Locally-adapted Mimulus ecotypes differentially impact rhizosphere bacterial and archaeal communities in an environment-dependent manner

Plant root-microbe interactions influence plant productivity, health, and resistance to stress. Although there is evidence that plant species and even genotypes can alter soil microbial community structure, environmental conditions can potentially outweigh plant genetic effects. Here, we used a reciprocal transplant experiment to understand the contributions of the environment and the host plant to rhizosphere microbiome composition in locally-adapted ecotypes of Mimulus guttatus (syn. Erythranthe guttata (Fisch. ex DC.) G.L. Nesom). Two genotypes of a coastal ecotype and two genotypes of an inland ecotype were planted at coastal and inland sites. After three months, we collected rhizosphere and bulk soil and assessed microbial communities by 16S rRNA gene sequencing. We found that local environment (coastal versus inland site) strongly influenced rhizosphere communities, at least in part due to distinct local microbial species pools. Host identity played a smaller role: at each site, the ecotypes exhibited remarkably similar composition of microbial communities at the class level, indicating that divergent M. guttatus ecotypes recruit phylogenetically similar rhizosphere communities, even in environments to which they are maladapted. Nevertheless, the two ecotypes significantly differed in community composition at the inland site due to an exclusive set of rare taxa associated with each ecotype. Although our results indicate that locally-adapted M. guttatus ecotypes are genetically diverged in factors shaping rhizosphere communities, environmental factors can trump genetic factors in shaping the M. guttatus microbiome. Overall, our findings demonstrate that wild plants strongly impact root-associated microbial communities, but hierarchical drivers interact to shape microbial community assembly outcomes.