River contamination shapes the microbiome and antibiotic resistance in sharpbelly (Hemiculter leucisculus)

Highlights: • Water contamination altered fish gut bacterial community composition. • Water bacteria were main stressors to perturb fish gut microbiome. • Aggravated external environment elicited the enhancement of antibiotic resistance. • External heavy metals, gut integron and microbiome dominated gut ARGs structure. • Integron and bacteria contributed to ARGs transmission through water–fish pathway. Animals living in urban river systems play critical roles in the dissemination of microbiome and antibiotic resistance that poses a strong threat to public health. This study provides a comprehensive profile of microbiota and antibiotic resistance genes (ARGs) of sharpbelly (Hemiculter leucisculus) and the surrounding water from five sites along the Ba River. Results showed Proteobacteria, Firmicutes and Fusobacteria were the dominant bacteria in gut of H. leucisculus. With the aggravation of water pollution, bacterial biomass of fish gut significantly decreased and the proportion of Proteobacteria increased to become the most dominant phylum eventually. To quantify the contributions of influential factors on patterns of gut microbiome with structural equation model (SEM), water bacteria were confirmed to be the most stressors to perturb fish gut microbiome. SourceTracker model indicated that deteriorating living surroundings facilitated the invasion of water pathogens to fish gut eco-environments. Additionally, H. leucisculus gut is an important reservoir of ARGs in Ba River with relative abundance up to 9.86 × 10⁻¹/copies. Among the ARGs, tetracycline and quinolone resistance genes were detected in dominant abundance. Deterioration of external environments elicited the accumulation of ARGs in fish gut. Intestinal class I integron, environmental heavy metal residues and gut bacteria were identified as key drivers of intestinal ARGs profiles in H. leucisculus. Analysis of SEM and co-occurrence patterns between ARGs and bacterial hosts indicated that class I integron and bacterial community played vital roles in ARGs transmission through water-fish pathway. In general, this study highlighted hazards of water contamination to microbiome and ARGs in aquatic animals and provided a new perspective to better understand the bacteria and ARGs dissemination in urban river ecosystems.