Immune response genes and pathogen presence predict migration survival in wild salmon smolts

Abstract

We present the first data to link physiological responses and pathogen presence with subsequent fate during migration of wild salmonid smolts. We tagged and non-lethally sampled gill tissue from sockeye salmon (Oncorhynchus nerka) smolts as they left their nursery lake (Chilko Lake, BC, Canada) to compare gene expression profiles and freshwater pathogen loads with migration success over the first ~1150 km of their migration to the North Pacific Ocean using acoustic telemetry. Fifteen per cent of smolts were never detected again after release, and these fish had gene expression profiles consistent with an immune response to one or more viral pathogens compared with fish that survived their freshwater migration. Among the significantly upregulated genes of the fish that were never detected postrelease were MX (interferon-induced GTP-binding protein Mx) and STAT1 (signal transducer and activator of transcription 1-alpha/beta), which are characteristic of a type I interferon response to viral pathogens. The most commonly detected pathogen in the smolts leaving the nursery lake was infectious haematopoietic necrosis virus (IHNV). Collectively, these data show that some of the fish assumed to have died after leaving the nursery lake appeared to be responding to one or more viral pathogens and had elevated stress levels that could have contributed to some of the mortality shortly after release. We present the first evidence that changes in gene expression may be predictive of some of the freshwater migration mortality in wild salmonid smolts.

Differential expression of long non-coding RNAs in three genetic lines of rainbow trout in response to infection with Flavobacterium psychrophilum

“…GPB1 gene transcript also shows correlated expression with lncRNA in human26. Previous reports suggested that gbp1 is one of the differentially regulated immune response genes against microbial pathogens in salmon and trout927.…”

Nutrigenomics and immune function in fish: new insights from omics technologies

“…The pathogen exposure in fish starts immediately after hatching from their protective chorions and is further enhanced during the mouth and gut opening stages and at the onset of exogenous feeding (Castro et al., 2015). Furthermore, many fish species are exposed to different and unfamiliar pathogens when they switch between fresh and salt water environments (Jeffries et al., 2014). Evidence is also growing that some fish, including non-migratory species, are being exposed to novel pathogens as a result of climate change (Crozier and Hutchings, 2014).…”

Molecular indices of viral disease development in wild migrating salmon†

“…Collections occurred over 3 years, 2007, 2011 and 2012 at the Fraser River Chilko Lake smolt fence. In 2012, smolts were acoustically tagged and tracked (Jeffries et al 2014). 2007 was a year of very poor smolt survivalA.TissueChallengeSockeyeAtlanticChumTotalHead kidneyInjected45 (45)40 (25)45 (20)Waterborne5011645GillInjected455Waterborne4511543Liver45Injected45Spleen45Injected45Grand total275276133 684 B.TissueTotalJaundice/anemiaGill3616Head kidney3516Liver3616Spleen3113Heart3616Grand total…”

“…In 2012, we conducted an acoustic tracking study and assessed linkages between 18 infectious agents and 50 stress and immune-related genes and migratory fate. We showed that fish with high loads of IHNv and those containing a correlated antiviral type signature (including up-regulation of MX and STAT1, the two genes overlapping with the VDD biomarkers) generally disappeared within the first 80 km of downstream migration (Jeffries et al , 2014), likely due to enhanced risk of predation by resident Bull trout (Furey, 2016). We applied the validated VDD biomarkers on the 213 smolts from the Jeffries study collected at the Chilko smolt fence in 2007, 2011 and 2012 to determine if there was evidence of viral disease in these fish (Table 1D).…”

“…For the audit samples, 50 assays to 49 infectious agents were applied, including all agents outlined in Miller et al (2016) plus three additional pathogenic bacteria known to cause disease on salmon farms: Moritella viscosa , Tenacibaculum maritimum and Yersinia ruckeri (assays in Table 2). These panels were applied to the (i) multi-species IHNv challenge trials to assess performance across species and tissues; (ii) jaundice/anemia Chinook salmon farm outbreak, including multiple tissues to validate performance of the VDD panel on a novel disease hypothesized to be virally induced; (iii) farm audit samples to assess the ability of the VDD panel to differentiate viral versus bacterial or parasitic diseases; and (iv) wild migrating sockeye salmon smolts to discern whether the VDD panel could identify the presence of a viral disease state associated with IHNv infection from non-destructive gill biopsy samples of wild salmon (Jeffries et al , 2014) (experimental designs outlined in Table 1; schematic in Fig. 1).…”