The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia

BACKGROUND: Increases in ocean temperatures and in the frequency and severity of hypoxic events are expected with climate change, and may become a challenge for cultured Atlantic salmon and negatively affect their growth, immunology and welfare. Thus, we examined how an incremental temperature incre...

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Published in:BMC Genomics
Main Authors: Beemelmanns, Anne, Zanuzzo, Fábio S., Xue, Xi, Sandrelli, Rebeccah M., Rise, Matthew L., Gamperl, A. Kurt
Format: Text
Language:English
Published: BioMed Central 2021
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042886/
http://www.ncbi.nlm.nih.gov/pubmed/33845767
https://doi.org/10.1186/s12864-021-07464-x
id ftpubmed:oai:pubmedcentral.nih.gov:8042886
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spelling ftpubmed:oai:pubmedcentral.nih.gov:8042886 2023-05-15T15:32:04+02:00 The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia Beemelmanns, Anne Zanuzzo, Fábio S. Xue, Xi Sandrelli, Rebeccah M. Rise, Matthew L. Gamperl, A. Kurt 2021-04-12 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042886/ http://www.ncbi.nlm.nih.gov/pubmed/33845767 https://doi.org/10.1186/s12864-021-07464-x en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042886/ http://www.ncbi.nlm.nih.gov/pubmed/33845767 http://dx.doi.org/10.1186/s12864-021-07464-x © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. CC0 PDM CC-BY BMC Genomics Research Article Text 2021 ftpubmed https://doi.org/10.1186/s12864-021-07464-x 2021-04-18T00:48:50Z BACKGROUND: Increases in ocean temperatures and in the frequency and severity of hypoxic events are expected with climate change, and may become a challenge for cultured Atlantic salmon and negatively affect their growth, immunology and welfare. Thus, we examined how an incremental temperature increase alone (Warm & Normoxic-WN: 12 → 20 °C; 1 °C week(− 1)), and in combination with moderate hypoxia (Warm & Hypoxic-WH: ~ 70% air saturation), impacted the salmon’s hepatic transcriptome expr\ession compared to control fish (CT: 12 °C, normoxic) using 44 K microarrays and qPCR. RESULTS: Overall, we identified 2894 differentially expressed probes (DEPs, FDR < 5%), that included 1111 shared DEPs, while 789 and 994 DEPs were specific to WN and WH fish, respectively. Pathway analysis indicated that the cellular mechanisms affected by the two experimental conditions were quite similar, with up-regulated genes functionally associated with the heat shock response, ER-stress, apoptosis and immune defence, while genes connected with general metabolic processes, proteolysis and oxidation-reduction were largely suppressed. The qPCR assessment of 41 microarray-identified genes validated that the heat shock response (hsp90aa1, serpinh1), apoptosis (casp8, jund, jak2) and immune responses (apod, c1ql2, epx) were up-regulated in WN and WH fish, while oxidative stress and hypoxia sensitive genes were down-regulated (cirbp, cyp1a1, egln2, gstt1, hif1α, prdx6, rraga, ucp2). However, the additional challenge of hypoxia resulted in more pronounced effects on heat shock and immune-related processes, including a stronger influence on the expression of 14 immune-related genes. Finally, robust correlations between the transcription of 19 genes and several phenotypic traits in WH fish suggest that changes in gene expression were related to impaired physiological and growth performance. CONCLUSION: Increasing temperature to 20 °C alone, and in combination with hypoxia, resulted in the differential expression of genes involved in ... Text Atlantic salmon Salmo salar PubMed Central (PMC) BMC Genomics 22 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Beemelmanns, Anne
Zanuzzo, Fábio S.
Xue, Xi
Sandrelli, Rebeccah M.
Rise, Matthew L.
Gamperl, A. Kurt
The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
topic_facet Research Article
description BACKGROUND: Increases in ocean temperatures and in the frequency and severity of hypoxic events are expected with climate change, and may become a challenge for cultured Atlantic salmon and negatively affect their growth, immunology and welfare. Thus, we examined how an incremental temperature increase alone (Warm & Normoxic-WN: 12 → 20 °C; 1 °C week(− 1)), and in combination with moderate hypoxia (Warm & Hypoxic-WH: ~ 70% air saturation), impacted the salmon’s hepatic transcriptome expr\ession compared to control fish (CT: 12 °C, normoxic) using 44 K microarrays and qPCR. RESULTS: Overall, we identified 2894 differentially expressed probes (DEPs, FDR < 5%), that included 1111 shared DEPs, while 789 and 994 DEPs were specific to WN and WH fish, respectively. Pathway analysis indicated that the cellular mechanisms affected by the two experimental conditions were quite similar, with up-regulated genes functionally associated with the heat shock response, ER-stress, apoptosis and immune defence, while genes connected with general metabolic processes, proteolysis and oxidation-reduction were largely suppressed. The qPCR assessment of 41 microarray-identified genes validated that the heat shock response (hsp90aa1, serpinh1), apoptosis (casp8, jund, jak2) and immune responses (apod, c1ql2, epx) were up-regulated in WN and WH fish, while oxidative stress and hypoxia sensitive genes were down-regulated (cirbp, cyp1a1, egln2, gstt1, hif1α, prdx6, rraga, ucp2). However, the additional challenge of hypoxia resulted in more pronounced effects on heat shock and immune-related processes, including a stronger influence on the expression of 14 immune-related genes. Finally, robust correlations between the transcription of 19 genes and several phenotypic traits in WH fish suggest that changes in gene expression were related to impaired physiological and growth performance. CONCLUSION: Increasing temperature to 20 °C alone, and in combination with hypoxia, resulted in the differential expression of genes involved in ...
format Text
author Beemelmanns, Anne
Zanuzzo, Fábio S.
Xue, Xi
Sandrelli, Rebeccah M.
Rise, Matthew L.
Gamperl, A. Kurt
author_facet Beemelmanns, Anne
Zanuzzo, Fábio S.
Xue, Xi
Sandrelli, Rebeccah M.
Rise, Matthew L.
Gamperl, A. Kurt
author_sort Beemelmanns, Anne
title The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
title_short The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
title_full The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
title_fullStr The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
title_full_unstemmed The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
title_sort transcriptomic responses of atlantic salmon (salmo salar) to high temperature stress alone, and in combination with moderate hypoxia
publisher BioMed Central
publishDate 2021
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042886/
http://www.ncbi.nlm.nih.gov/pubmed/33845767
https://doi.org/10.1186/s12864-021-07464-x
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source BMC Genomics
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8042886/
http://www.ncbi.nlm.nih.gov/pubmed/33845767
http://dx.doi.org/10.1186/s12864-021-07464-x
op_rights © The Author(s) 2021
https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
op_rightsnorm CC0
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