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Simple Summary: "Rhizobia" are alpha- and beta-proteobacteria with the ability to associate in symbiosis with legumes, establishing complex root structures (nodules) where the process of biological N2-fixation takes place. The knowledge of these bacteria which efficiently associate with particular legumes is a key aspect in understanding the origin, diversification, practical use, and improvement of the symbiotic systems. In this work, we present the phenotypic and genomic characteristics of a collection of bacterial isolates of the genera Sinorhizobium, present in soils of northwest Argentina and able to associate with plants of the Desmanthus virgatus complex. Results showed an important genetic diversity among the local isolates (including different species), heterogeneous profiles of tolerance to abiotic stresses, and an outstanding capacity to support plant growth in the absence of fixed nitrogen. Upon the genomic and phylogenetic analyses of selected isolates, evidence of the horizontal gene transfer of nodulation (nod) genes was obtained, accounting for current genomic constitution of the local symbionts of Desmanthus. Desmanthus spp. are legumes with the ability to associate with diverse α-proteobacteria—a microsymbiont—in order to establish nitrogen-fixing root nodules. A previous investigation from our laboratory revealed that the main bacteria associated with Desmanthus paspalaceus in symbiosis in central Argentina (Province of Santa Fe) were quite diverse and belonged to the genera Rhizobium and Mesorhizobium. To achieve a more extensive view of the local microsymbionts associated with Desmanthus spp., we sampled three different sites in Jujuy and Salta, in northwest Argentina. Matrix-assisted Laser-Desorption-Ionization Time-of-Flight mass spectrometry (MALDI-TOF) typing, 16S-rDNA analysis, and genome sequencing demonstrated that the dominant root-nodule microsymbionts belonged to the genus Sinorhizobium, with some sequenced genomes related to Sinorhizobium mexicanum, Sinorhizobium chiapanecum, and Sinorhizobium psoraleae. An analysis of nodA and nodC markers indicated that, in some of the isolates, horizontal gene transfer appeared to be responsible for the lack of congruence between the phylogenies of the chromosome and of the symbiotic region. These results revealed diverse evolutionary strategies for reaching the current Desmanthus-microsymbiont diversity. What is remarkable beside their observed genetic diversity is that the tolerance profiles of these isolates to abiotic stresses (temperature, salt concentration, pH) were quite coincident with the separation of the sinorhizobia according to place of origin, suggesting possible ecoedaphic adaptations. This observation, together with the higher aerial dry-weight matter that some isolates generated in Desmanthus virgatus cv. Marc when compared to the biomass generated by the commercial strain Sinorhizobium terangae CB3126, distinguish the collected sinorhizobia as constituting valuable germplasm for evaluation in local fields to select for more efficient symbiotic pairs. [ABSTRACT FROM AUTHOR]