Detoxification of coumarins by rumen anaerobic fungi: insights into microbial degradation pathways and agricultural applications

Abstract

Coumarins are toxic phytochemicals found in a variety of plants and are known to limit microbial degradation and interfere with nutrient cycling. While the degradation of coumarins by fungi has been studied in an environmental context, little is known about their degradation in the gastrointestinal system of herbivores after ingestion. In this study, we investigated in vitro fermentation by microbial enrichment, transcriptome sequencing, and high-resolution mass spectrometry to evaluate the ability of rumen anaerobic fungi to degrade coumarins. The results showed that despite the low abundance of anaerobic fungi in the rumen microbiota, they were able to effectively degrade coumarins. Specifically, Pecoramyces ruminantium F1 could tolerate coumarin concentrations up to 3 mmol/L and degrade it efficiently via metabolic pathways involving alpha/beta hydrolases and NAD(P)H oxidoreductases within the late growth phase. The fungus metabolized coumarin to less toxic compounds, including o-coumaric acid and melilotic acid, highlighting the detoxification potential of anaerobic fungi. This study is the first to demonstrate the ability of rumen anaerobic fungi to degrade coumarin, providing new insights into the use of anaerobic fungi in sustainable agricultural practices and environmental detoxification strategies.