Global distribution of microbial carrageenan foraging pathways reveals widespread latent traits within the genetic dark matter of ruminant intestinal microbiomes

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 applied 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 distal gut over the rumen, and bacterial isolates had capacity to use carrageenans as a sole carbon source. Carrageenan-active polysaccharide utilization loci (CarPULs) were identified and recombinant enzymes were characterized to provide insights into pathway specialization of divergent CarPULs. Selective enrichment and metagenomic mining revealed that carrageenan catabolism is widespread among geographically and taxonomically distinct ruminants, suggesting it is a globally distributed latent trait within the order Ruminantia and carried within microbiome 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.