Injury improves tolerance to acute heat stress through induction of heat shock protein expression in the annelid Pristina leidyi

Evolutionary patterns of regeneration ability in animals may reflect the relative costs of injury versus regeneration on organismal function. While the cost of injury seems obvious, the investment of resources and other physiological effects produced by regeneration may be considerable, and the effects of both injury and regeneration may depend upon myriad factors intrinsic to organisms or within their environments. Such effects and how they vary are not well understood. We investigated the physiological effects of amputation injury and subsequent regeneration of tissue in the annelid Pristina leidyi, using environmental stress tolerance as a relevant measure of performance. Unexpectedly, injury improved survival under heat stress, but improved heat tolerance was unrelated to changes in metabolic rate. We performed TagSeq to investigate the transcriptional basis of injury-induced heat tolerance and found that injured worms produced an exaggerated response to subsequent heat stress compared to either injury or heat stress alone. Both injury and heat stress commonly induced the expression of just two heat shock family proteins. Pharmacological inhibition of one of these proteins, mortalin, drastically reduced heat tolerance in both uninjured and injured worms and substantially impaired anterior tissue regeneration. We posit that injury-induced expression of mortalin and other cellular stress response factors briefly confers improved resistance to broad forms of stress. Our work demonstrates that injury may have unpredictable effects and points to a shared ancestral response to various forms of biological damage with a critical role in animal function during the regeneration process.