Significance

Plant multitrophic interactions are extremely complex, and the underlying mechanisms are not easy to unravel. Using tomato plants as a model system, we demonstrated that a soil fungus, Trichoderma afroharzianum, widely used as a biocontrol agent of plant pathogens, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the gut microbiota and its symbiotic contribution to larval nutrition. Our results indicate that insect-plant interactions can be correctly interpreted only at the metaorganism level, focusing on the broad network of interacting holobionts which spans across the soil and the above-ground biosphere. Here, we provide a new functional framework for studying these intricate trophic networks and their ecological relevance.

Abstract

Plants generate energy flows through natural food webs, driven by competition for resources among organisms, which are part of a complex network of multitrophic interactions. Here, we demonstrate that the interaction between tomato plants and a phytophagous insect is driven by a hidden interplay between their respective microbiotas. Tomato plants colonized by the soil fungus Trichoderma afroharzianum, a beneficial microorganism widely used in agriculture as a biocontrol agent, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the larval gut microbiota and its nutritional support to the host. Indeed, experiments aimed to restore the functional microbial community in the gut allow a complete rescue. Our results shed light on a novel role played by a soil microorganism in the modulation of plant–insect interaction, setting the stage for a more comprehensive analysis of the impact that biocontrol agents may have on ecological sustainability of agricultural systems.