Water Exchange Rate Shapes Intestinal Microbiota–Metabolite Interactions and Physiological Responses in Babylonia areolata

In aquaculture, reduced water exchange helps constrain exogenous pathogen invasion, lower pumping costs, and improve management efficiency; nevertheless, its effects on the growth of cultured aquatic animals remain poorly characterized. This study compared two daily water-exchange rates (100% and 0%) to evaluate growth and associated intestinal responses in Babylonia areolata (ivory shell). Growth performance and intestinal enzyme activities were measured, while 16S rRNA gene sequencing and untargeted metabolomics were used to characterize microbial composition and metabolite profiles. The low-water-exchange group exhibited significantly lower weight gain rate (WGR, p < 0.0001), specific growth rate (SGR, p < 0.0001), daily increments in shell length (DISL, p = 0.0060), and shell width (DISW, p = 0.0012). Intestinal total superoxide dismutase (T-SOD, p < 0.0001) and lipase (LIP, p = 0.0011) activities were also significantly lower. The relative abundances of Vibrio, Halodesulfovibrio, and Fusibacter were higher, whereas that of Christensenellaceae_R-7_group was lower. Lipid-related metabolic pathways showed the most pronounced intestinal differences. Intestinal levels of prostaglandins (PGs), leukotrienes (LTs), and sphingosine (Sph) were significantly higher under low-water-exchange conditions. The relative abundance of Halodesulfovibrio correlated positively with PGs and LTs but negatively with lysophospholipids (Lpc) and T-SOD activity. The relative abundance of Christensenellaceae_R-7_group correlated positively with LIP activity and was significantly associated with metabolites involved in primary bile acid biosynthesis. Overall, low-water-exchange conditions were associated with coordinated changes in growth, intestinal enzyme activities, microbial composition, and metabolite profiles, although the underlying mechanisms require functional validation. These findings provide new insights into intestinal microbiota–metabolite responses to low-water-exchange conditions and may guide future validation and intervention studies in RAS-based ivory shell culture.