Are Plant–Soil Feedbacks Caused by Many Weak Microbial Interactions?

SIMPLE SUMMARY: Soil organism communities are typically different under different plant species. Often, soil bacteria and fungi that feed on a plant species will accumulate and decrease the growth of the dominant species. This effect has long been recognized in agricultural systems and more recently in more diverse and natural systems. Yet, little is known about the soil organisms that cause these effects. Here, we described the soil organisms in common garden experiments in North America and Europe and found that soil organisms vary widely among sites, among years, and between bulk soils and the soils around roots. Plant effects on the soil microbial community were only detected in root-associated soils. In these soils, plants changed dozens to hundreds of soil organisms. In short, plants affected a small but diverse portion of the soil microbial community, and these changes were found to affect subsequent plant growth. The results suggest that microbial-based management of plant growth will likely have to manipulate a small but diverse subset of the soil microbial community and not individual plant pathogens or symbionts. ABSTRACT: We used high-throughput sequencing and multivariate analyses to describe soil microbial community composition in two four-year field plant–soil feedback (PSF) experiments in Minnesota, USA and Jena, Germany. In descending order of variation explained, microbial community composition differed between the two study sites, among years, between bulk and rhizosphere soils, and among rhizosphere soils cultivated by different plant species. To try to identify soil organisms or communities that may cause PSF, we correlated plant growth responses with the microbial community composition associated with different plants. We found that plant biomass was correlated with values on two multivariate axes. These multivariate axes weighted dozens of soil organisms, suggesting that PSF was not caused by individual pathogens or symbionts but instead was caused by ‘many weak’ plant–microbe interactions. Taken together, the results suggest that PSFs result from complex interactions that occur within the context of a much larger soil microbial community whose composition is determined by factors associated with ‘site’ or year, such as soil pH, soil type, and weather. The results suggest that PSFs may be highly variable and difficult to reproduce because they result from complex interactions that occur in the context of a larger soil microbial community.