Lifetime exposure to known and emerging groundwater contaminants significantly alters poultry microbiome and metabolome

Abstract

The exposome encompasses all lifetime environmental exposures affecting health. Its complexity and high data dimensionality make it challenging to link specific exposure combinations to adverse health outcomes. Establishing relevant exposome criteria is key to addressing current knowledge gaps. This study evaluated contaminant levels in Wisconsin groundwater and their effects on host health. We focused on three co-occurring chemicals that were detected at concentrations exceeding groundwater standards, nitrate, atrazine and imidacloprid, and the emerging contaminant, microplastics. In this study, broilers were exposed to a low dose chemical mixture (35,000 ppb nitrate + 1.7 ppb atrazine + 0.58 ppb imidacloprid) and high dose chemical mixture (100,000 ppb nitrate + 3,000 ppb atrazine + 3,000 ppb imidacloprid) or polyethylene microplastics (PE MPs) for 49 days. We observed that both ternary mixtures and PE fiber MPs significantly altered the cecal microbiomes as determined by the enrichment of genera, Fournierella, Ruminococcus and an unclassified genus in the family Coriobacteriaceae. In addition, +PE fiber presence dysregulated metabolic pathways associated with bile acid biosynthesis and lipid metabolism. Similarly, perturbations to cecal microbial activity for both ternary chemical mixtures were confirmed via modulation of six metabolites including methylisopelletierine which had a higher total ion intensity than the control group. Interestingly, there were no detectable pathological effects to either the +PE fiber or ternary mixture treatment groups. Overall, the data presented here demonstrates that low doses of environmental contaminants are sufficient to dysregulate cecal taxonomic composition and microbial activity without inducing detectable pathological effects. ImportanceWe found that exposure to mixtures of environmental toxins caused gut dysbiosis observed by changes to the chicken cecal microbiome and metabolome. This highlights the importance of conducting such studies with environmentally relevant mixtures of contaminants at detected concentrations to understand the actual risks associated with exposures like drinking contaminated groundwater over a long period of time. Our findings demonstrate that gut microbial metabolites, now known to be key regulators and signaling molecules in a wide range of host health issues, are the source of the negative health outcomes; superseding cell death or pathological damage that are caused by acute exposures. These changes have implications for predicting negative long-term chronic health outcomes.