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

Abstract 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 fe...

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Main Authors: Bilyk, Kevin, Vargas-Chacoff, Luis, C.-H.Christina Cheng
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2018
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.4238360
https://figshare.com/collections/Evolution_in_chronic_cold_varied_loss_of_cellular_response_to_heat_in_Antarctic_notothenioid_fish/4238360
id ftdatacite:10.6084/m9.figshare.c.4238360
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.4238360 2023-05-15T13:48:16+02:00 Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish Bilyk, Kevin Vargas-Chacoff, Luis C.-H.Christina Cheng 2018 https://dx.doi.org/10.6084/m9.figshare.c.4238360 https://figshare.com/collections/Evolution_in_chronic_cold_varied_loss_of_cellular_response_to_heat_in_Antarctic_notothenioid_fish/4238360 unknown Figshare https://dx.doi.org/10.1186/s12862-018-1254-6 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Cell Biology Genetics FOS Biological sciences Molecular Biology Physiology Biotechnology Evolutionary Biology 59999 Environmental Sciences not elsewhere classified FOS Earth and related environmental sciences Ecology Marine Biology Inorganic Chemistry FOS Chemical sciences 111714 Mental Health FOS Health sciences 110309 Infectious Diseases Plant Biology Computational Biology Collection article 2018 ftdatacite https://doi.org/10.6084/m9.figshare.c.4238360 https://doi.org/10.1186/s12862-018-1254-6 2021-11-05T12:55:41Z Abstract 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. Article in Journal/Newspaper Antarc* Antarctic Icefish Southern Ocean DataCite Metadata Store (German National Library of Science and Technology) Antarctic Southern Ocean The Antarctic
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Biotechnology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Marine Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
110309 Infectious Diseases
Plant Biology
Computational Biology
spellingShingle Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Biotechnology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Marine Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
110309 Infectious Diseases
Plant Biology
Computational Biology
Bilyk, Kevin
Vargas-Chacoff, Luis
C.-H.Christina Cheng
Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish
topic_facet Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Biotechnology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Marine Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
110309 Infectious Diseases
Plant Biology
Computational Biology
description Abstract 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.
format Article in Journal/Newspaper
author Bilyk, Kevin
Vargas-Chacoff, Luis
C.-H.Christina Cheng
author_facet Bilyk, Kevin
Vargas-Chacoff, Luis
C.-H.Christina Cheng
author_sort Bilyk, Kevin
title 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_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_sort evolution in chronic cold: varied loss of cellular response to heat in antarctic notothenioid fish
publisher Figshare
publishDate 2018
url https://dx.doi.org/10.6084/m9.figshare.c.4238360
https://figshare.com/collections/Evolution_in_chronic_cold_varied_loss_of_cellular_response_to_heat_in_Antarctic_notothenioid_fish/4238360
geographic Antarctic
Southern Ocean
The Antarctic
geographic_facet Antarctic
Southern Ocean
The Antarctic
genre Antarc*
Antarctic
Icefish
Southern Ocean
genre_facet Antarc*
Antarctic
Icefish
Southern Ocean
op_relation https://dx.doi.org/10.1186/s12862-018-1254-6
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.4238360
https://doi.org/10.1186/s12862-018-1254-6
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