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

Tamsyn M. Uren Webster (Corresponding Author), Deiene Rodriguez-Barreto, Samuel A. M. Martin, Cock van Oosterhout, Pablo Orozco-terWengel, Joanne Cable, Alastair Hamilton, Carlos Garcia de Leaniz, Sofia Consuegra

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

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.
Original languageEnglish
Pages (from-to)1191-1207
Number of pages17
JournalEpigenetics
Volume13
Issue number12
Early online date13 Dec 2018
DOIs
Publication statusPublished - 2018

Fingerprint

Salmo salar
Transcriptome
Epigenomics
Health
DNA Methylation
Disease Management
Mental Competency
Methylation
Genes
Embryonic Development
Lipopolysaccharides
Immune System
Immunity
Shock
RNA
Gene Expression

Keywords

  • DNA Methylation
  • RRBS
  • transcription
  • rna-seq
  • aquaculture
  • stress
  • early life
  • immune response
  • pathogen

Cite this

Uren Webster, T. M., Rodriguez-Barreto, D., Martin, S. A. M., van Oosterhout, C., Orozco-terWengel, P., Cable, J., ... Consuegra, S. (2018). Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. Epigenetics, 13(12), 1191-1207. https://doi.org/10.1080/15592294.2018.1554520

Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. / Uren Webster, Tamsyn M. (Corresponding Author); Rodriguez-Barreto, Deiene; Martin, Samuel A. M.; van Oosterhout, Cock; Orozco-terWengel, Pablo; Cable, Joanne; Hamilton, Alastair; Garcia de Leaniz, Carlos; Consuegra, Sofia.

In: Epigenetics, Vol. 13, No. 12, 2018, p. 1191-1207.

Research output: Contribution to journalArticle

Uren Webster, TM, Rodriguez-Barreto, D, Martin, SAM, van Oosterhout, C, Orozco-terWengel, P, Cable, J, Hamilton, A, Garcia de Leaniz, C & Consuegra, S 2018, 'Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon' Epigenetics, vol. 13, no. 12, pp. 1191-1207. https://doi.org/10.1080/15592294.2018.1554520
Uren Webster, Tamsyn M. ; Rodriguez-Barreto, Deiene ; Martin, Samuel A. M. ; van Oosterhout, Cock ; Orozco-terWengel, Pablo ; Cable, Joanne ; Hamilton, Alastair ; Garcia de Leaniz, Carlos ; Consuegra, Sofia. / Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. In: Epigenetics. 2018 ; Vol. 13, No. 12. pp. 1191-1207.
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abstract = "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.",
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N1 - Acknowledgements We are grateful to Sam Fieldwick for assistance with sampling and Dr Angela Marchbank at the Cardiff Genomics Research Hub for facilitating the RRBS sequencing. Funding details This work was funded by a BBSRC-NERC Aquaculture grant (BB/M026469/1) to CGL and by the Welsh Government and Higher Education Funding Council for Wales (HEFCW) through the Sêr Cymru National Research Network for Low Carbon Energy and Environment (NRN-LCEE) to SC.

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N2 - 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.

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