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: Tamsyn M. Uren Webster, Deiene Rodriguez-Barreto, Samuel A.M. Martin, Cock Van Oosterhout, Pablo Orozco-terWengel, Joanne Cable, Alastair Hamilton, Carlos Garcia De Leaniz, Sofia Consuegra
Format: Article in Journal/Newspaper
Language:English
Published: Taylor & Francis Group 2018
Subjects:
Online Access:https://doi.org/10.1080/15592294.2018.1554520
https://doaj.org/article/f8542576ebd04e1ba996c3112b8b71dd
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spelling ftdoajarticles:oai:doaj.org/article:f8542576ebd04e1ba996c3112b8b71dd 2023-10-09T21:49:57+02:00 Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon Tamsyn M. Uren Webster Deiene Rodriguez-Barreto Samuel A.M. Martin Cock Van Oosterhout Pablo Orozco-terWengel Joanne Cable Alastair Hamilton Carlos Garcia De Leaniz Sofia Consuegra 2018-12-01T00:00:00Z https://doi.org/10.1080/15592294.2018.1554520 https://doaj.org/article/f8542576ebd04e1ba996c3112b8b71dd EN eng Taylor & Francis Group http://dx.doi.org/10.1080/15592294.2018.1554520 https://doaj.org/toc/1559-2294 https://doaj.org/toc/1559-2308 1559-2294 1559-2308 doi:10.1080/15592294.2018.1554520 https://doaj.org/article/f8542576ebd04e1ba996c3112b8b71dd Epigenetics, Vol 13, Iss 12, Pp 1191-1207 (2018) dna methylation rrbs transcriptomics rna-seq aquaculture stress early life immune response pathogen Genetics QH426-470 article 2018 ftdoajarticles https://doi.org/10.1080/15592294.2018.1554520 2023-09-24T00:36:43Z 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 Directory of Open Access Journals: DOAJ Articles Epigenetics 13 12 1191 1207
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic dna methylation
rrbs
transcriptomics
rna-seq
aquaculture
stress
early life
immune response
pathogen
Genetics
QH426-470
spellingShingle dna methylation
rrbs
transcriptomics
rna-seq
aquaculture
stress
early life
immune response
pathogen
Genetics
QH426-470
Tamsyn M. Uren Webster
Deiene Rodriguez-Barreto
Samuel A.M. Martin
Cock Van Oosterhout
Pablo Orozco-terWengel
Joanne Cable
Alastair Hamilton
Carlos Garcia De Leaniz
Sofia Consuegra
Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
topic_facet dna methylation
rrbs
transcriptomics
rna-seq
aquaculture
stress
early life
immune response
pathogen
Genetics
QH426-470
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 Tamsyn M. Uren Webster
Deiene Rodriguez-Barreto
Samuel A.M. Martin
Cock Van Oosterhout
Pablo Orozco-terWengel
Joanne Cable
Alastair Hamilton
Carlos Garcia De Leaniz
Sofia Consuegra
author_facet Tamsyn M. Uren Webster
Deiene Rodriguez-Barreto
Samuel A.M. Martin
Cock Van Oosterhout
Pablo Orozco-terWengel
Joanne Cable
Alastair Hamilton
Carlos Garcia De Leaniz
Sofia Consuegra
author_sort Tamsyn M. Uren Webster
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 Group
publishDate 2018
url https://doi.org/10.1080/15592294.2018.1554520
https://doaj.org/article/f8542576ebd04e1ba996c3112b8b71dd
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Epigenetics, Vol 13, Iss 12, Pp 1191-1207 (2018)
op_relation http://dx.doi.org/10.1080/15592294.2018.1554520
https://doaj.org/toc/1559-2294
https://doaj.org/toc/1559-2308
1559-2294
1559-2308
doi:10.1080/15592294.2018.1554520
https://doaj.org/article/f8542576ebd04e1ba996c3112b8b71dd
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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