Discovery and validation of candidate smoltification gene expression biomarkers across multiple species and ecotypes of Pacific salmonids

Abstract

Early marine survival of juvenile salmon is intimately associated with their physiological condition during smoltification and ocean entry. Smoltification (parr–smolt transformation) is a developmental process that allows salmon to acquire seawater tolerance in preparation for marine living. Traditionally, this developmental process has been monitored using gill Na+/K+-ATPase (NKA) activity or plasma hormones, but gill gene expression offers the possibility of another method. Here, we describe the discovery of candidate genes from gill tissue for staging smoltification using comparisons of microarray studies with particular focus on the commonalities between anadromous Rainbow trout and Sockeye salmon datasets, as well as a literature comparison encompassing more species. A subset of 37 candidate genes mainly from the microarray analyses was used for TaqMan quantitative PCR assay design and their expression patterns were validated using gill samples from four groups, representing three species and two ecotypes: Coho salmon, Sockeye salmon, stream-type Chinook salmon and ocean-type Chinook salmon. The best smoltification biomarkers, as measured by consistent changes across these four groups, were genes involved in ion regulation, oxygen transport and immunity. Smoltification gene expression patterns (using the top 10 biomarkers) were confirmed by significant correlations with NKA activity and were associated with changes in body brightness, caudal fin darkness and caudal peduncle length. We incorporate gene expression patterns of pre-smolt, smolt and de-smolt trials from acute seawater transfers from a companion study to develop a preliminary seawater tolerance classification model for ocean-type Chinook salmon. This work demonstrates the potential of gene expression biomarkers to stage smoltification and classify juveniles as pre-smolt, smolt or de-smolt.

Discovery and surveillance of viruses from salmon in British Columbia using viral immune-response biomarkers, metatranscriptomics, and high-throughput RT-PCR

“…Our results confirm the previous finding via RT-PCR that PsNV primarily infects gill tissue. This finding supports our previous hypothesis that disease caused by the virus is manifested when fish undergo physical stress due to osmotic imbalance as they move from fresh to marine waters during smoltification ( Houde et al. 2019 ; Mordecai et al.…”

Identification of Hypoxia-Specific Biomarkers in Salmonids Using RNA-Sequencing and Validation Using High-Throughput qPCR

“…Indeed, adjustments of gill morphology, which includes the morphological changes in the gills, along with possible changes in gill ventilation and perfusion to secure oxygen uptake, have a negative effect on the ionoregulatory status of the fish (Matey et al 2008). Therefore, our results suggest that hypoxia may also affect the expression of osmoregulation and ionoregulation genes in gill tissue, which is important given that this tissue is the primary organ involved in both osmoregulation and ionoregulation (Houde et al 2019b).…”

Photoperiod-dependent developmental reprogramming of the transcriptional response to seawater entry in Atlantic salmon (Salmo salar)

“…Triggers may include osmotic stress due to the hyper-osmotic SW environment as well as direct responses to changes in the concentrations of specific ions either in the gill or in internal organs such as the kidney and intestine ( Evans and Somero 2008 ; Evans 2010 ; Kültz 2012 ). However, the specific response is expected to differ drastically between SW-ready smolts and unprepared juveniles ( Stagg et al 1989 ; Houde et al 2018 ). The importance of SW-exposure for completion of the smolting process and establishment of a SW phenotype is clearly demonstrated by the process of “de-smoltification,” which occurs if migration to SW is prevented and involves a loss of tolerance to SW ( Stefansson et al 1998 ; Arnesen et al 2003 ).…”