Abstract
BackgroundFishes show seasonal patterns of immunity, but such phenomena are imperfectly understood in vertebrates generally, even in humans and mice. As these seasonal patterns may link to infectious disease risk and individual condition, the nature of their control has real practical implications. Here we characterize seasonal dynamics in the expression of conserved vertebrate immunity genes in a naturally-occurring piscine model, the three-spined stickleback.ResultsWe made genome-wide measurements (RNAseq) of whole-fish mRNA pools (n = 36) at the end of summer and winter in contrasting habitats (riverine and lacustrine) and focussed on common trends to filter habitat-specific from overarching temporal responses. We corroborated this analysis with targeted year-round whole-fish gene expression (Q-PCR) studies in a different year (n = 478). We also considered seasonal tissue-specific expression (6 tissues) (n = 15) at a third contrasting (euryhaline) locality by Q-PCR, further validating the generality of the patterns seen in whole fish analyses. Extremes of season were the dominant predictor of immune expression (compared to sex, ontogeny or habitat). Signatures of adaptive immunity were elevated in late summer. In contrast, late winter was accompanied by signatures of innate immunity (including IL-1 signalling and non-classical complement activity) and modulated toll-like receptor signalling. Negative regulators of T-cell activity were prominent amongst winter-biased genes, suggesting that adaptive immunity is actively down-regulated during winter rather than passively tracking ambient temperature. Network analyses identified a small set of immune genes that might lie close to a regulatory axis. These genes acted as hubs linking summer-biased adaptive pathways, winter-biased innate pathways and other organismal processes, including growth, metabolic dynamics and responses to stress and temperature. Seasonal change was most pronounced in the gill, which contains a considerable concentration of T-cell activity in the stickleback.ConclusionsOur results suggest major and predictable seasonal re-adjustments of immunity. Further consideration should be given to the effects of such responses in seasonally-occurring disease.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2701-7) contains supplementary material, which is available to authorized users.
Highlights
Fishes show seasonal patterns of immunity, but such phenomena are imperfectly understood in vertebrates generally, even in humans and mice
Seasonal expression bias of immune system genes occurs against a well-defined genome-wide seasonal signature We analyzed the global transcriptomes of G. aculeatus from two contrasting habitats in mid Wales, River (Afon) Rheidol (RHD) and Lake (Llyn) Frongoch (FRN), in September 2012 and March 2013
Genes that were seasonally differentially expressed at both localities tended, overwhelmingly, to show synchronous expression
Summary
Fishes show seasonal patterns of immunity, but such phenomena are imperfectly understood in vertebrates generally, even in humans and mice As these seasonal patterns may link to infectious disease risk and individual condition, the nature of their control has real practical implications. We chose to primarily use global mRNA extracts from individual whole fishes rather than from isolated cell populations or tissues This was because a fully reductionist approach to cell populations would be impractical, and because the majority of the teleost immune system is likely to be diffusely distributed in the gut, under the skin and mucosal surfaces and in association with the gills and liver (where, for example, complement proteins are mostly synthesized) [12,13,14,15,16]
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