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: Article in Journal/Newspaper
Language:English
Published: 2018
Subjects:
Online Access:https://ueaeprints.uea.ac.uk/id/eprint/69596/
https://ueaeprints.uea.ac.uk/id/eprint/69596/1/Epigenetics_UrenWebster_2018.pdf
https://doi.org/10.1080/15592294.2018.1554520
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spelling ftuniveastangl:oai:ueaeprints.uea.ac.uk:69596 2023-05-15T15:31:47+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 application/pdf https://ueaeprints.uea.ac.uk/id/eprint/69596/ https://ueaeprints.uea.ac.uk/id/eprint/69596/1/Epigenetics_UrenWebster_2018.pdf https://doi.org/10.1080/15592294.2018.1554520 en eng https://ueaeprints.uea.ac.uk/id/eprint/69596/1/Epigenetics_UrenWebster_2018.pdf 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 and Consuegra, Sofia (2018) Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. Epigenetics, 13 (12). pp. 1191-1207. ISSN 1559-2294 doi:10.1080/15592294.2018.1554520 cc_by CC-BY Article PeerReviewed 2018 ftuniveastangl https://doi.org/10.1080/15592294.2018.1554520 2023-01-30T21:49:37Z 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. Article in Journal/Newspaper Atlantic salmon Salmo salar University of East Anglia: UEA Digital Repository Epigenetics 13 12 1191 1207
institution Open Polar
collection University of East Anglia: UEA Digital Repository
op_collection_id ftuniveastangl
language English
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 Article in Journal/Newspaper
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
spellingShingle 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
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
publishDate 2018
url https://ueaeprints.uea.ac.uk/id/eprint/69596/
https://ueaeprints.uea.ac.uk/id/eprint/69596/1/Epigenetics_UrenWebster_2018.pdf
https://doi.org/10.1080/15592294.2018.1554520
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation https://ueaeprints.uea.ac.uk/id/eprint/69596/1/Epigenetics_UrenWebster_2018.pdf
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 and Consuegra, Sofia (2018) Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. Epigenetics, 13 (12). pp. 1191-1207. ISSN 1559-2294
doi:10.1080/15592294.2018.1554520
op_rights cc_by
op_rightsnorm CC-BY
op_doi https://doi.org/10.1080/15592294.2018.1554520
container_title Epigenetics
container_volume 13
container_issue 12
container_start_page 1191
op_container_end_page 1207
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