Abstract
BackgroundConfined within the freezing Southern Ocean, the Antarctic notothenioids have evolved to become both cold adapted and cold specialized. A marked signature of cold specialization is an apparent loss of the cellular heat shock response (HSR). As the HSR has been examined in very few notothenioid species to-date, it remains unknown whether HSR loss pervades the Antarctic radiation, or whether the broader cellular responses to heat stress has sustained similar loss. Understanding the evolutionary status of these responses in this stenothermal taxon is crucial for evaluating its adaptive potential to ocean warming under climate change.ResultsIn this study, we used an acute heat stress protocol followed by RNA-Seq analyses to study the evolution of cellular-wide transcriptional responses to heat stress across three select notothenioid lineages - the basal temperate and nearest non-Antarctic sister species Eleginops maclovinus serving as ancestral proxy, the cryopelagic Pagothenia borchgrevinki and the icefish Chionodraco rastrospinosus representing cold-adapted red-blooded and hemoglobinless Antarctic notothenioids respectively. E. maclovinus displayed robust cellular stress responses including the ER Unfolded Protein Response and the cytosolic HSR, cementing the HSR as a plesiomorphy that preceded Antarctic notothenioid radiation. While the transcriptional response to heat stress was minimal in P. borchgrevinki, C. rastrospinosus exhibited robust responses in the broader cellular networks especially in inflammatory responses despite lacking the classic HSR and UPR.ConclusionThe disparate patterns observed in these two archetypal Antarctic species indicate the evolutionary status in cellular ability to mitigate acute heat stress varies even among Antarctic lineages, which may affect their adaptive potential in coping with a warming world.
Highlights
Confined within the freezing Southern Ocean, the Antarctic notothenioids have evolved to become both cold adapted and cold specialized
As the most relevant ancestral proxy for Antarctic notothenioids, the heat induced transcriptional response of the basal temperate E. maclovinus provides a window into its status prior to the influence of chronic freezing polar marine conditions
With an organized response to denatured proteins specific to just E. maclovinus, this study shows that both the classic heat shock response (HSR) and the endoplasmic reticulum (ER) specific Unfolded Protein Response (UPR) appear missing in response to severe heat stress among the Antarctic notothenioids
Summary
Confined within the freezing Southern Ocean, the Antarctic notothenioids have evolved to become both cold adapted and cold specialized. A marked signature of cold specialization is an apparent loss of the cellular heat shock response (HSR). As the HSR has been examined in very few notothenioid species to-date, it remains unknown whether HSR loss pervades the Antarctic radiation, or whether the broader cellular responses to heat stress has sustained similar loss. Evolution in the unrelenting cold of the isolated Southern Ocean has profoundly shaped the biology of the endemic Antarctic notothenioid fishes. Apart from HSR, the full nature and extent of broader cellular responses, which are normally activated by heat shock, remain incompletely understood. The accumulation of denatured, unfolded, and misfolded proteins within the lumen of the endoplasmic reticulum (ER) leads to ER stress and activates ER-specific molecular chaperones in the Unfolded Protein Response (UPR) [12, 13]
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