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Transcriptomic responses to high water temperature in two species of Pacific salmon.

Jeffries KM, Hinch SG, Sierocinski T, Pavlidis P, Miller KM - Evol Appl (2013)

Bottom Line: We detected the differential expression of 49 microarray features (29 unique annotated genes and one gene with unknown function) associated with protein folding, protein synthesis, metabolism, oxidative stress and ion transport that were common between populations and species of Pacific salmon held at 19°C compared with fish held at a cooler temperature (13 or 14°C).There was higher mortality in fish held at 19°C, which suggests a possible relationship between a temperature-induced CSR and mortality in these species.Our results suggest that frequently encountered water temperatures ≥19°C, which are capable of inducing a common CSR across species and populations, may increase risk of upstream spawning migration failure for pink and sockeye salmon.

View Article: PubMed Central - PubMed

Affiliation: Centre for Applied Conservation Research Department of Forest and Conservation Sciences, University of British Columbia Vancouver, BC, Canada.

ABSTRACT
Characterizing the cellular stress response (CSR) of species at ecologically relevant temperatures is useful for determining whether populations and species can successfully respond to current climatic extremes and future warming. In this study, populations of wild-caught adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon from the Fraser River, British Columbia, Canada, were experimentally treated to ecologically relevant 'cool' or 'warm' water temperatures to uncover common transcriptomic responses to elevated water temperature in non-lethally sampled gill tissue. We detected the differential expression of 49 microarray features (29 unique annotated genes and one gene with unknown function) associated with protein folding, protein synthesis, metabolism, oxidative stress and ion transport that were common between populations and species of Pacific salmon held at 19°C compared with fish held at a cooler temperature (13 or 14°C). There was higher mortality in fish held at 19°C, which suggests a possible relationship between a temperature-induced CSR and mortality in these species. Our results suggest that frequently encountered water temperatures ≥19°C, which are capable of inducing a common CSR across species and populations, may increase risk of upstream spawning migration failure for pink and sockeye salmon.

No MeSH data available.


Related in: MedlinePlus

Heat map showing the 49 differentially regulated microarray features common between population and species, and the relative fold change (warm treatment relative to the cool treatment). Genes are grouped based on function (1: Molecular chaperones; 2: Transcription/translation/protein transport; 3: Metabolic processes; 4: Oxidative stress/ion binding/signal transduction; 5: Transmembrane transport; 6: DNA repair, cell structure, no gene symbol available). Gene expression levels in the heat map are presented as normalized log2 ratios between an individual fish and the pooled reference. Relative expression levels are indicated by the colour scale, with yellow indicating upregulation and blue indicating down-regulation. Gene symbols or annotation ID's (if gene symbols are not available) are presented along the right side of the heat map.
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fig04: Heat map showing the 49 differentially regulated microarray features common between population and species, and the relative fold change (warm treatment relative to the cool treatment). Genes are grouped based on function (1: Molecular chaperones; 2: Transcription/translation/protein transport; 3: Metabolic processes; 4: Oxidative stress/ion binding/signal transduction; 5: Transmembrane transport; 6: DNA repair, cell structure, no gene symbol available). Gene expression levels in the heat map are presented as normalized log2 ratios between an individual fish and the pooled reference. Relative expression levels are indicated by the colour scale, with yellow indicating upregulation and blue indicating down-regulation. Gene symbols or annotation ID's (if gene symbols are not available) are presented along the right side of the heat map.

Mentions: The effects of temperature and sex were directly compared for each year using two-factor anovas. At q < 0.01, 103 microarray features in 2007, 243 features in 2008, and 3541 features in 2009 had significantly different levels of expression between the temperature treatments (Fig. 3). For the gene lists that differed significantly with temperature, 49 features had common expression patterns (i.e. directional change) between both species, and among populations within species. This represents 47.6%, 20.2% and 1.4% of the significant features in 2007, 2008 and 2009 respectively. Of the 49 features, there were 29 unique annotated genes and 1 gene with an unknown function (Fig. 4). Several of the 29 annotated genes [HSP90AB1, HSP90AA1, SERPINH1 (also known as HSP47), EEF2 and CIRBP] are known to be thermally responsive or have been previously determined to be thermally responsive in sockeye salmon using cDNA microarray techniques (e.g. Jeffries et al. 2012a). Of the 49 features, SERPINH1 had the greatest fold change increase in fish exposed to 19°C, followed by HSP90AB1 and HSP90AA1, while FKBP10 and CIRBP had the greatest fold change decreases (Fig. 4). Other significant genes with multiple copies were ATP1A1, COX6B1, SEPW1 and two splicing factors (SFRS2 and SFRS9). In addition to being thermally responsive, the 30 unique genes are generally involved in cell redox homeostasis, protein folding, calcium and ion homeostasis, protein biosynthesis and metabolism. Additional information for the 49 features can be found in Table S4. Within the 19°C treatments, MAP3K14 was consistently positively correlated with post-sampling survival (P < 0.05; r = 0.60, 0.74, 0.45 in 2007, 2008 and 2009 respectively). Additionally, HSP90AB1 (r = 0.64), SFRS2 (two copies; r = 0.66 and 0.57) and C1orf124 (r = 0.76) were positive correlated and PARK7 (r = −0.66) was negatively correlated with post-sampling survival in 2007, COX6B1 (r = 0.58) was positively correlated and EIF4A2 (r = −0.59) was negatively correlated with post-sampling survival in 2008, and EEF2 (r = −0.66) and ST6GALNAC6 (r = −0.63) were negatively correlated with post-sampling survival in 2009.


Transcriptomic responses to high water temperature in two species of Pacific salmon.

Jeffries KM, Hinch SG, Sierocinski T, Pavlidis P, Miller KM - Evol Appl (2013)

Heat map showing the 49 differentially regulated microarray features common between population and species, and the relative fold change (warm treatment relative to the cool treatment). Genes are grouped based on function (1: Molecular chaperones; 2: Transcription/translation/protein transport; 3: Metabolic processes; 4: Oxidative stress/ion binding/signal transduction; 5: Transmembrane transport; 6: DNA repair, cell structure, no gene symbol available). Gene expression levels in the heat map are presented as normalized log2 ratios between an individual fish and the pooled reference. Relative expression levels are indicated by the colour scale, with yellow indicating upregulation and blue indicating down-regulation. Gene symbols or annotation ID's (if gene symbols are not available) are presented along the right side of the heat map.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3927889&req=5

fig04: Heat map showing the 49 differentially regulated microarray features common between population and species, and the relative fold change (warm treatment relative to the cool treatment). Genes are grouped based on function (1: Molecular chaperones; 2: Transcription/translation/protein transport; 3: Metabolic processes; 4: Oxidative stress/ion binding/signal transduction; 5: Transmembrane transport; 6: DNA repair, cell structure, no gene symbol available). Gene expression levels in the heat map are presented as normalized log2 ratios between an individual fish and the pooled reference. Relative expression levels are indicated by the colour scale, with yellow indicating upregulation and blue indicating down-regulation. Gene symbols or annotation ID's (if gene symbols are not available) are presented along the right side of the heat map.
Mentions: The effects of temperature and sex were directly compared for each year using two-factor anovas. At q < 0.01, 103 microarray features in 2007, 243 features in 2008, and 3541 features in 2009 had significantly different levels of expression between the temperature treatments (Fig. 3). For the gene lists that differed significantly with temperature, 49 features had common expression patterns (i.e. directional change) between both species, and among populations within species. This represents 47.6%, 20.2% and 1.4% of the significant features in 2007, 2008 and 2009 respectively. Of the 49 features, there were 29 unique annotated genes and 1 gene with an unknown function (Fig. 4). Several of the 29 annotated genes [HSP90AB1, HSP90AA1, SERPINH1 (also known as HSP47), EEF2 and CIRBP] are known to be thermally responsive or have been previously determined to be thermally responsive in sockeye salmon using cDNA microarray techniques (e.g. Jeffries et al. 2012a). Of the 49 features, SERPINH1 had the greatest fold change increase in fish exposed to 19°C, followed by HSP90AB1 and HSP90AA1, while FKBP10 and CIRBP had the greatest fold change decreases (Fig. 4). Other significant genes with multiple copies were ATP1A1, COX6B1, SEPW1 and two splicing factors (SFRS2 and SFRS9). In addition to being thermally responsive, the 30 unique genes are generally involved in cell redox homeostasis, protein folding, calcium and ion homeostasis, protein biosynthesis and metabolism. Additional information for the 49 features can be found in Table S4. Within the 19°C treatments, MAP3K14 was consistently positively correlated with post-sampling survival (P < 0.05; r = 0.60, 0.74, 0.45 in 2007, 2008 and 2009 respectively). Additionally, HSP90AB1 (r = 0.64), SFRS2 (two copies; r = 0.66 and 0.57) and C1orf124 (r = 0.76) were positive correlated and PARK7 (r = −0.66) was negatively correlated with post-sampling survival in 2007, COX6B1 (r = 0.58) was positively correlated and EIF4A2 (r = −0.59) was negatively correlated with post-sampling survival in 2008, and EEF2 (r = −0.66) and ST6GALNAC6 (r = −0.63) were negatively correlated with post-sampling survival in 2009.

Bottom Line: We detected the differential expression of 49 microarray features (29 unique annotated genes and one gene with unknown function) associated with protein folding, protein synthesis, metabolism, oxidative stress and ion transport that were common between populations and species of Pacific salmon held at 19°C compared with fish held at a cooler temperature (13 or 14°C).There was higher mortality in fish held at 19°C, which suggests a possible relationship between a temperature-induced CSR and mortality in these species.Our results suggest that frequently encountered water temperatures ≥19°C, which are capable of inducing a common CSR across species and populations, may increase risk of upstream spawning migration failure for pink and sockeye salmon.

View Article: PubMed Central - PubMed

Affiliation: Centre for Applied Conservation Research Department of Forest and Conservation Sciences, University of British Columbia Vancouver, BC, Canada.

ABSTRACT
Characterizing the cellular stress response (CSR) of species at ecologically relevant temperatures is useful for determining whether populations and species can successfully respond to current climatic extremes and future warming. In this study, populations of wild-caught adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon from the Fraser River, British Columbia, Canada, were experimentally treated to ecologically relevant 'cool' or 'warm' water temperatures to uncover common transcriptomic responses to elevated water temperature in non-lethally sampled gill tissue. We detected the differential expression of 49 microarray features (29 unique annotated genes and one gene with unknown function) associated with protein folding, protein synthesis, metabolism, oxidative stress and ion transport that were common between populations and species of Pacific salmon held at 19°C compared with fish held at a cooler temperature (13 or 14°C). There was higher mortality in fish held at 19°C, which suggests a possible relationship between a temperature-induced CSR and mortality in these species. Our results suggest that frequently encountered water temperatures ≥19°C, which are capable of inducing a common CSR across species and populations, may increase risk of upstream spawning migration failure for pink and sockeye salmon.

No MeSH data available.


Related in: MedlinePlus