Herbicide-induced metabolic changes in a plant-aphid system: How soil bacteria drive the fate and impact of an environmental dose of Isoproturon

The intensification of agriculture, based on massive use of pesticides, led to the widespread contamination of terrestrial ecosystems. Although soil contaminations with pesticide residues have been demonstrated, their impacts on terrestrial biotic interactions remain unclear. To address this matter, we studied the effects of an environmental dose of a photosynthesis inhibitor herbicide (isoproturon) on an isoproturon-degrading soil bacteria-poacea-aphid system in the lab, mimicking below and aboveground interactions within buffer strips. We found that isoproturon and its main degradation product flow through this system, accumulating in plant shoots. No macroscopic effect of the herbicide was observed but metabolic shifts occurred in both plants (especially when exposed for a short time) and phytophages. Inoculation of isoproturon-degrading bacteria in the substrate suppressed most of these effects but some metabolic reshuffles in the longer run suggest secondary effects of Isoproturon degradation products. Moreover, inoculation of the non-degrading bacterial strain also impacted plant metabolism, underlying the close link between soil microbiota and aboveground organisms. This study shows that pesticide residues can transfer in terrestrial trophic networks, altering the physiology of each biological level, and highlights the importance of considering plant-bacteria interactions when assessing the response of semi-natural ecosystems to chronic contamination.