Facing warm temperatures during migration: cardiac mRNA responses of two adult Oncorhynchus nerka populations to warming and swimming challenges

Abstract

The main findings of the current study were that exposing adult sockeye salmon Onchorhynchus nerka to a warm temperature that they regularly encounter during their river migration induced a heat shock response at an mRNA level, and this response was exacerbated with forced swimming. Similar to the heat shock response, increased immune defence-related responses were also observed after warm temperature treatment and with a swimming challenge in two different populations (Chilko and Nechako), but with some important differences. Microarray analyses revealed that 347 genes were differentially expressed between the cold (12-13° C) and warm (18-19° C) treated fish, with stress response (GO:0006950) and response to fungus (GO:0009620) elevated with warm treatment, while expression for genes involved in oxidative phosphorylation (GO:0006119) and electron transport chain (GO:0022900) elevated for cold-treated fish. Analysis of single genes with real-time quantitative PCR revealed that temperature had the most significant effect on mRNA expression levels, with swimming and population having secondary influences. Warm temperature treatment for the Chilko population induced expression of heat shock protein (hsp) 90α, hsp90β and hsp30 as well as interferon-inducible protein. The Nechako population, which is known to have a narrower thermal tolerance window than the Chilko population, showed even more pronounced stress responses to the warm treatment and there was significant interaction between population and temperature treatment for hsp90β expression. Moreover, significant interactions were noted between temperature treatment and swimming challenge for hsp90α and hsp30, and while swimming challenge alone increased expression of these hsps, the expression levels were significantly elevated in warm-treated fish swum to exhaustion. In conclusion, it seems that adult O. nerka currently encounter conditions that induce several cellular defence mechanisms during their once-in-the-lifetime migration. As river temperatures continue to increase, it remains to be seen whether or not these cellular defences provide sufficient protection for all O. nerka populations.

Developing specific molecular biomarkers for thermal stress in salmonids

“…Concordance of several of the discovered and published signatures on chronic and acute temperature stress on 16 K, 32 K and 44 K GRASP platforms (using Blast search-based mapping) are shown in Table 1 . Quinn et al [ 32 ] and Jeffries et al [ 30 ] provided chronic temperature stress signatures while the Quinn et al [ 33 ], Lewis et al [ 34 ] and Anttila et al [ 12 ] studies provided acute temperature stress signatures. There are more features in common between the Quinn et al [ 32 ] (chronic) and Anttila et al [ 12 ] (chronic) signatures (17 EST identifiers) than between the Quinn et al [ 33 ] (acute) and Anttila et al [ 12 ] (chronic) signatures (11 EST identifiers).…”

“…Presented for each gene are the temperature stress response signatures, EST ID for the 44 K cGRASP microarray, and Atlantic salmon gene ID. The symbol ‘x’ indicates that the gene was included in the thermal response signature for the specified analysis Gene Name Gene Symbol EST ID Gene ID Chromosome Intersect 2007, 2008, 2009 (CS0101i) Jeffries et al [ 9 ] (ES0013) 2007 Sockeye (EX0102a) 2008 Sockeye (EX0103a) 2009 Pink (EX0101a) Jeffries et al [ 30 ] publication: (16 K) Quinn et al [ 32 ] publication Table S1 (32 K) Anttila et al [ 12 ] publication Table S1 (16 K) Quinn et al [ 33 ] publication Table S2 (32 K) Lewis et al [ 34 ] (24 h) Lewis et al [ 34 ] (4 h) Protein folding and rescue Serpin H1 precursor SERPINH1 C044R036 106,581,278 20 x x x x x C265R019 x x x x x C205R085 x x x x x C101R077 x CA063723 x x C009R155 106,613,072 9 x ...…”

“…Given the overlap of selected candidate thermal stress biomarkers in different tissues, nine EST identifiers from the Anttila et al [ 12 ] dataset on sockeye heart muscle mapped to HSP90a (ch15), HSP90ab1 (ch15), SFRF2, and CIRBP (Table 3 ).…”

“…Although expression of proteins can be changed by multiple mechanisms during synthesis and degradation, temperature dependent changes in transcription of genes are one of the key events in modifying the proteome of the tissues [ 11 ]. The expression of mRNA represents a primary response to environmental change that often, but not always, leads to changes in protein expression and cell function [ 12 ]. Stress responses involve expression of a series of evolutionarily conserved stress-responsive genes that include genes controlling cell cycle, protein folding and repair, DNA and chromatin stabilization and repair, removal of damaged proteins, and energy metabolism [ 13 ].…”

Proteomic analysis of cardiac response to thermal acclimation in the eurythermal goby fishGillichthys mirabilis

“…However, despite the crucial role played by the cardiac system in determining thermal tolerance, little is known about gene and protein level responses to temperature in fish hearts, apart from a few transcriptomic studies focusing on highly active fish species (Vornanen et al, 2005;Castilho et al, 2009;Anttila et al, 2014). Recent developments in proteomics technology and the increasing availability of genomic sequence information to facilitate protein identification have allowed for the successful use of proteomic experimental approaches to investigate non-model organisms (Tomanek, 2005(Tomanek, , 2011(Tomanek, , 2014Dowd et al, 2008Dowd et al, , 2010Tomanek and Zuzow, 2010;Serafini et al, 2011;Fields et al, 2012).…”