Trophic interactions as determinants of the arbuscular mycorrhizal fungal community with cascading plant-promoting consequences

The soil mycobiome is composed of a complex and diverse fungal community, which includes functionally diverse species ranging from plant pathogens to mutualists. Among the latter are arbuscular mycorrhizal fungi (AMF) that provide phosphorous (P) to plants. While plant hosts and abiotic parameters are known to structure AMF communities, it remains largely unknown how higher trophic level organisms, including protists and nematodes, affect AMF abundance and community composition. Here, we explored the connections between AMF, fungivorous protists and nematodes that could partly reflect trophic interactions, and linked those to rhizosphere P dynamics and plant performance in a long-term manure application setting. Our results revealed that manure addition increased AMF biomass and the density of fungivorous nematodes, and tailored the community structures of AMF, fungivorous protists, and nematodes. We detected a higher abundance of AMF digested by the dominant fungivorous nematodes Aphelenchoides and Aphelenchus in high manure treatments compared to no manure and low manure treatments. Structural equation modeling combined with network analysis suggested that predation by fungivorous protists and nematodes stimulated AMF biomass and modified the AMF community composition. The mycorrhizal-fungivore interactions catalyzed AMF colonization and expression levels of the P transporter gene ZMPht1;6 in maize roots, which resulted in enhanced plant productivity. Our study highlights the importance of predation as a key element in shaping the composition and enhancing the biomass of AMF, leading to increased plant performance. As such, we clarify novel biological mechanism of the complex interactions between AMF, fungivorous protists, and nematodes in driving P absorption and plant performance. Video Abstract.