Distribution of microbial carrageenan foraging pathways reveals a widespread latent trait within the ruminant intestinal microbiome

Abstract Seaweeds represent a promising source of sustainable, alternative feeds for livestock. Despite their increasing popularity in agriculture, the dietary fate of seaweed polysaccharides, such as carrageenan, is unknown. Here, we apply functional microbiome analyses of ruminant gastrointestinal tract microbiomes to discover catabolic enzymes specific for carrageenan digestion from the red seaweed Mazzaella japonica . M. japonica preferentially increased Bacteroides abundance within the feces over the rumen, and bacterial isolates have the capacity to use carrageenans as a sole carbon source. We identify carrageenan-active polysaccharide utilization loci (CarPULs) and characterize recombinant GH16 subfamily 17 carrageenases, informing previously uncharacterized substrate specificities for the subfamily, and providing insights into pathway specialization of divergent CarPULs. Selective enrichment and metagenomic mining reveals that carrageenan catabolism is widespread among geographically and taxonomically distinct ruminants, suggesting it is a latent trait widely distributed in the Order Artiodactyla and carried within their microbiomes as part of the microbial “dark matter”. These pathways are structurally distinct from those found in marine bacteria, highlighting a complex and ancient evolutionary history of CarPULs in ruminant microbiomes.