Dietary phytochemicals modulate skin gene expression and reduce lice counts after infection in Atlantic salmon

BACKGROUND: The use of phytochemicals is a promising solution in biological control against salmon louse (Lepeophtheirus salmonis). Glucosinolates (Gls) belong to a diverse group of compounds used as protection against herbivores by plants in the Brassicaceae family, while in vertebrates, ingested glucosinolates exert health-promoting effects due to their antioxidant and detoxifying properties as well as effects on cell proliferation and growth. The aim of this study was to investigate if Atlantic salmon fed two different doses of glucosinolate-enriched feeds would be protected against lice infection. The effects of feeding high dose of glucosinolates before the infection, and of high and low doses 5 weeks into the infection were studied. METHODS: Skin was screened by 15k oligonucleotide microarray and qPCR. RESULTS: 25% reduction (p < 0.05) in lice counts was obtained in the low dose group and 17% reduction in the high dose group compared to fish fed control feed. Microarray analysis revealed induction of over 50 interferon (IFN)-related genes prior to lice infection. Genes upregulated 5 weeks into the infection in glucosinolate-enriched dietary groups included Type 1 pro-inflammatory factors, antimicrobial and acute phase proteins, extracellular matrix remodeling proteases and iron homeostasis regulators. In contrast, genes involved in muscle contraction, lipid and glucose metabolism were found more highly expressed in the skin of infected control fish. CONCLUSIONS: Atlantic salmon fed glucosinolates had a significantly lower number of sea lice at the end of the experimental challenge. Feeding glucosinolates coincided with increased expression of IFN-related genes, and higher expression profiles of Type 1 immune genes late into the infection. In addition, regulation of genes involved in the metabolism of iron, lipid and sugar suggested an interplay between metabolism of nutrients and mechanisms of resistance. Atlantic salmon received feeds enriched in plant derived glucosinolates (Gls), with the approximate GLs content of 7.3 μmol/g and 26.4 μmol/g in the low dose group (LD) or the high dose group (HD), respectively.The treatment groups tested in this part of the study were named: infected C (I-C) infected LD (I-LD) and infected HD (I-HD), in three tank replicates. Skin samples were collected before infection and after 31-35 days of experimental lice infection. In addition, six tanks of fish were used in a parallel feed study to assess the effect of GLs feeding per se (without infection). These groups of fish were named not-infected high dose (NI-HD) and not-infected control (NI-C) respectively. Sampling of skin tissue was performed after 17-18 days of feeding using the same protocol as for the infected fish. Five individuals from each group were analyzed with microarrays, and 4 fish from NI-HD. Pooled skin samples of two salmon from each dietary group were used as a reference.