Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon

Stress experienced during early life may have lasting effects on the immune system, with impacts on health and disease dependent on the nature and duration of the stressor. The epigenome is especially sensitive to environmental stimuli during early life and represents a potential mechanism through w...

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Published in:Epigenetics
Main Authors: Uren Webster, Tamsyn M., Rodriguez-Barreto, Deiene, Martin, Samuel A.M., Van Oosterhout, Cock, Orozco-terWengel, Pablo, Cable, Joanne, Hamilton, Alastair, Garcia De Leaniz, Carlos, Consuegra, Sofia
Format: Text
Language:English
Published: Taylor & Francis 2018
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986783/
http://www.ncbi.nlm.nih.gov/pubmed/30526303
https://doi.org/10.1080/15592294.2018.1554520
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spelling ftpubmed:oai:pubmedcentral.nih.gov:6986783 2023-05-15T15:31:44+02:00 Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon Uren Webster, Tamsyn M. Rodriguez-Barreto, Deiene Martin, Samuel A.M. Van Oosterhout, Cock Orozco-terWengel, Pablo Cable, Joanne Hamilton, Alastair Garcia De Leaniz, Carlos Consuegra, Sofia 2018-12-13 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986783/ http://www.ncbi.nlm.nih.gov/pubmed/30526303 https://doi.org/10.1080/15592294.2018.1554520 en eng Taylor & Francis http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986783/ http://www.ncbi.nlm.nih.gov/pubmed/30526303 http://dx.doi.org/10.1080/15592294.2018.1554520 © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. CC-BY Research Paper Text 2018 ftpubmed https://doi.org/10.1080/15592294.2018.1554520 2020-02-16T01:18:34Z Stress experienced during early life may have lasting effects on the immune system, with impacts on health and disease dependent on the nature and duration of the stressor. The epigenome is especially sensitive to environmental stimuli during early life and represents a potential mechanism through which stress may cause long-lasting health effects. However, the extent to which the epigenome responds differently to chronic vs acute stressors is unclear, especially for non-mammalian species. We examined the effects of acute stress (cold-shock during embryogenesis) and chronic stress (absence of tank enrichment during larval-stage) on global gene expression (using RNA-seq) and DNA methylation (using RRBS) in the gills of Atlantic salmon (Salmo salar) four months after hatching. Chronic stress induced pronounced transcriptional differences, while acute stress caused few lasting transcriptional effects. However, both acute and chronic stress caused lasting and contrasting changes in the methylome. Crucially, we found that acute stress enhanced transcriptional immune response to a pathogenic challenge (bacterial lipopolysaccharide, LPS), while chronic stress suppressed it. We identified stress-induced changes in promoter and gene-body methylation that were associated with altered expression for a small proportion of immune-related genes, and evidence of wider epigenetic regulation within signalling pathways involved in immune response. Our results suggest that stress can affect immuno-competence through epigenetic mechanisms, and highlight the markedly different effects of chronic larval and acute embryonic stress. This knowledge could be used to harness the stimulatory effects of acute stress on immunity, paving the way for improved stress and disease management through epigenetic conditioning. Text Atlantic salmon Salmo salar PubMed Central (PMC) Epigenetics 13 12 1191 1207
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Paper
spellingShingle Research Paper
Uren Webster, Tamsyn M.
Rodriguez-Barreto, Deiene
Martin, Samuel A.M.
Van Oosterhout, Cock
Orozco-terWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Garcia De Leaniz, Carlos
Consuegra, Sofia
Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
topic_facet Research Paper
description Stress experienced during early life may have lasting effects on the immune system, with impacts on health and disease dependent on the nature and duration of the stressor. The epigenome is especially sensitive to environmental stimuli during early life and represents a potential mechanism through which stress may cause long-lasting health effects. However, the extent to which the epigenome responds differently to chronic vs acute stressors is unclear, especially for non-mammalian species. We examined the effects of acute stress (cold-shock during embryogenesis) and chronic stress (absence of tank enrichment during larval-stage) on global gene expression (using RNA-seq) and DNA methylation (using RRBS) in the gills of Atlantic salmon (Salmo salar) four months after hatching. Chronic stress induced pronounced transcriptional differences, while acute stress caused few lasting transcriptional effects. However, both acute and chronic stress caused lasting and contrasting changes in the methylome. Crucially, we found that acute stress enhanced transcriptional immune response to a pathogenic challenge (bacterial lipopolysaccharide, LPS), while chronic stress suppressed it. We identified stress-induced changes in promoter and gene-body methylation that were associated with altered expression for a small proportion of immune-related genes, and evidence of wider epigenetic regulation within signalling pathways involved in immune response. Our results suggest that stress can affect immuno-competence through epigenetic mechanisms, and highlight the markedly different effects of chronic larval and acute embryonic stress. This knowledge could be used to harness the stimulatory effects of acute stress on immunity, paving the way for improved stress and disease management through epigenetic conditioning.
format Text
author Uren Webster, Tamsyn M.
Rodriguez-Barreto, Deiene
Martin, Samuel A.M.
Van Oosterhout, Cock
Orozco-terWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Garcia De Leaniz, Carlos
Consuegra, Sofia
author_facet Uren Webster, Tamsyn M.
Rodriguez-Barreto, Deiene
Martin, Samuel A.M.
Van Oosterhout, Cock
Orozco-terWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Garcia De Leaniz, Carlos
Consuegra, Sofia
author_sort Uren Webster, Tamsyn M.
title Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
title_short Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
title_full Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
title_fullStr Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
title_full_unstemmed Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
title_sort contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of atlantic salmon
publisher Taylor & Francis
publishDate 2018
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986783/
http://www.ncbi.nlm.nih.gov/pubmed/30526303
https://doi.org/10.1080/15592294.2018.1554520
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986783/
http://www.ncbi.nlm.nih.gov/pubmed/30526303
http://dx.doi.org/10.1080/15592294.2018.1554520
op_rights © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
http://creativecommons.org/licenses/by/4.0/
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1080/15592294.2018.1554520
container_title Epigenetics
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