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

Akbarzadeh, Arash; Houde, Aimee Lee S; Sutherland, Ben J G; Günther, Oliver P; Miller, Kristina M

doi:10.1534/g3.120.401487

Cited by 41Environmental Toxicology and EcotoxicologyPhysiological and biochemical adaptationsAquaculture disease management and microbiota

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

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Akbarzadeh, Arash, Houde, Aimee Lee S, Sutherland, Ben J G, Günther, Oliver P, Miller, Kristina M·2020·G3 Genes|Genomes|Genetics

DOI 10.1534/g3.120.401487PMC PMC7466982

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Abstract

Identifying early gene expression responses to hypoxia (i.e., low dissolved oxygen) as a tool to assess the degree of exposure to this stressor is crucial for salmonids, because they are increasingly exposed to hypoxic stress due to anthropogenic habitat change, e.g., global warming, excessive nutrient loading, and persistent algal blooms. Our goal was to discover and validate gill gene expression biomarkers specific to the hypoxia response in salmonids across multi-stressor conditions. Gill tissue was collected from 24 freshwater juvenile Chinook salmon (Oncorhynchus tshawytscha), held in normoxia [dissolved oxygen (DO) > 8 mg L-1] and hypoxia (DO = 4‒5 mg L-1) in 10 and 18° temperatures for up to six days. RNA-sequencing (RNA-seq) was then used to discover 240 differentially expressed genes between hypoxic and normoxic conditions, but not affected by temperature. The most significantly differentially expressed genes had functional roles in the cell cycle and suppression of cell proliferation associated with hypoxic conditions. The most significant genes (n = 30) were selected for real-time qPCR assay development. These assays demonstrated a strong correlation (r = 0.88; P < 0.001) between the expression values from RNA-seq and the fold changes from qPCR. Further, qPCR of the 30 candidate hypoxia biomarkers was applied to an additional 322 Chinook salmon exposed to hypoxic and normoxic conditions to reveal the top biomarkers to define hypoxic stress. Multivariate analyses revealed that smolt stage, water salinity, and morbidity status were relevant factors to consider with the expression of these genes in relation to hypoxic stress. These hypoxia candidate genes will be put into application screening Chinook salmon to determine the identity of stressors impacting the fish.

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Upregulation of cyclin-dependent kinase inhibitors CDKN1B and CDKN1C in hepatocellular carcinoma-derived cells via goniothalamin-mediated protein stabilization and epigenetic modifications
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Identification of an Endothelin-converting Enzyme-2-specific Fluorigenic Substrate and Development of an in Vitro and ex Vivo Enzymatic Assay*
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Identification of a transient Sox5 expressing progenitor population in the neonatal ventral forebrain by a novel cis-regulatory element
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Salmonid gene expression biomarkers indicative of physiological responses to changes in salinity, temperature, but not dissolved oxygen
Houde, A. L. S., Akbarzadeh, A., Günther, O. P., Li, S., Patterson, D. A., Farrell, A. P., Hinch, S. G., & Miller, K. M. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.198036 · Cited by 61 · see citing works
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Genomic approaches in the identification of hypoxia biomarkers in model fish species
Zhang, Z., Ju, Z., Wells, M. C., & Walter, R. B. (2009) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2009.07.021 · Cited by 50 · see citing works
Hypoxic Stress Induced Gene Modulation in Medaka (Oryzias latipes) and Xiphophorus maculatus
Kirk, L. M. (2009) · Cited by 1 · see citing works
The Atlantic salmon’s stress- and immune-related transcriptional responses to moderate hypoxia, an incremental temperature increase, and these challenges combined
Beemelmanns, A., Zanuzzo, F. S., Sandrelli, R. M., Rise, M. L., & Gamperl, A. K. (2021) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkab102 · Cited by 51 · see citing works
The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
Beemelmanns, A., Zanuzzo, F. S., Xue, X., Sandrelli, R. M., Rise, M. L., & Gamperl, A. K. (2021) · BMC Genomics · doi:10.1186/s12864-021-07464-x · Cited by 125 · see citing works

Authors: Akbarzadeh, A., Houde, A. L. S., Sutherland, B. J. G., Günther, O. P., & Miller, K. M.
Affiliations: Fisheries and Oceans Canada (CA)
Günther Analytics, Vancouver, BC Canada
Corresponding author: Akbarzadeh, Arash
Miller, Kristina M
ORCID: Akbarzadeh, Arash
Houde, Aimee Lee S
Sutherland, Ben J G
Günther, Oliver P
Miller, Kristina M
Venue: G3 Genes|Genomes|Genetics
Publisher: Oxford University Press (OUP)
Published: 2020-09-01
Volume: 10
Issue: 9
Pages: 3321-3336
ISSN: 2160-1836 (ISSN-L)
DOI: 10.1534/g3.120.401487
PMC: PMC7466982
OpenAlex: W3044719851
Cited by: 40
References: 101
Citations by year: 2026: 8 · 2025: 9 · 2024: 10 · 2023: 4 · 2022: 5 · 2021: 4
FWCI: 1.30
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: G3 Genes Genomes Genetics (publishedVersion, cc-by)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (cc-by)
Funders: Pacific Salmon Foundation
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Keywords: hypoxia, hypoxia markers, Oncorhynchus tshawytscha, gill gene expression, dissolved oxygen, differentially expressed genes, cell cycle, cell proliferation, qPCR assay validation, water salinity, stressor identification
MeSH terms: Animals, Hypoxia, RNA, Salmonidae, Biomarkers, Sequence Analysis, RNA

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

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