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

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.

SUBMITTER: Uren Webster TM

PROVIDER: S-EPMC6986783 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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

Uren Webster Tamsyn M TM Rodriguez-Barreto Deiene D Martin Samuel A M SAM Van Oosterhout Cock C Orozco-terWengel Pablo P Cable Joanne J Hamilton Alastair A Garcia De Leaniz Carlos C Consuegra Sofia S

Epigenetics 20181213 12

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 ex ...[more]

PMID: 30526303

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Project description:BackgroundThe immune response is an energy demanding process, which has effects in many physiological pathways in the body including protein and lipid metabolism. During an inflammatory response the liver is required to produce high levels of acute phase response proteins that attempt to neutralise an invading pathogen. Although this has been extensively studied in both mammals and fish, little is known about how high and low energy reserves modulate the response to an infection in fish which are ectothermic vertebrates. Food withdrawal in fish causes a decrease in metabolic rate so as to preserve protein and lipid energy reserves, which occurs naturally during the life cycle of many salmonids. Here we investigated how the feeding or fasting of Atlantic salmon affected the transcriptional response in the liver to an acute bacterial infection.ResultsTotal liver RNA was extracted from four different groups of salmon. Two groups were fed or starved for 28 days. One of each of the fed or starved groups was then exposed to an acute bacterial infection. Twenty four hours later (day 29) the livers were isolated from all fish for RNA extraction. The transcriptional changes were examined by micro array analysis using a 17 K Atlantic salmon cDNA microarray. The expression profiling results showed major changes in gene transcription in each of the groups. Enrichment for particular biological pathways was examined by analysis of gene ontology. Those fish that were starved decreased immune gene transcription and reduced production of plasma protein genes, and upon infection there was a further decrease in genes encoding plasma proteins but a large increase in acute phase response proteins. The latter was greater in magnitude than in the fish that had been fed prior to infection. The expression of several genes that were found altered during microarray analysis was confirmed by real time PCR.ConclusionsWe demonstrate that both starvation and infection have profound effects on transcription in the liver of salmon. There was a significant effect on the transcriptional response to infection depending on the prior feeding regime of the fish. It is likely that the energy demands on protein synthesis for acute phase response proteins are relatively high in the starved fish which have reduced energy reserves. This has implications for dietary control of fish if an immune response is anticipated.

Project description:BACKGROUND: Cardiomyopathy syndrome (CMS) is a disease associated with severe myocarditis primarily in adult farmed Atlantic salmon (Salmo salar L.), caused by a double-stranded RNA virus named piscine myocarditis virus (PMCV) with structural similarities to the Totiviridae family. Here we present the first characterisation of host immune responses to CMS assessed by microarray transcriptome profiling. RESULTS: Unvaccinated farmed Atlantic salmon post-smolts were infected by intraperitoneal injection of PMCV and developed cardiac pathology consistent with CMS. From analysis of heart samples at several time points and different tissues at early and clinical stages by oligonucleotide microarrays (SIQ2.0 chip), six gene sets representing a broad range of immune responses were identified, showing significant temporal and spatial regulation. Histopathological examination of cardiac tissue showed myocardial lesions from 6 weeks post infection (wpi) that peaked at 8-9 wpi and was followed by a recovery. Viral RNA was detected in all organs from 4 wpi suggesting a broad tissue tropism. High correlation between viral load and cardiac histopathology score suggested that cytopathic effect of infection was a major determinant of the myocardial changes. Strong and systemic induction of antiviral and IFN-dependent genes from 2 wpi that levelled off during infection, was followed by a biphasic activation of pathways for B cells and MHC antigen presentation, both peaking at clinical pathology. This was preceded by a distinct cardiac activation of complement at 6 wpi, suggesting a complement-dependent activation of humoral Ab-responses. Peak of cardiac pathology and viral load coincided with cardiac-specific upregulation of T cell response genes and splenic induction of complement genes. Preceding the reduction in viral load and pathology, these responses were probably important for viral clearance and recovery. CONCLUSIONS: By comparative analysis of gene expression, histology and viral load, the temporal and spatial regulation of immune responses were characterised and novel immune genes identified, ultimately leading to a more complete understanding of host-virus responses and pathology and protection in Atlantic salmon during CMS.

Project description:Non-native species may be introduced either intentionally or unintentionally, and their impact can range from benign to highly disruptive. Non-native salmonids were introduced into Lake Ontario, Canada, to provide recreational fishing opportunities; however, the establishment of those species has been proposed as a significant barrier to the reintroduction of native Atlantic salmon (Salmo salar) due to intense interspecific competition. In this study, we compared population differences of Atlantic salmon in transcriptome response to interspecific competition. We reared Atlantic salmon from two populations (LaHave River and Sebago Lake) with fish of each of three non-native salmonids (Chinook salmon Oncorhynchus tshawytscha, rainbow trout O. mykiss, and brown trout S. trutta) in artificial streams. We used RNA-seq to assess transcriptome differences between the Atlantic salmon populations and the responses of these populations to the interspecific competition treatments after 10 months of competition in the stream tanks. We found that population differences in gene expression were generally greater than the effects of interspecific competition. Interestingly, we found that the two Atlantic salmon populations exhibited similar responses to interspecific competition based on functional gene ontologies, but the specific genes within those ontologies were different. Our transcriptome analyses suggest that the most stressful competitor (as measured by the highest number of differentially expressed genes) differs between the two study populations. Our transcriptome characterization highlights the importance of source population selection for conservation applications, as organisms with different evolutionary histories can possess different transcriptional responses to the same biotic stressors. The results also indicate that generalized predictions of the response of native species to interactions with introduced species may not be appropriate without incorporating potential population-specific response to introduced species.

Dataset Information

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

Publications

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

Similar Datasets

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