Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont

Abstract

Given the need to predict the outcomes of (co)evolution in host-associated microbiomes, whether microbial and host fitnesses tend to trade-off, generating conflict, remains a pressing question. Examining the relationships between host and microbe fitness proxies at both the phenotypic and genomic levels can illuminate the mechanisms underlying interspecies cooperation and conflict. We examined naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti , paired with each of two host Medicago truncatula genotypes in single- or multi-strain experiments to determine how multiple proxies of microbial and host fitness were related to one another and test key predictions about mutualism evolution at the genomic scale, while also addressing the challenge of measuring microbial fitness. We found little evidence for interspecies fitness conflict; loci tended to have concordant effects on both microbe and host fitnesses, even in environments with multiple co-occurring strains. Our results emphasize the importance of quantifying microbial relative fitness for understanding microbiome evolution and thus harnessing microbiomes to improve host fitness. Additionally, we find that mutualistic coevolution between hosts and microbes acts to maintain, rather than erode, genetic diversity, potentially explaining why variation in mutualism traits persists in nature.

Host-Associated Rhizobial Fitness: Dependence on Nitrogen, Density, Community Complexity, and Legume Genotype

“…Consistent with previous work on the same strains ( 64 ), with an overlapping set of strains ( 28 , 63 ), and with an independent collection of rhizobial strains ( 29 ), the strain composition of the nodule communities was strongly affected by host genotype ( Fig. 2 and Fig.…”

“…Results from single-strain experiments may not be directly translatable to multistrain environments because between-strain competition can strongly affect nodulation success ( 27 ). Indeed, strain fitness proxies in single-strain environments are not strongly correlated with strain fitness in multistrain communities ( 28 , 29 ).…”

Mosaic of local adaptation between white clover and rhizobia along an urbanization gradient

“…Alternatively, the absence of a correlation can arise despite ongoing coevolution because traits could be mismatched (Gomulkiewicz et al., 2007; Nuismer et al., 2010; Thompson, 2005). Further investigation of potential coevolution between white clover and rhizobia in urban environments requires characterizing selection acting on both white clover and rhizobia, and ideally genomic signatures of selection on genes associated with the mutualism (Batstone, Burghardt, et al., 2022; Batstone, Lindgren, et al., 2022; Epstein et al., 2023; Gomulkiewicz et al., 2007; Hoeksema, 2010).…”

Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes

“…Uncovering the complex genetics of how two (or more) genomes interact with each other to generate trait variation is an important step to better understanding how these traits (co)evolve ( 6 ) and how to better manipulate traits in the future to address societal challenges ( 37 , 118 ). For example, identifying the loci underlying mutualistic traits allows us to address longstanding debates within mutualism theory ( 119 ), including how readily conflict evolves ( 120 ), and how genetic variation is maintained despite host selection for the “best” symbiont ( 95 ).…”