Experimental metal contamination reduces gut microbiota diversity and alters its composition and function in wild-caught fish

Abstract

Wild organisms face environmental stressors that can interact and affect their health unexpectedly. Evidence suggests that responses to stressors may be mediated by changes in the gut microbiota, with cascading effects on host health. However, the combined effects of multiple stressors on host microbiota are still overlooked. Here, we investigated the single and interactive effects of realistic metal contamination (i.e., a mixture of Cd, Cu, Zn) and an immune challenge (i.e., lipopolysaccharides - LPS and phytohaemagglutinin - PHA) mimicking a parasite attack on the taxonomic and functional diversity and composition of gut microbiota among several wild freshwater fish (Gobio occitaniae) populations sampled along a gradient of contamination in streams. We found that the experimental metal contamination strongly altered the gut microbial community, with no interaction with the immune secondary stressor. Indeed, metal contamination reduced both taxonomic and functional gut microbial diversity, affecting the microbial communitys taxonomic and functional composition, with predicted consequences for their functional role in fish. Metal contamination reduced microbial function related to molecule biosyntheses (e.g., cell structure and amino acid precursors) while increasing functions associated with energy production (e.g., anaerobic respiration). In addition, populations sampled along a gradient of pollution in the wild did not differ in their response, suggesting a consistent impact of contaminants irrespective of the hosts past exposure to pollution. Our results highlight how realistic levels of metal contamination alter the fish gut microbiota, potentially affecting their ability to cope with environmental stressors, though long-term fitness implications are still unclear.