Soil microbiomes drive aboveground plant-pathogen-insect interactions

Plants interact with a large diversity of microbes and insects, both below and above ground. While studies have shown that belowground microbes affect the performance of plants and aboveground organisms, we lack insights into how belowground microbial communities may shape interactions between aboveground pathogens and insects. We investigated how soil microbiomes and aboveground organisms affect plant growth and development, and whether differences in soil microbiomes influence interactions between aboveground organisms. We conducted a growth-chamber experiment with oak seedlings Quercus robur growing in three soils with similar abiotic soil properties but with distinct natural soil microbiomes. Seedlings were subjected to single or dual attack by powdery mildew Erysiphe alphitoides and aphids Tuberculatus annulatus, either in the presence or absence of prior attack by a free-feeding caterpillar Phalera bucephala. Soil microbiomes were associated with differences in seedling height, and seedlings with multiple aboveground organisms had more but smaller leaves than healthy seedlings. The soil microbiome affected the severity of powdery mildew infection, and mediated the impact of co-occurring aboveground organisms on aphid population size. Our study highlights that plant performance is affected by natural soil microbiomes as well as aboveground organisms, and that natural soil microbiomes can affect interactions between pathogens and insects. These findings are important to understand species interactions in natural systems, as well as for practical applications, such as manipulation of soil microbiomes to manage agricultural pests and diseases.