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...
Published in: | Epigenetics |
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Language: | English |
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Taylor & Francis: STM, Behavioural Science and Public Health Titles
2018
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Online Access: | https://orca.cardiff.ac.uk/id/eprint/117116/ https://doi.org/10.1080/15592294.2018.1554520 https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf |
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ftunivcardiff:oai:https://orca.cardiff.ac.uk:117116 2023-05-15T15:31:46+02:00 Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon Uren Webster, Tamsyn Rodriguez-Barreto, Deiene Martin, Samuel Van Oosterhout, Cock Orozco Ter Wengel, Pablo Cable, Joanne Hamilton, Alistair Garcia de Leaniz, Carlos Conseuegra, Sofia 2018-12-13 application/pdf https://orca.cardiff.ac.uk/id/eprint/117116/ https://doi.org/10.1080/15592294.2018.1554520 https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf en eng Taylor & Francis: STM, Behavioural Science and Public Health Titles https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf Uren Webster, Tamsyn, Rodriguez-Barreto, Deiene, Martin, Samuel, Van Oosterhout, Cock, Orozco Ter Wengel, Pablo https://orca.cardiff.ac.uk/view/cardiffauthors/A337280B.html orcid:0000-0002-7951-4148 orcid:0000-0002-7951-4148, Cable, Joanne https://orca.cardiff.ac.uk/view/cardiffauthors/A042952A.html orcid:0000-0002-8510-7055 orcid:0000-0002-8510-7055, Hamilton, Alistair, Garcia de Leaniz, Carlos and Conseuegra, 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. 10.1080/15592294.2018.1554520 https://doi.org/10.1080/15592294.2018.1554520 file https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf doi:10.1080/15592294.2018.1554520 Article PeerReviewed 2018 ftunivcardiff https://doi.org/10.1080/15592294.2018.1554520 2022-10-27T22:45:56Z 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 Cardiff University: ORCA (Online Research @ Cardiff) Epigenetics 13 12 1191 1207 |
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Cardiff University: ORCA (Online Research @ Cardiff) |
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ftunivcardiff |
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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 Rodriguez-Barreto, Deiene Martin, Samuel Van Oosterhout, Cock Orozco Ter Wengel, Pablo Cable, Joanne Hamilton, Alistair Garcia de Leaniz, Carlos Conseuegra, Sofia |
spellingShingle |
Uren Webster, Tamsyn Rodriguez-Barreto, Deiene Martin, Samuel Van Oosterhout, Cock Orozco Ter Wengel, Pablo Cable, Joanne Hamilton, Alistair Garcia de Leaniz, Carlos Conseuegra, Sofia Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon |
author_facet |
Uren Webster, Tamsyn Rodriguez-Barreto, Deiene Martin, Samuel Van Oosterhout, Cock Orozco Ter Wengel, Pablo Cable, Joanne Hamilton, Alistair Garcia de Leaniz, Carlos Conseuegra, Sofia |
author_sort |
Uren Webster, Tamsyn |
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: STM, Behavioural Science and Public Health Titles |
publishDate |
2018 |
url |
https://orca.cardiff.ac.uk/id/eprint/117116/ https://doi.org/10.1080/15592294.2018.1554520 https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_relation |
https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf Uren Webster, Tamsyn, Rodriguez-Barreto, Deiene, Martin, Samuel, Van Oosterhout, Cock, Orozco Ter Wengel, Pablo https://orca.cardiff.ac.uk/view/cardiffauthors/A337280B.html orcid:0000-0002-7951-4148 orcid:0000-0002-7951-4148, Cable, Joanne https://orca.cardiff.ac.uk/view/cardiffauthors/A042952A.html orcid:0000-0002-8510-7055 orcid:0000-0002-8510-7055, Hamilton, Alistair, Garcia de Leaniz, Carlos and Conseuegra, 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. 10.1080/15592294.2018.1554520 https://doi.org/10.1080/15592294.2018.1554520 file https://orca.cardiff.ac.uk/id/eprint/117116/1/Uren_Webster_et_al_revised_manuscript.pdf doi:10.1080/15592294.2018.1554520 |
op_doi |
https://doi.org/10.1080/15592294.2018.1554520 |
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Epigenetics |
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12 |
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1207 |
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