Abstract

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 asButyrivibrio_sp_X503,Rhizobium daejeonense,Hoylesella buccalis,Ezakiella coagulans,Enterococcus cecorum,Ruminococcus_sp_zg-924,Polystyrenella longa, andMethylacidimicrobium fagopyrumacross 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.

Keywords

Data Availability

All the raw sequences obtained during the sequencing in this study were available at the NCBI database with the accession number PRJNA1250112.

Abbreviations

  • ADF:: Acid detergent fiber
  • AHLs:: Acyl-homoserine lactones
  • AI-2:: Autoinducer-2
  • Ca:: Calcium
  • CON:: Control
  • CP:: Crude Protein
  • DM:: Dry matter
  • DPD:: (S)-4,5-dihydroxy-2,3-pentanedione
  • EE:: Ether extract
  • HPLC-FD:: High performance liquid chromatography equipped with a fluorescence detector
  • HSL:: Homoserine lactone
  • KEGG:: Kyoto Encyclopedia of Genes and Genomes
  • LDA:: Linear discriminant analysis
  • LEfSe:: Linear discriminant analysis effect size
  • LPS:: Lipopolysaccharide
  • MCP:: Microbial protein
  • MIMOSA2:: Model-based integration of metabolite observations and species abundances 2
  • NDF:: Neutral detergent fiber
  • NH3-N:: Ammonia nitrogen
  • OTU:: Operational taxonomic unit
  • P:: Phosphorus
  • PCA:: Principal components analysis
  • PCoA:: Principal coordinate analysis
  • PICRUSt2:: Phylogenetic investigation of communities by reconstruction of unobserved states 2
  • PLS-DA:: Partial least squares discriminant analysis
  • QQ:: Quorum quenching
  • QS:: Quorum sensing
  • RUSITEC:: Rumen simulation technique
  • SRA:: Sequence read archive
  • TMR:: Total mixed ration
  • TVFA:: Total volatile fatty acid
  • UHPLC-MS:: Ultra-high performance liquid chromatography-mass spectrometry
  • VFAs:: Volatile fatty acids
  • VIP:: Variable importance in projection
  • ZEN:: Zearalenone

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Acknowledgements

The authors would like to acknowledge the assistance from Prof. Shaoxun Tang and technicians of the Institute of Subtropical Agriculture, Chinese Academy of Sciences (Changsha, China), as well as the Biotree Biomed. Tech. Co., Ltd. (Shanghai, China).

Funding

The present work was financially supported by the National Natural Science Foundation of China (Grant No. 32302764), Hunan Provincial Natural Science Foundation (Grant No. 2024JJ5179), Key laboratory for the feed and biology technique of Xinjiang Uygur Autonomous Region (Grant No. XJSLSW-2023001), and Hunan Herbivores Industry Technological System (Grant No. HARS-08).

Ethics Declaration

Ethics approval and consent to participate

All procedures involving animals in this experiment were reviewed and approved by the Animal Care Committee (approval number: 20241003), College of Animal Science and Technology, Hunan Agricultural University (Changsha, China).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

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