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Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish
BACKGROUND: 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 nototh...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146603/ https://www.ncbi.nlm.nih.gov/pubmed/30231868 http://dx.doi.org/10.1186/s12862-018-1254-6 |
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author | Bilyk, Kevin T. Vargas-Chacoff, Luis Cheng, C.-H.Christina |
author_facet | Bilyk, Kevin T. Vargas-Chacoff, Luis Cheng, C.-H.Christina |
author_sort | Bilyk, Kevin T. |
collection | PubMed |
description | BACKGROUND: 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. Understanding the evolutionary status of these responses in this stenothermal taxon is crucial for evaluating its adaptive potential to ocean warming under climate change. RESULTS: In 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. CONCLUSION: The 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 MATERIAL: The online version of this article (10.1186/s12862-018-1254-6) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6146603 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-61466032018-09-24 Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish Bilyk, Kevin T. Vargas-Chacoff, Luis Cheng, C.-H.Christina BMC Evol Biol Research Article BACKGROUND: 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. Understanding the evolutionary status of these responses in this stenothermal taxon is crucial for evaluating its adaptive potential to ocean warming under climate change. RESULTS: In 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. CONCLUSION: The 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 MATERIAL: The online version of this article (10.1186/s12862-018-1254-6) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-19 /pmc/articles/PMC6146603/ /pubmed/30231868 http://dx.doi.org/10.1186/s12862-018-1254-6 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Bilyk, Kevin T. Vargas-Chacoff, Luis Cheng, C.-H.Christina Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title | Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title_full | Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title_fullStr | Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title_full_unstemmed | Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title_short | Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish |
title_sort | evolution in chronic cold: varied loss of cellular response to heat in antarctic notothenioid fish |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146603/ https://www.ncbi.nlm.nih.gov/pubmed/30231868 http://dx.doi.org/10.1186/s12862-018-1254-6 |
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