90 Microbiome-Derived Bioactive Molecules to Reduce Enteric Methane Emissions

Abstract

Abstract Microorganisms are pivotal for the development, health, and productivity of livestock. In adult ruminants, the microbiota colonizing the rumen is essential for efficient depolymerization of indigestible carbohydrates from plant biomass and their conversion into microbial protein and fermentation end-products that are used by the host for growth. In the last decades, next-generation sequencing and omics technologies provided unparalleled insights into the composition, structure, and function of the gastrointestinal (GI) tract microbiome of ruminants and helped improve our understanding of relationships between the rumen microbiota with cattle performance (efficiency) traits, as well as health and disease and greenhouse gas emissions. The ecological interactions between microbes within the rumen ecosystem are complex and involve, among others, cross-feeding, predation, parasitism, antagonism, and competition for novel (empty) niches and available resources. These diverse associations of ecological traits across distinct microbial populations that coexist in the same ecosystem represent a goldmine for the discovery of novel bioactive molecules, including compounds with potential to modulate rumen fermentation and inhibit methane emissions from enteric fermentation. These effects often result from metabolic shifts in the rumen fermentation that lead to increased production of propionate, but can also be caused by direct inhibition of methanogenic archaea or through a reduction in the production of substrates for methanogenesis. Culture-independent approaches based on genome mining and functional metagenomics demonstrated that the rumen is an underexplored resource for bioactive molecules, such as antimicrobial peptides, non-ribosomal peptides, polyketides, and secondary metabolites involved in intercellular (microbe-microbe) communication. Rumen metatranscriptomic data indicate that the expression of genes potentially encoding some of these molecules is increased during the colonization of plant biomass that enters the rumen. Nonetheless, some representatives of key taxa from the core rumen microbiome cannot be found in culture collections, which is critical to validate phenotypic predictions from genomic and metagenomic data and obtain ecological insights about the interplay between individual microbial populations in the microbiome. Culturomic technologies and high-throughput identification and characterization of microbial species that colonize the rumen could contribute to building a unique biotechnological resource that can be explored for sourcing novel bioactive compounds with anti-methanogenic activity and developing fermentation products that could reduce rumen methanogenesis while improving the health status and productivity of cattle.