhizobium sp.…”

“…Aeschynomene establishes a symbiotic relationship with bacteria belonging to the genus Bradyrhizobium, and the nitrogen-fixing nodules are formed on roots and/or stems (28,29). Three cross-inoculation (CI) groups among Aeschynomene species have been described according to their symbiotic bacteria (27). Members of CI group 1, such as A. americana and A. elaphroxylon, are nodulated only on their roots by nonphotosynthetic bradyrhizobia.…”

Replicon-Dependent Differentiation of Symbiosis-Related Genes in Sinorhizobium Strains Nodulating Glycine max

“…As symbiotic bacteria, two categories of genomic components, core and accessory genomes, have been reported (3,4), and the symbiosis genes (nif, nod, and many other related genes) are a part of the accessory genome. However, the canonical nodABC genes are not required in some Bradyrhizobium strains for symbiosis with legumes (5,6). Based on previous research into genetics and comparative genomics, it was hypothesized that no genes are common and specific to all the rhizobia (3,7).…”