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

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.

Host–parasite transcriptomics during immunostimulant-enhanced rejection of salmon lice (Lepeophtheirus salmonis) by Atlantic salmon (Salmo salar)

“…Similarly, il-8 was found to be up-regulated at 7 d post infection in pink salmon anterior kidney and skin (Jones et al 2007). In the present study, up-regulation of il-1β occurred consistently in LD-fed Atlantic salmon (the feed group with the lowest infection), as it did in pink salmon skin in previous studies, also coinciding with early responses (6 d after exposure; Sutherland et al 2014). Between HD and LD, the LD was optimal here in terms of il-1β induction and reduction in lice infection levels.…”

“…Although not significant (p = 0.07), there was a trend towards the overexpression of il-8 in the LD salmon; an insignificant trend towards overexpression was also previously observed in Atlantic and pink salmon skin (Sutherland et al 2014). Earlier work found elevated il-8 expression in head kidney/spleen pooled tissues at 7 and 14 d post infection in juvenile chum (Oncorhynchus keta) and pink salmon but no consistent response in il-1β (Jones et al 2008a).…”

“…Increased il-1β expression and innate defenses are important for host rejection of salmon lice; this response is not typical of Atlantic salmon, but rather is typical of the more liceresistant pink salmon and coho salmon (Johnson and Albright 1992;Jones et al 2007;Braden et al 2012Braden et al , 2015Sutherland et al 2014). However, in previous studies of CpG-ODN immunostimulation, Atlantic salmon fed the treatment diet overexpressed il-1β and had lower lice infection levels than controls (Covello et al 2012;Poley et al 2013).…”

“…Up-regulation of il-1β in the skin in response to L. salmonis has been previously observed. For example, il-1β expression was up-regulated specifically in the skin of infected pink salmon (considered to be more resistant) but not Atlantic salmon (Sutherland et al 2014). Considering the potential for immunosuppression of Atlantic salmon by lice-derived PGE 2 and other compounds (Fast et al 2004, it is interesting that the immunostimulation induced a response more characteristic of a successful rejection, as immunostimulation can negate immune suppression (for review see Vadstein 1997).…”

“…Among species, strong inflammatory and cellular immune responses are associated with reduced infection intensities in coho salmon (Oncorhynchus kisutch) and pink salmon (Oncorhynchus gorbuscha) (Johnson and Albright 1992;Jones et al 2007;Braden et al 2012Braden et al , 2015Sutherland et al 2014). Within species, heritable differences in susceptibility indicate potential for selective breeding (Kolstad et al 2005;Gjerde et al 2011).…”