Abstract
Although complex interactions between hosts and microbial associates are increasingly well documented, we still know little about how and why hosts shape microbial communities in nature. In addition, host genetic effects on microbial communities vary widely depending on the environment, obscuring conclusions about which microbes are impacted and which plant functions are important. We characterized the leaf microbiota of 200 A. thaliana genotypes in eight field experiments and detected consistent host effects on specific, broadly distributed microbial OTU’s. Host genetics disproportionately influenced hubs within the microbial communities, with their impact then percolating through the community, as evidenced by a decline in the heritability of particular OTUs with their distance to the nearest hub. By simultaneously measuring host performance, we found that host genetics associated with microbial hubs explained over 10% of the variation in lifetime seed production among host genotypes across sites and years. We successfully cultured one of these microbial hubs and demonstrated its growth-promoting effects on plants grown in sterile conditions. Finally, genome-wide association mapping identified many putatively causal genes with small effects on the relative abundance of microbial hubs across sites and years, and these genes were enriched for those involved in the synthesis of specialized metabolites, auxins and the immune system. Using untargeted metabolomics, we corroborate the consistent association of variation in specialized metabolites and microbial hubs across field sites. Together, our results reveal that host natural variation impacts the microbial communities in consistent ways across environments and that these effects contribute to fitness variation among host genotypes.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
In this new version we added two major results supporting our previous conclusions: - Against all odds, we were able to isolate, culture and sequence one of the microbial hubs we identified and found it had a growth promoting effect in sterile conditions consistent with our field results, lending credence to our analyses. Reliability of our analyses is further supported by the enrichment for biological processes and pathways involved in host-microbiome interactions that we find in our GWAS analyses. - In this study we found that heritable ecological hubs are unusually widespread, playing a similar role across sites and years and suggesting that host control can extend across environmental variability. We have now added an analysis of plant specialized metabolites. This new results suggests that they are not only heritable and impact many hubs, but their expression is robust to variation across our field trials, providing one potential mechanism for broad host control.