Impact of zearalenone on quorum sensing signaling molecules and its association with the suppression of ruminal microbial fermentation in a RUSITEC system

BACKGROUND: Zearalenone (ZEN), a common mycotoxin in ruminant diets, could disturb the rumen ecosystem and impair rumen fermentation. Noticeably, ZEN has been shown to reduce the relative abundances of specific bacterial taxa that potentially possess quorum sensing (QS) functions, which are deemed essential for the microbial interactions and adaptations during rumen fermentation. Nonetheless, whether QS communications participate in the responses of rumen microbial fermentation to ZEN remains unknown. Therefore, the present trial was performed to explore the potential roles of QS during the alterations of rumen microbial fermentation by ZEN through a rumen simulation technique (RUSITEC) system, in a replicated 4 × 4 Latin square design. RESULTS: ZEN significantly (P < 0.05) reduced QS signal autoinducer-2 (AI-2), and tended to (P = 0.051) downregulate QS signal C4-homoserine lactone (HSL). ZEN also significantly (P < 0.05) decreased total volatile fatty acid (TVFA), acetate, propionate, isobutyrate, isovalerate, organic matter disappearance (OMD), neutral detergent fiber disappearance (NDFD), and acid detergent fiber disappearance (ADFD) in different manners. The linear discriminant analysis effect size (LEfSe) analysis indicated significantly (P < 0.05) differential enrichments of a series of bacterial taxa such as Butyrivibrio_sp_X503, Rhizobium daejeonense, Hoylesella buccalis, Ezakiella coagulans, Enterococcus cecorum, Ruminococcus_sp_zg-924, Polystyrenella longa, and Methylacidimicrobium fagopyrum across different treatments. The phylogenetic investigation of communities by reconstruction of unobserved states 2 (PICRUSt2) analysis suggested that QS were predicted to be significantly (P < 0.05) affected by ZEN. The metabolomics analysis detected considerable significantly (P < 0.05) differing metabolites and implied that ZEN challenge significantly (P < 0.05) influenced the indole alkaloid biosynthesis, biosynthesis of alkaloids derived from shikimate pathway, and sesquiterpenoid and triterpenoid biosynthesis. Significant (P < 0.05) interconnections of QS molecules with the differential rumen fermentation traits, differential bacterial taxa, and differential metabolites were exhibited by Spearman analysis. CONCLUSIONS: ZEN negatively affected the QS signals of AI-2 and C4-HSL, which was found to correlate with the fluctuations in specific rumen fermentation characteristics, ruminal bacterial populations, and ruminal metabolisms. These interrelationships implied the potential involvement of QS in the reactions of rumen microbiota to ZEN contamination, and probably contributed to the inhibition of rumen fermentation.