The crucial role of fish mucus in regulating progeny inflammation and microbial homeostasis

Abstract

Maternal immunity plays a vital role in protecting offspring from pathogen invasion, and it is present in nearly all vertebrates. As the most ancient vertebrates, teleost fish continuously secrete a substantial amount of mucus due to their unique living environment, and often exhibit schooling behavior. Previous studies have highlighted the presence of numerous immune components in the mucus of fish, that plays a crucial role in resisting pathogens. We hypothesize that this represents a distinctive maternal immune response mechanism in fish. In this study, we established a dextran sulfate sodium (DSS)-induced injury model by immersing zebrafish larvae in 0.5% DSS. This elicited robust inflammatory responses and showed DSS-induced alterations in microbial abundance via 16S rRNA sequencing. These changes included the disruption of normal gut structure; an increase in goblet cells; increased expression of inflammatory cytokines; and infiltration of neutrophils and macrophages into the gut, as well as an increase in pathogenic bacteria and a decline in probiotic bacteria. Furthermore, we conducted a mucus protection test by adding adult zebrafish mucus in fish tank water containing 0.5% DSS to test our hypothesis. As suspected, the mucus from adult zebrafish exhibited a protective role in defending zebrafish larvae against DSS-induced enteritis by alleviating excessive inflammatory responses and increasing probiotic abundance. In conclusion, our results confirm a significant role of adult fish mucus in the immune response of teleost fish to DSS-induced inflammation. Collectively, our findings show that the mucus of adult zebrafish may represent a novel form of maternal immunization, playing roles analogous to mammalian milk in immune regulatory functions.