Genomic analysis of the Lotus tenuis symbiont Aminobacter ciceronei BA135 reveals horizontal acquisition of a Mesorhizobium symbiosis island

Abstract Legume-rhizobia symbioses are critical for biological nitrogen fixation in marginal soils, yet the occurrence of nitrogen-fixing symbioses in lineages outside the classical rhizobial genera suggest that the evolutionary boundaries of this association are broader than traditionally assumed. We report the complete genomic characterization of Aminobacter BA135, a non-canonical nitrogen-fixing symbiont of Lotus tenuis isolated from the alkaline-sodic soils of the Flooding Pampa, Argentina. A symbiosis chromosomal island was identified, integrated at a Phe-tRNA site orthologous to the integration site of Mesorhizobium japonicum R7A, and encoding complete nodulation and nitrogen fixation gene sets, conjugative transfer machinery and cofactors biosynthesis genes, all conserved in symbiotic Mesorhizobium strains. BA135 forms determinate nodules and supports plant growth under nitrogen-free conditions. Both the nodulation genes and the conjugative transfer backbone of BA135 were nearly identical to strains co-isolated from the same soils, placing BA135 within symbiovar loti and providing strong evidence for local horizontal island exchange. The genome further encodes complete pathways for methylamine and glyphosate degradation, heavy metal resistance, and predicted plant growth-promoting traits. Our results further establish that the island of the other known Aminobacter symbiont, A. anthyllidis LMG26462, derives from a different Mesorhizobium lineage, indicating at least two independent transfers between the two genera.