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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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 |
_version_ |
1779313005950926848 |