Lost in translation? Evidence for a muted proteomic response to thermal stress in a stenothermal Antarctic fish and possible evolutionary mechanisms.

Abstract

Stenothermal Antarctic notothenioid fishes are noteworthy for their history of isolation in extreme cold and their corresponding lack of the canonical heat shock response. Despite extensive transcriptomic studies, the mechanistic basis for stenothermy has not been fully elucidated. Given that the proteome better represents an organism's physiology, the possibility exists that some aspects of stenothermy arise post-transcriptionally. Here, Antarctic emerald rockcod (Trematomus bernacchii) were sampled after exposure to chronic and/or acute high temperatures, followed by thorough assessment of proteomic responses in brain, gill, and kidney. Few cellular stress response proteins were induced, and overall responses were modest in terms of numbers of differentially expressed proteins and their fold changes. Inconsistencies in protein induction across treatments and tissues are suggestive of dysregulation, rather than an adaptive response. Changes in regulation of the translational machinery in Antarctic notothenioids could explain these patterns. Some components of translational regulatory pathways are highly conserved (e.g., Ser-52 of eIF2α), but proteins comprising the cellular "integrative stress response" - specifically, the eIF2α kinases GCN2 and PERK - may have evolved along different trajectories in Antarctic fishes. Taken together, these observations suggest a novel hypothesis for stenothermy and the absence of a coordinated cellular stress response in Antarctic fishes.