Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and on immune response to a pathogen challenge in Atlantic salmon

Exposure to environmental stress during early life may have long lasting effects on immunity and disease resistance, with health outcomes dependent on the nature of the stressor. Evidence from mammalian systems suggests that epigenetic modifications may play a role in mediating these lasting effects of stress. However, the effects of early-life stress on the immune system of non-model organisms, and the underlying molecular mechanisms, are largely unknown. We examined the effects of an acute stress (temperature shock during late embryogenesis) and a chronic stress (absence of tank enrichment/cover during larval stage) on the gill transcriptome and methylome four months later, in Atlantic salmon. We found that acute stress had a limited lasting impact on the gill transcriptome, but that chronic stress was associated with pronounced differences in transcription. However, both acute and chronic stress caused lasting, and contrasting, changes in the gill methylome, and we identified a small proportion of genes for which stress-induced changes in promoter methylation may be linked to differences in expression. We also examined transcriptional response to a model pathogenic challenge (lipopolysaccharide, LPS) and found that acute and chronic stress enhanced and suppressed inflammatory immune responses, respectively. We discuss the potential for the observed stress-induced changes in baseline promoter methylation to contribute to an alteration in transcriptional response to pathogen exposure, on a gene-specific basis. Functional analysis revealed that early life stress may also alter the wider epigenetic regulation of a number of cellular signalling pathways involved in immune response to pathogen exposure.