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

'One Health' emphasizes the ecological relationships between environmental, plant, animal and human health such as for instance in a food chain. Microbiomes play important roles in these relationships, as they modify the health and performance of the different components, and play a crucial role at the interface between food chain components (plant root microbiome, animal gut microbiome). Yet, whether the microbiomes of diverse components along the food chain could be influenced by common environmental and anthropogenic chemicals such as potentially toxic trace elements, bioactive plant metabolites, agrochemicals and whether there is any commonality in microbiomes' responses is not known. Here, we systematically challenged a model food chain, including water and sediment, soil, plants and animals with defined ranges of chemical stresses consisting of heavy metal (arsenic, As) an abundant bioactive plant metabolite (benzoxazinoid, Bx), and a herbicide (terbuthylazine, Tb). In soil, microbial diversity and richness decreased in all treated groups in comparison to control, whereas they increased in the mouse gut microbiome, and did not change in the other components. Microbial community composition markedly reduced following treatments with As, Bx or Tb, in all components of the food chain except for animal, where the microbial community composition of treated samples became more heterogeneous as compared to that in the control groups. Additionally, we observed dispersion in microbial communities in the low diversity microbiomes of plants and animals after treatment. Microbiome network properties significantly changed following experimental treatment with either decreased (water, sediment, plant, animal) or increased (soil) numbers of hub taxa in treated groups as compared to controls. This suggests major re-distribution of the roles and associations specific taxa may have, with the community stability of plant and animal microbiomes being the most affected by common chemical stresses. Overall, we observed diverse, component-specific responses to chemical stressors in microbiomes from components along an idealized food chain, which could have significant implications for One Health.