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...

Full description

Bibliographic Details
Main Authors: Tamsyn M. Uren Webster, Deiene Rodriguez-Barreto, Martin, Samuel A.M., Oosterhout, Cock Van, Orozco-TerWengel, Pablo, Cable, Joanne, Hamilton, Alastair, Leaniz, Carlos Garcia De, Consuegra, Sofia
Format: Article in Journal/Newspaper
Language:unknown
Published: Taylor & Francis 2018
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.7448834.v1
https://tandf.figshare.com/articles/Contrasting_effects_of_acute_and_chronic_stress_on_the_transcriptome_epigenome_and_immune_response_of_Atlantic_salmon/7448834/1
id ftdatacite:10.6084/m9.figshare.7448834.v1
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.7448834.v1 2023-05-15T15:31:54+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 Martin, Samuel A.M. Oosterhout, Cock Van Orozco-TerWengel, Pablo Cable, Joanne Hamilton, Alastair Leaniz, Carlos Garcia De Consuegra, Sofia 2018 https://dx.doi.org/10.6084/m9.figshare.7448834.v1 https://tandf.figshare.com/articles/Contrasting_effects_of_acute_and_chronic_stress_on_the_transcriptome_epigenome_and_immune_response_of_Atlantic_salmon/7448834/1 unknown Taylor & Francis https://dx.doi.org/10.1080/15592294.2018.1554520 https://dx.doi.org/10.6084/m9.figshare.7448834 Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode cc-by-4.0 CC-BY Genetics FOS Biological sciences Molecular Biology Immunology FOS Clinical medicine 69999 Biological Sciences not elsewhere classified Science Policy 111714 Mental Health FOS Health sciences Other CreativeWork Online resource article 2018 ftdatacite https://doi.org/10.6084/m9.figshare.7448834.v1 https://doi.org/10.1080/15592294.2018.1554520 https://doi.org/10.6084/m9.figshare.7448834 2021-11-05T12:55:41Z 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 DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Genetics
FOS Biological sciences
Molecular Biology
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Science Policy
111714 Mental Health
FOS Health sciences
spellingShingle Genetics
FOS Biological sciences
Molecular Biology
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Science Policy
111714 Mental Health
FOS Health sciences
Tamsyn M. Uren Webster
Deiene Rodriguez-Barreto
Martin, Samuel A.M.
Oosterhout, Cock Van
Orozco-TerWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Leaniz, Carlos Garcia De
Consuegra, Sofia
Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
topic_facet Genetics
FOS Biological sciences
Molecular Biology
Immunology
FOS Clinical medicine
69999 Biological Sciences not elsewhere classified
Science Policy
111714 Mental Health
FOS Health sciences
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
Martin, Samuel A.M.
Oosterhout, Cock Van
Orozco-TerWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Leaniz, Carlos Garcia De
Consuegra, Sofia
author_facet Tamsyn M. Uren Webster
Deiene Rodriguez-Barreto
Martin, Samuel A.M.
Oosterhout, Cock Van
Orozco-TerWengel, Pablo
Cable, Joanne
Hamilton, Alastair
Leaniz, Carlos Garcia De
Consuegra, Sofia
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
publishDate 2018
url https://dx.doi.org/10.6084/m9.figshare.7448834.v1
https://tandf.figshare.com/articles/Contrasting_effects_of_acute_and_chronic_stress_on_the_transcriptome_epigenome_and_immune_response_of_Atlantic_salmon/7448834/1
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation https://dx.doi.org/10.1080/15592294.2018.1554520
https://dx.doi.org/10.6084/m9.figshare.7448834
op_rights Creative Commons Attribution 4.0 International
https://creativecommons.org/licenses/by/4.0/legalcode
cc-by-4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.7448834.v1
https://doi.org/10.1080/15592294.2018.1554520
https://doi.org/10.6084/m9.figshare.7448834
_version_ 1766362397544546304