Component specific responses of the microbiomes to common chemical stressors in the human food chain

Abstract Along a food chain, microbiomes occur in each component and often contribute to the functioning or the health of their host or environment. ‘One Health’ emphasizes the connectivity of each component’s health. Chemical stress typically causes dysbiotic microbiomes, but it remains unclear whether chemical stressors consistently affect the microbiomes along food chain components. Here, we systematically challenged a model food chain, including water, sediments, soil, plants, and animals, with three chemical stresses consisting of arsenic (a toxic trace element), benzoxazinoids (an abundant bioactive plant metabolites), and terbuthylazine (an herbicide typically found along a human food chain). The analysis of 1,064 microbiome profiles for commonalities and differences in their stress responses indicated that chemical stressors decreased microbiome diversity in soil and animal, but not in the other microbiomes. In response to stress, all food chain communities strongly shifted in their composition, generally becoming compositionally more similar to each other. In addition, we observed stochastic effects in host-associated communities (plant, animal). Dysbiotic microbiomes were characterized by different sets of bacteria, which responded specifically to the three chemical stressors. Microbial co-occurrence patterns significantly shifted with either decreased (water, sediment, plant, animal) or increased (soil) network sparsity and numbers of keystone taxa following stress treatments. This suggested major re-distribution of the roles that specific taxa may have, with the community stability of plant and animal microbiomes being the most affected by chemical stresses. Overall, we observed stress- and component-specific responses to chemical stressors in microbiomes along the model food chain, which could have implications on food chain health.