Abstract
BackgroundReduction of Lepeophtheirus salmonis infection in Atlantic salmon achieved by glucosinolates (GLs) from Brassica plants was recently reported. However, wider application of functional feeds based on GLs requires better knowledge of their positive and adverse effects.MethodsLiver, distal kidney and muscle transcriptomes of salmon exposed to the extreme dose of GLs were profiled by microarray, while qPCR analysis followed up selected hepatic and renal responses under the extreme and moderate GLs dose during the L. salmonis challenge. Transcriptional analysis were complemented with measurements of organ indices, liver steatosis and plasma profiling, including indicators of cytolysis and bilirubin. Finally, the third trial was performed to quantify the effect of lower GLs doses on growth.ResultsThe extreme GLs dose caused a decrease in hepatic fat deposition and growth, in line with microarray findings, which suggested tissue remodeling and reduction of cellular proliferation in the skeletal muscle and liver. Lower GLs inclusion levels in a follow-up trial did not show negative effects on growth. Microarray analysis of the distal kidney pointed to activation of anti-fibrotic responses under the overexposure. However, analyses of ALT, CK and AST enzymes in plasma provided no evidence of increased cytolysis and organ damage. Prevalent activation of phase-2 detoxification genes that occurred in all three tissues could be considered part of beneficial effects caused by the extreme dose of GLs. In addition, transcriptomic evidence suggested GLs-mediated iron and heme withdrawal response, including increased heme degradation in muscle (upregulation of heme oxygenase-1), decrease of its synthesis in liver (downregulation of porphobilinogen deaminase) and increased iron sequestration from blood (hepatic induction of hepcidin-1 and renal induction of intracellular storage protein ferritin). This response could be advantageous for salmon upon encountering lice, which depend on the host for the provision of iron carrying heme. Most of the hepatic genes studied by qPCR showed similar expression levels in fish exposed to GLs, lice and their combination, while renal induction of leptin suggested heightened stress by the combination of extreme dose of GLs and lice. High expression of interferon γ (cytokine considered organ-protective in mammalian kidney) was detected at the moderate GLs level. This fish also showed highest plasma bilirubin levels (degradation product of heme), and had lowest number of attached lice, further supporting hypothesis that making heme unavailable to lice could be part of an effective anti-parasitic strategy.ConclusionsModulation of detoxification and iron metabolism in Atlantic salmon tissues could be beneficial prior and during lice infestations. Investigation of anti-lice functional feeds based on low and moderate GLs inclusion levels thus deserves further attention.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1921-7) contains supplementary material, which is available to authorized users.
Highlights
Reduction of Lepeophtheirus salmonis infection in Atlantic salmon achieved by glucosinolates (GLs) from Brassica plants was recently reported
Fish growth In Trial 1, no significant reduction in growth was seen in parasite free not infected with lice (NI)-13 fish at the end of the 17–18 day exposure period to the extreme dose of GLs (Table 1)
Alanine aminotransferase (ALT) and aspartate aminotransferase (AST) are found in liver parenchymal cells, and in kidney, muscle and other tissues [38], while creatine kinase (CK) is an enzyme that mainly increases due to leakage from muscle cells [39, 40]
Summary
Reduction of Lepeophtheirus salmonis infection in Atlantic salmon achieved by glucosinolates (GLs) from Brassica plants was recently reported. Several recent studies describe the severity of the situation in detail, including incurred economic losses [2], mortalities associated with application of chemical treatments [1] and in wild salmonid populations [3,4,5], risk of pathogenic virus transmission [6,7,8], and development of resistance to available parasiticides [9,10,11,12]. As chemical treatments are becoming limited and less efficient, there is an increasing interest in the development of anti-lice functional feeds. GLs are hydrolyzed by the enzyme myrosinase into compounds that defend plants against a wide range of herbivores, including insects and aquatic invertebrates (reviewed by [19]). Isothiocyanates (ITCs) constitute the major bioactive fraction of the hydrolysis products of GLs, with antibacterial properties in vitro [21], and antifungal effector properties in live plant cells [22]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
