Comparative transcriptomics of Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha during infections with salmon lice Lepeophtheirus salmonis

Ben Jg Sutherland,Ryosuke Yazawa,Motoshige Yasuike,Kim W Koczka,Simon Rm Jones,Ben F Koop,Stuart G Jantzen

doi:10.1186/1471-2164-15-200

Abstract

BackgroundSalmon species vary in susceptibility to infections with the salmon louse (Lepeophtheirus salmonis). Comparing mechanisms underlying responses in susceptible and resistant species is important for estimating impacts of infections on wild salmon, selective breeding of farmed salmon, and expanding our knowledge of fish immune responses to ectoparasites. Herein we report three L. salmonis experimental infection trials of co-habited Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha, profiling hematocrit, blood cortisol concentrations, and transcriptomic responses of the anterior kidney and skin to the infection.ResultsIn all trials, infection densities (lice per host weight (g)) were consistently highest on chum salmon, followed by Atlantic salmon, and lowest in pink salmon. At 43 days post-exposure, all lice had developed to motile stages, and infection density was uniformly low among species. Hematocrit was reduced in infected Atlantic and chum salmon, and cortisol was elevated in infected chum salmon. Systemic transcriptomic responses were profiled in all species and large differences in response functions were identified between Atlantic and Pacific (chum and pink) salmon. Pink and chum salmon up-regulated acute phase response genes, including complement and coagulation components, and down-regulated antiviral immune genes. The pink salmon response involved the largest and most diverse iron sequestration and homeostasis mechanisms. Pattern recognition receptors were up-regulated in all species but the active components were often species-specific. C-type lectin domain family 4 member M and acidic mammalian chitinase were specifically up-regulated in the resistant pink salmon.ConclusionsExperimental exposures consistently indicated increased susceptibility in chum and Atlantic salmon, and resistance in pink salmon, with differences in infection density occurring within the first three days of infection. Transcriptomic analysis suggested candidate resistance functions including local inflammation with cytokines, specific innate pattern recognition receptors, and iron homeostasis. Suppressed antiviral immunity in both susceptible and resistant species indicates the importance of future work investigating co-infections of viral pathogens and lice.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-200) contains supplementary material, which is available to authorized users.

Highlights

Salmon species vary in susceptibility to infections with the salmon louse (Lepeophtheirus salmonis)
Infection density and louse development Infection density (lice per host weight (g)) in Trial 1 was highest in chum salmon, followed by Atlantic salmon and lowest in pink salmon (p < 0.00001) (Figure 1A)
Cortisol, and hematocrit There was a reduction in weight gain in infected chum salmon relative to controls in Trial 1 (p = 0.012), but no differences were identified in Trials 2 and 3

Summary

Introduction

Salmon species vary in susceptibility to infections with the salmon louse (Lepeophtheirus salmonis). Comparing mechanisms underlying responses in susceptible and resistant species is important for estimating impacts of infections on wild salmon, selective breeding of farmed salmon, and expanding our knowledge of fish immune responses to ectoparasites. In the Northern Hemisphere, the salmon louse L. salmonis has the largest impact [1] and must be properly managed to prevent excessive infections and possible damage to wild salmon populations [2]. Lice disperse as free-swimming nauplii and molt to infective copepodids which attach to a host, develop through later stages and feed on skin and mucus [3]. Louse-derived compounds secreted at the site of attachment can be immunomodulatory (e.g., trypsin-like proteases; prostaglandin E2 [16,17,18,19,20]) and may facilitate secondary infections

Results

Discussion

Conclusion