Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish

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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1254-6) contains supplementary material, which is available to authorized users.

Historical contingency shapes adaptive radiation in Antarctic fishes

“…These results provide an alternative view on the impact of climate change in driving extreme adaptations in the Southern Ocean (28,29). As we march further into the Anthropocene, our results caution that as both ecosystems and climate continue to change worldwide, the expectation that rapid adaptation will be dominant factor in predicting the response of biodiversity requires careful consideration (30).…”

Transcriptomic profiling revealed key signaling pathways for cold tolerance and acclimation of two carp species

“…Differentially expressed genes were classi ed with Venn's diagrams by online tools (https://bioinfogp.cnb.csic.es/tools/venny/index.html). KEGG (Kyoto Encyclopedia of Genes and Genomes) and GO (Gene Ontology) enrichment analysis were performed using TBtools software (https://github.com/CJ-Chen/TBtools) [13]. REVIGO tool (http://revigo.irb.hr/) [70] was used to cluster and prune GO terms on the basis of p-values obtained from TBtools.…”

“…Antarctic notothenioids have evolved to become both cold adapted and cold specialized and a marked signature of cold specialization is an apparent loss of the cellular heat shock response (HSR) [12]. The transcriptional response to acute heat stress was minimal in cold-adapted and red-blooded ice sh P. borchgrevinki, but robust responses in the C. rastrospinosus that represents the hemoglobinless Antarctic notothenioids occurred in the broader cellular networks especially in in ammatory responses despite lacking the classic HSR and unfolded protein response (UPR) [13]. In addition, many of closely related sh species including some members of the carp family exhibit distinctive abilities of tolerance to low temperature [14].…”

A tale of two genes: divergent evolutionary fate of haptoglobin and hemopexin in hemoglobinless antarctic icefishes

“…The complete coding sequences of Hp, Hx and mitochondrial ND2 genes for a subset of teleost fishes were obtained from Ensembl to serve as the reference set. Additional notothenioid Hp and Hx sequences came from the Parachaenichthys charcoti genome (Ahn et al, 2017) and the Eleginops maclovinus reference transcriptome (Bilyk et al, 2018). We then performed six comparisons to detect molecular evolutionary signals: (i) all icefish branches against all redblooded Antarctic notothenioid branches, (ii) all icefish branches against reference teleosts, (iii) all red-blooded Antarctic notothenioid branches against reference teleosts, (iv) the single ancestral branch to icefish against all other icefish branches, (v) the single ancestral branch to icefish against all red-blooded notothenioid branches, and (vi) the single ancestral branch to icefish against reference teleosts.…”