Soil microbiota and herbivory influence the structure of plant-associated microbial communities in tomato plants

Plant-associated microbial communities are key to shaping many aspects of plant biology, including their fitness, ecology, and evolution. While several studies focused on testing the effect of different factors (e.g., plant genotype, soil, biotic and abiotic stressors) on the assembly of plant microbiomes, we still know little about the possible mechanisms that drive these effects. In this study we tested whether soil microbial community and herbivory influence the microbial community of tomato plants, and whether their influence in different plant compartments is driven by active (via plant) or passive (via microbial spillover) mechanisms. We grew our plants in soils hosting three different microbial communities, we covered (or not) the soil surface to prevent (or allow) passive microbial spillover between compartments, and we exposed them (or not) to herbivory by Manduca sexta. Results suggest that, while microbiomes mainly differentiated by compartment (rhizosphere, roots, leaves, herbivore), soil microbial community followed by herbivory influenced the structure of plant-associated microbial communities. The soil-driven effect was detected regardless of soil coverage, suggesting that this effect might be mediated by the plant. On the other hand, we found that the herbivore-driven effect on the rhizosphere microbiota was detected only when the soil cover was absent, suggesting that this effect might be driven by passive microbial spillover (e.g., via frass). These results promote understanding of the drivers of plant microbiome assembly, their relative strength, and the mechanisms behind them.