Herbivorous fish microbiome adaptations to sulfated dietary polysaccharides

Abstract Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three different species of macro-algivorous Hawaiian kyphosids have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Assembled metagenomes from terrestrial ruminant microbiota containing carbohydrate-utilizing bacterial taxa closely related to those found in kyphosid fish, including Alistipes-related Bacteroidota and Clostridia-related Bacillota, were used as negative controls to identify shared features common to both marine and non-marine saccharolytic intestinal bacteria. This strategy provided the statistical power necessary to distinguish macro-algivorous digestion-specific activities from more generalized aspects of carbohydrate metabolism. Gene co-localization patterns of enriched digestive enzyme families on assembled contigs were used to identify polysaccharide utilization locus associations, and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides, providing foundational resources for future investigations into suppression of coral reef macroalgal overgrowth, fish host physiology, the use of macroalgal feedstocks in terrestrial and aquaculture animal feeds, and the bioconversion of macroalgae biomass into value-added commercial fuel and chemical products.