Hindguts of Kyphosus sydneyanus harbor phylogenetically and genomically distinct Alistipes capable of degrading algal polysaccharides and diazotrophy.

The genus Alistipes (Bacteroidota) is most often associated with human clinical samples and livestock. However, Alistipes are also prevalent in the hindgut of the marine herbivorous fish Kyphosus sydneyanus (Silver Drummer), and analysis of their carbohydrate-active enzyme (CAZyme) encoding gene repertoires suggests Alistipes degrade macroalgal biomass to support fish nutrition. To further explore host-associated traits unique to K. sydneyanus-derived Alistipes, we compared 445 high-quality genomes of Alistipes available in public databases (e.g., human and ruminant associated) with 99 metagenome-assembled genomes (MAGs) from the K. sydneyanus gut. Analyses showed that Alistipes from K. sydneyanus are phylogenetically distinct from other hosts and comprise 26 species based on genomic average nucleotide identity (ANI) analyses. Ruminant- and fish-derived Alistipes had significantly smaller genomes than human-derived strains, and lower GC contents, possibly reflecting a symbiotic relationship with their hosts. The fish-derived Alistipes were further delineated by their genetic capacity to fix nitrogen, biosynthesize cobalamin (vitamin B12), and utilize marine polysaccharides (e.g., alginate and carrageenan). The distribution of CAZymes encoded by Alistipes from K. sydneyanus was not phylogenetically conserved. Distinct CAZyme gene compositions were observed between closely related species. Conversely, CAZyme gene clusters (operons) targeting the same substrates were found across diverse species. Nonetheless, transcriptional data suggest that closely related Alistipes target specific groups of substrates within the fish hindgut. Results highlight host-specific adaptations among Alistipes in the fish hindgut that likely contribute to K. sydneyanus digesting their seaweed diet, and diverse and redundant carbohydrate-degrading capabilities across these Alistipes species.IMPORTANCEDespite numerous reports of the Alistipes genus in humans and ruminants, its diversity and function remain understudied, and there is no clear consensus on whether it positively or negatively impacts host health. Given the symbiotic role of gut communities in the Kyphosus sydneyanus hindgut, where Alistipes are prevalent, and the diversity of carbohydrate-active enzymes (CAZymes) encoded that likely contribute to the breakdown of important substrates in the host diet, it is likely that this genus provides essential services to the fish host. Therefore, considering its metabolism in various contexts and hosts is crucial for understanding the ecology of the genus. Our study highlights the distinct genetic traits of Alistipes based on host association, and the potential of fish-associated Alistipes to transform macroalgae biomass into nutraceuticals (alginate oligosaccharides, β-glucans, sulfated galactans, and sulfated fucans).