Abstract:
Symbiotic gut microbiota carry out a number of functions in host animals. In silver drummer, Kyphosus sydneyanus, a temperate, marine, herbivorous fish, the microbiota ferment refractory carbohydrates from dietary brown algae to short chain fatty acids, aswell as fixing nitrogen. The aims of this study were twofold: to identify the community composition of the hindgut microbiota in silver drummer, and to analyse the functional genomic profiles of the microbiota by identifying selected CAZymes potentially involved in algal breakdown. Silver drummer were collected from the Hauraki Gulf in north-eastern New Zealand and samples were taken from different intestinal regions to represent both axial (sections III, IV, and V) and radial (mucosa and lumen) variation in gut location. Community composition of the hindgut microbiota was determined via PCR amplification and sequencing of the variable regions 3 and 4 of the 16SrRNA gene. Firmicutes, Bacteroidetes, and Proteobacteria dominated at phyla level, while considerable inter-individual variation was observed at lower taxonomic levels. Community composition in axial and radial samples showed distinct biogeographic trends, likely as a result of the differing selection pressures (including pH, oxygen-gradient, and mucous availability) exerted between these locations. The axial sections carry out different fermentation reactions as both the fish and the gut microbiota carry out the fermentation of different substrates along the gut. Additionally, species diversity and density were shown to increase along the gut. A subset of the original samples was sequenced using shotgun metagenomic sequencing to investigate the functional potential of the hindgut microbiota. The metagenomic data across all four KEGG levels showed that there was great similarity between individual fish and gut sections in the relative abundances of important CAZyme and nitrogenase genes. This finding contrasted with the high inter-individual variation in taxonomic composition. These results suggest that the host selects for functional ability in symbionts rather than taxonomic identity. In this herbivorous fish species, the concept of a ‘core microbiome’ should be focussed on rather than a ‘core microbiota’. Examination of functionally annotated genes revealed the metabolic pathways used by the hindgut microbiota for the degradation of alginate and mannitol, the two most abundant carbohydrates in the diet, as well as the pathway used in the fixation of nitrogen. This work provides the first evidence of the genomic potential of the hindgut microbiota in silver drummer to convert highly refractory algal carbohydrates into metabolically useful short chain fatty acids.