Variation in aquaculture systems shapes the intestinal microbiota of Acrossocheilus fasciatus , a freshwater cyprinid, via environmental drivers

Abstract

Aquaculture system design alters aquatic habitats and influences host-associated microbiota, but its effects on gut taxonomic and functional organization remain poorly understood. Here, we compared Acrossocheilus fasciatus (a freshwater cyprinid) cultured under four representative systems (high-level ponds, earthen ponds, land-based circular tanks, and rice–fish integrated farming) using water physicochemical measurements, 16S and 18S ribosomal RNA gene profiling of aquatic microbial communities, and intestinal shotgun metagenomics. Aquaculture systems exhibited distinct environmental profiles. Earthen ponds were warm, nutrient rich, and oxygen poor, whereas rice–fish systems were characterized by higher dissolved oxygen, alkaline pH, and lower nitrogen concentrations. Aquatic bacterial and microeukaryotic communities differed significantly among systems and reflected these environmental gradients. In the gut, aquaculture mode significantly affected community composition without altering Shannon diversity, indicating that system effects were primarily reflected in taxonomic turnover. Gut functional profiles showed even stronger system-level differentiation, with replication-, repair-, and biosynthesis-related pathways enriched in high-level ponds and rice–fish systems, while hypoxia- and stress-associated pathways were enriched in earthen ponds. Structural equation modeling further indicated associations among environmental gradients, aquatic microbial community structure, gut taxonomic profiles, gut functional profiles, and growth-related variation. Together, our findings indicate that aquaculture systems are associated with coordinated variation in the rearing environment, aquatic microbial reservoirs, and gut microbiome taxonomic and functional organization in A. fasciatus. These results provide a microbiome-informed basis for incorporating microbial indicators alongside conventional water quality metrics when evaluating and refining aquaculture system performance.