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Host nutrient supply can mediate host–pathogen and pathogen–pathogen interactions. In terrestrial systems, plant nutrient supply is mediated by soil microbes, suggesting a potential role of soil microbes in plant diseases beyond soil‐borne pathogens and induced plant defenses. Long‐term nitrogen (N) enrichment can shift pathogenic and nonpathogenic soil microbial community composition and function, but it is unclear if these shifts affect plant–pathogen and pathogen–pathogen interactions. In a growth chamber experiment, we tested the effect of long‐term N enrichment on infection by Barley Yellow Dwarf Virus (BYDV‐PAV) and Cereal Yellow Dwarf Virus (CYDV‐RPV), aphid‐vectored RNA viruses, in a grass host. We inoculated sterilized growing medium with soil collected from a long‐term N enrichment experiment (ambient, low, and high N soil treatments) to isolate effects mediated by the soil microbial community. We crossed soil treatments with a N supply treatment (low, high) and virus inoculation treatment (mock‐, singly‐, and co‐inoculated) to evaluate the effects of long‐term N enrichment on plant–pathogen and pathogen–pathogen interactions, as mediated by N availability. We measured the proportion of plants infected (i.e., incidence), plant biomass, and leaf chlorophyll content. BYDV‐PAV incidence (0.96) declined with low N soil (to 0.46), high N supply (to 0.61), and co‐inoculation (to 0.32). Low N soil mediated the effect of N supply on BYDV‐PAV: instead of N supply reducing BYDV‐PAV incidence, the incidence increased. Additionally, ambient and low N soil ameliorated the negative effect of co‐inoculation on BYDV‐PAV incidence. BYDV‐PAV infection only reduced chlorophyll when plants were grown with low N supply and ambient N soil. There were no significant effects of long‐term N soil on CYDV‐RPV incidence. Soil inoculant with different levels of long‐term N enrichment had different effects on host–pathogen and pathogen–pathogen interactions, suggesting that shifts in soil microbial communities with long‐term N enrichment may mediate disease dynamics., Soil microbes alter plant nutrient supply and plant defenses, both of which can modify plant‐pathogen and pathogen‐pathogen interactions. It is unclear if changes in soil microbial communities exposed to long‐term nitrogen (N) enrichment affect their mediation of plant diseases. In a laboratory experiment, soil exposed to long‐term N enrichment neutralized the negative effects of nitrogen and co‐inoculation on infection incidence of a grass virus.

SummaryNutrient supply rates to hosts can mediate host–pathogen interactions. In terrestrial systems, nutrient supply to plants is mediated by soil microbes, suggesting a potential indirect effect of soil microbes on plant–pathogen interactions. Soil microbes also may affect plant pathogens by inducing plant defenses.We tested the role of soil microbes, nitrogen supply to plant hosts, and co-inoculation on infection by aphid-vectored RNA viruses, Barley Yellow Dwarf Virus (BYDV-PAV) and Cereal Yellow Dwarf Virus (CYDV-RPV), in a grass host grown in soil microbes collected from a long-term nitrogen enrichment experiment.BYDV-PAV incidence declined with high nitrogen supply, co-inoculation, or presence of soil microbes exposed to long-term low nitrogen enrichment. However, when combined, the negative effects of these treatments were sub-additive: nitrogen and co-inoculation did not reduce BYDV-PAV incidence in plants grown with the soil microbes. While soil microbes impacted leaf chlorophyll, they did not alter biomass or CYDV-RPV incidence.Soil microbes mediated the effects of nitrogen supply and co-inoculation on infection incidence and the effects of infection on host symptoms. Thus, soil microbial communities can indirectly control disease dynamics, altering the effects of nitrogen enrichment on plant–pathogen and pathogen–pathogen interactions in terrestrial systems.