Abstract
ABSTRACTStress 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.
Highlights
The stress response is a fundamental survival mechanism that provides a critical adaptive response to many environmental challenges, but may compromise the immune system [1,2]
There was a significant effect of treatment on growth rate during pre- and early-feeding (748 and 1019 degree days (DD)), whereby fish exposed to chronic stress initially lost weight while those in the control and acute stress groups did not, but this difference in size was no longer apparent at later sampling points (492 DD: F3,114 = 0.37, P = 0.718; 748 DD: F3,114 = 15.82, P = 0.025; 1019 DD: F3,114 = 15.42, P = 0.026; 1323 DD: F3,114 = 1.63, P = 0.330, 1532 DD: F3,114 = 4.78, P = 0.117; Table S1)
We found that acute stress applied during embryogenesis and chronic stress experienced during larval development induced contrasting effects on gill transcription and immune response in Atlantic salmon
Summary
The stress response is a fundamental survival mechanism that provides a critical adaptive response to many environmental challenges, but may compromise the immune system [1,2]. The precise impacts of environmental stress on immune function often depend on the timing, duration, magnitude, and nature of the stressor [3]. Acute stressors, lasting for minutes to hours, are less likely to impair immune function, and may even enhance immune response by stimulating the maturation, secretion and redistribution of immune cells and cytokines [5]. Early life stages may be sensitive to environmental stress due to developmental plasticity during critical periods of differentiation and maturation of the nervous and immune systems [6]. It is well established that early-life stress can have longlasting adverse effects on health and disease susceptibility. Maternal stress during pregnancy predisposes the offspring to developmental, immunological and behavioural
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