Abstract
BACKGROUND: Aflatoxin B(1) (AFB(1)), a highly carcinogenic and hepatotoxic mycotoxin frequently contaminating animal feed, presents serious health risks to both humans and livestock. Although AFB(1)'s hepatotoxicity and other organ damage are extensively characterized, how this mycotoxin influences ruminal microbiota dynamics and functional activities in ruminants remains underexplored. Although some studies suggest that AFB(1) reduces nutrient digestibility and performance in ruminants, the underlying mechanisms are unclear. To aid in developing effective mitigation strategies for aflatoxicosis in ruminants, this study randomly divided Saanen goats into three groups. The CON group received the standard ration without additives, whereas LD and HD groups were provided identical basal diets fortified with 50 or 500 μg/kg AFB(1). Throughout the study, alterations in ruminal fermentation parameters, microbiome, and metabolome profiles were analyzed. RESULTS: With increasing AFB(1) levels, ruminal pH, the concentration of total volatile fatty acids (VFA), acetate, and propionate decreased quadratically, while butyrate decreased linearly. Metagenomic profiling indicated suppressed populations of Pelagibacter and Flavobacterium following AFB(1) exposure, contrasting with promoted growth of Cryptobacteroides. Additionally, seven carbohydrate-active enzymes (CAZymes), specifically GT92, GT20, CE7, GT32, GT35, GT57, and GT50, were found to be more prevalent in the rumen of the CON group. Statistically higher viral loads characterized the HD group when benchmarked against CON group. Metabolomics analysis identified 1197 differential metabolites among the CON, LD, and HD groups, including cytochalasin Ppho and chrysophanol, both known for their teratogenic properties and their ability to induce cell death. CONCLUSIONS: This study indicates that dietary AFB(1) exposure can alter the ruminal microbial and metabolomic profiles, induce prophage activation, and impact carbohydrate degradation and microbial protein turnover. These alterations may contribute to reductions in ruminal pH and volatile fatty acid concentrations, thereby impairing feed digestibility and animal performance. The findings provide valuable insights into AFB(1)'s effects on rumen health, and further investigations of these metabolic pathways may help develop precision interventions to mitigate AFB(1)-induced rumen dysfunction and productivity losses. Video Abstract.