Reciprocal influence of soil, phyllosphere, and aphid microbiomes

Background: The effect of soil on the plant microbiome is well-studied. However, less is known about the impact of the soil microbiome in multitrophic systems. Here we examined the effect of soil on plant and aphid microbiomes, and the reciprocal effect of aphid herbivory on the plant and soil microbiomes. We designed microcosms, which separate below and aboveground compartments, to grow oak seedlings with and without aphid herbivory in soils with three different microbiomes. We used amplicon sequencing and qPCR to characterize the bacterial and fungal communities in soils, phyllospheres, and aphids. Results: Soil microbiomes significantly affected the microbial communities of phyllospheres and, to a lesser extent, aphid microbiomes, indicating plant-mediated assembly processes from soil to aphids. While aphid herbivory significantly decreased microbial diversity in phyllospheres independent of soil microbiomes, the effect of aphid herbivory on the community composition in soil varied among the three soils. Conclusions: This study provides experimental evidence for the reciprocal influence of soil, plant, and aphid microbiomes, with the potential for the development of new microbiome-based pest management strategies.