Herbivorous fish microbiome adaptations to sulfated dietary polysaccharides

Abstract Background. Gut microbiota of kyphosid herbivorous fish, known for feeding almost exclusively on red and brown macroalgae rich in sulfated polysaccharides, contain highly compartmentalized, herbivore-specific taxonomic compositions. The current study explores protein functional activities of microbial taxa comprising this system in digestive compartment-specific metagenomes, identifying specific enzyme associations contributing to macroalgal decomposition. Results. Assembled metagenomes from proximal gut samples were enriched in taxa most closely related to environmental marine species, especially Vibrio-related Gammaproteobacteria, which progressively decline in hindgut compartments in favor of host-specific groups often found in terrestrial vertebrate microbiomes, including Alistipes-related Bacteroidota, Clostridia-related Bacillota, uncharacterized Verrucomicrobiota, and Desulfovibrio-related Deltaproteobacteria. Predicted degradative capacity for sulfated macroalgal polysaccharides is highly enriched in fish hindgut samples, concomitant with expansion of Bacteroidota, Bacillota, and Verrucomicrobiota clades. Extracellularly exported arylsulfatase (SulfAtlas) and carbohydrate active enzyme (CAZy) classes associated with red and brown macroalgal digestion are greatly expanded in kyphosid fish gut versus terrestrial ruminant metagenomes. Genomic mapping of these fish gut-enriched gene functions reveals quantitative signatures suggesting polysaccharide utilization loci associations and coordinated networks of extracellularly exported enzymes targeting specific macroalgal polysaccharides. Co-localization frequencies provide insight into potential gene duplication events and suggest preferred substrates for previously uncharacterized arylsulfatase classes. Conclusions. Metagenomic networks of co-localized polysaccharide hydrolysis and sulfatase gene functions have been used to demonstrate distinct patterns of fish gut compartment-specific microbial enzymes targeting complex sulfated polysaccharides. These patterns reveal previously undescribed potential for cooperative exported enzyme activities and highlight prospective contributions of multiple bacterial taxa to overall digestive capabilities.