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Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon

Tamsyn Uren Webster Orcid Logo, Deiene Rodriguez-Barreto, Samuel A.M. Martin, Cock Van Oosterhout, Pablo Orozco-terWengel, Joanne Cable, Alastair Hamilton, Carlos Garcia De Leaniz Orcid Logo, Sofia Consuegra, Sofia Consuegra del Olmo Orcid Logo

Epigenetics, Pages: 1 - 17

Swansea University Authors: Tamsyn Uren Webster Orcid Logo, Carlos Garcia De Leaniz Orcid Logo, Sofia Consuegra del Olmo Orcid Logo

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DOI (Published version): 10.1080/15592294.2018.1554520

Abstract

Stress experienced during early life may have lasting effects on the immune system. 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 epige...

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Published in: Epigenetics
ISSN: 1559-2294 1559-2308
Published: 2018
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URI: https://cronfa.swan.ac.uk/Record/cronfa46218
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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. 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spelling 2022-12-05T16:04:56.5821008 v2 46218 2018-12-04 Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon 3ea91c154926c86f89ea6a761122ecf6 0000-0002-0072-9745 Tamsyn Uren Webster Tamsyn Uren Webster true false 1c70acd0fd64edb0856b7cf34393ab02 0000-0003-1650-2729 Carlos Garcia De Leaniz Carlos Garcia De Leaniz true false 241f2810ab8f56be53ca8af23e384c6e 0000-0003-4403-2509 Sofia Consuegra del Olmo Sofia Consuegra del Olmo true false 2018-12-04 SBI Stress experienced during early life may have lasting effects on the immune system. 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. Journal Article Epigenetics 1 17 1559-2294 1559-2308 31 12 2018 2018-12-31 10.1080/15592294.2018.1554520 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University BBSRC; NERC 2022-12-05T16:04:56.5821008 2018-12-04T16:29:53.2176275 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Tamsyn Uren Webster 0000-0002-0072-9745 1 Deiene Rodriguez-Barreto 2 Samuel A.M. Martin 3 Cock Van Oosterhout 4 Pablo Orozco-terWengel 5 Joanne Cable 6 Alastair Hamilton 7 Carlos Garcia De Leaniz 0000-0003-1650-2729 8 Sofia Consuegra 9 Sofia Consuegra del Olmo 0000-0003-4403-2509 10 0046218-17122018150541.pdf UrenWebsteretal2018.pdf 2018-12-17T15:05:41.8730000 Output 3348683 application/pdf Corrected Version of Record true 2018-12-17T00:00:00.0000000 Released under the terms of a Creative Commons Attribution License (CC-BY). true eng
title Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
spellingShingle Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon
Tamsyn Uren Webster
Carlos Garcia De Leaniz
Sofia Consuegra del Olmo
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
author_id_str_mv 3ea91c154926c86f89ea6a761122ecf6
1c70acd0fd64edb0856b7cf34393ab02
241f2810ab8f56be53ca8af23e384c6e
author_id_fullname_str_mv 3ea91c154926c86f89ea6a761122ecf6_***_Tamsyn Uren Webster
1c70acd0fd64edb0856b7cf34393ab02_***_Carlos Garcia De Leaniz
241f2810ab8f56be53ca8af23e384c6e_***_Sofia Consuegra del Olmo
author Tamsyn Uren Webster
Carlos Garcia De Leaniz
Sofia Consuegra del Olmo
author2 Tamsyn 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
Sofia Consuegra del Olmo
format Journal article
container_title Epigenetics
container_start_page 1
publishDate 2018
institution Swansea University
issn 1559-2294
1559-2308
doi_str_mv 10.1080/15592294.2018.1554520
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
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description Stress experienced during early life may have lasting effects on the immune system. 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.
published_date 2018-12-31T03:57:58Z
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score 11.037319

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