Seasonal dietary shifts drive gut microbiome and metabolome adaptation in wild Northern Pike (Esox lucius)

The gut microbiome of fish faces challenges in maintaining stability during seasonal dietary shifts, which directly impacts host nutrition and fitness. In this study, environmental DNA metabarcoding, metagenomics, and metabolomics were employed to characterize seasonal differences in diet, gut microbiome composition, metabolites, and digestive enzyme activity of Esox lucius between spring and autumn. E. lucius exhibited broadly and opportunistically in spring but shifted to a markedly narrower in autumn. Microbiome composition exhibited marked seasonality, with spring dominated by Mycoplasma and Yersinia , whereas autumn were characterized by Aeromonas , Acinetobacter , environmental bacteria, and were accompanied by increased trypsin and lipase activities, which suggested a capacity for enhanced lipid and protein digestion for winter energy storage. Metabolomic analysis revealed enrichment of sphingolipid metabolites in autumn, which implicated in lipid metabolism and immune regulation. Furthermore, the autumn exhibited a greater diversity and abundance of antibiotic resistance genes. Our results demonstrated that seasonal dietary variation, digestive enzyme adaptation, microbiota reshaping, metabolite-mediated signaling collectively enabled E. lucius to regulate digestive physiology, as well as efficiently assimilating nutrients and maintaining energy balance in response to fluctuating resource availability in wild. Our study offers valuable insights into the ecological adaptation mechanisms of cold-water fish species.