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Plant–microbe symbioses such as the legume–rhizobium mutualism are vital in the web of ecological relationships within both natural and managed ecosystems, influencing primary productivity, crop yield, and ecosystem services. The outcome of these interactions for plant hosts varies quantitatively and can range from highly beneficial to even detrimental depending on natural genetic variation in microbial symbionts. Here, we take a systems genetics approach, harnessing the genetic diversity present in wild rhizobial populations to predict genes and molecular pathways crucial in determining partner quality, i.e., the benefits of symbiosis for legume hosts. We combine traits, dual-RNAseq of both partners from active nodules, pangenomics/pantranscriptomics, and Weighted Gene Co-expression Network Analysis (WGCNA) for a panel of 20Sinorhizobium melilotistrains that vary in symbiotic partner quality. We find that genetic variation in the nodule transcriptome predicts host plant biomass, and WGCNA reveals networks of genes in plants and rhizobia that are coexpressed and associated with high-quality symbiosis. Presence–absence variation of gene clusters on the symbiosis plasmid (pSymA), validated in planta, is associated with high or low-quality symbiosis and is found within important coexpression modules. Functionally our results point to management of oxidative stress, amino acid and carbohydrate transport, and NCR peptide signaling mechanisms in driving symbiotic outcomes. Our integrative approach highlights the complex genetic architecture of microbial partner quality and raises hypotheses about the genetic mechanisms and evolutionary dynamics of symbiosis. 

The ecologically and economically vital symbiosis between nitrogen-fixing rhizobia and leguminous plants is often thought of as a bi-partite interaction, yet studies increasingly show the prevalence of non-rhizobial endophytes (NREs) that occupy nodules alongside rhizobia. Yet, what impact these NREs have on plant or rhizobium fitness remains unclear. Here, we investigated four NRE strains found to naturally co-occupy nodules of the legume Medicago truncatula alongside Sinorhizobium meliloti in native soils. Our objectives were to (1) examine the direct and indirect effects of NREs on M. truncatula and S. meliloti fitness, and (2) determine whether NREs can re-colonize root and nodule tissues upon reinoculation. We identified one NRE strain (522) as a novel Paenibacillus species, another strain (717A) as a novel Bacillus species, and the other two (702A and 733B) as novel Pseudomonas species. Additionally, we found that two NREs (Bacillus 717A and Pseudomonas 733B) reduced the fitness benefits obtained from symbiosis for both partners, while the other two (522, 702A) had little effect. Lastly, we found that NREs were able to co-infect host tissues alongside S. meliloti. This study demonstrates that variation of NREs present in natural populations must be considered to better understand legume–rhizobium dynamics in soil communities. 

Many bacterial traits important to host-microbe symbiosis are determined by genes carried on extrachromosomal replicons such as plasmids, chromids, and integrative and conjugative elements. Multiple such replicons often coexist within a single cell and, due to horizontal mobility, have patterns of variation and evolutionary histories that are distinct from each other and from the bacterial chromosome. In nitrogen-fixing Rhizobium, genes carried on multiple plasmids make up almost 50% of the genome, are necessary for the formation of symbiosis, and underlie bacterial traits including host plant benefits. Thus the genomics and transmission of plasmids in Rhizobium underlie the ecology and evolution of this important model symbiont. Here we leverage a natural population of clover-associated Rhizobium in which partner quality has declined in response to long-term nitrogen fertilization. We use 62 novel, reference-quality genomes to characterize 257 replicons in the plasmidome and study their genomics and transmission patterns. We find that, of the four most frequent plasmid types, two (types II & III) have more stable size, larger core genomes, and track the chromosomal phylogeny (display more vertical transmission), while others (types I & IV – the symbiosis plasmid, or pSym) vary substantially in size, shared gene content, and have phylogenies consistent with frequent horizontal transmission. We also find differentiation in pSym subtypes driven by long-term nitrogen fertilization. Our results highlight the variation in plasmid transmission dynamics within a single symbiont and implicate plasmid horizontal transmission in the evolution of partner quality.