Herbicide‐induced metabolic changes in a plant–aphid system: how soil bacteria drive the fate and impact of a residual dose of Isoproturon?

Agriculture intensification, massively relying on pesticides, led to the widespread contamination of noncrop terrestrial ecosystems. Soil contamination with pesticide residues widely occurs but its cryptic effects on terrestrial biotic interactions remain unclear, especially at the metabolic scale. We studied the effects of an environmental dose of the herbicide isoproturon on an isoproturon-degrading Sphingomonas soil bacteria - Lolium perenne (Poaceae) and Rhopalosiphum padi (Hemiptera: aphididae) system - in the laboratory. This system is typical of contaminated peri-agricultural ecosystems, such as vegetated buffer strips. We found that isoproturon and its main degradation product transferred from the substrate to aphids, accumulating in plant shoots. No macroscopic effects of the herbicide were observed, but primary metabolites varied in both plants and herbivores. Inoculation of isoproturon-degrading bacteria reduced isoproturon levels in the substrate and suppressed most metabolic variations. Moreover, inoculation of the non-degrading bacterial strain impacted plant metabolism, potentially through mutualistic interaction, underlining the close link between soil microbiota and aboveground organisms. This study shows that isoproturon residues can transfer in a typical grassland trophic system, altering the metabolism of each biological level. It emphasizes the need to consider above- and belowground interactions when assessing seminatural ecosystems' responses to chronic contamination.