Metabolic specialization in the gut microbiome of aquatic mammalian herbivores

Sirenians, such as manatees, are the only extant mammals fully adapted to aquatic herbivory. Through specialized hindgut fermentation, they play a role in modulating nutrient fluxes and carbon cycling across tropical coastal and riverine ecosystems. However, our understanding of their gut microbiome and its metabolic potential remains elusive. Here we present an ultradeep genomic atlas of the gut microbiome from 47 freshwater and marine manatees spanning distinct developmental stages, comprising 1,215 non-redundant prokaryotic metagenome-assembled genomes and their associated virome. The manatee microbiome encodes a multilayered enzymatic repertoire for plant cell wall deconstruction, including free enzymes, cellulosomes and CAZyme-enriched outer membrane vesicles, alongside diverse pathways for aromatic catabolism. Combining biochemical and structural approaches, we characterize a previously unrecognized enzymatic pathway involving epilactase, which enables a specific Bacillota species to exploit a carbohydrate inaccessible to most microbial life, defining a specialized biochemical strategy for nutrient niche partitioning. Together, these findings uncover the microbial and metabolic basis of aquatic mammalian herbivory. This study elucidates the microbial and metabolic basis of mammalian aquatic herbivory, identifying a metabolic pathway for epilactose utilization that expands the known functional landscape of gut carbohydrate metabolism.