Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?

The evolution of antifreeze glycoproteins has enabled notothenioid fish to flourish in the freezing waters of the Southern Ocean.Whereas successful at the biodiversity level to life in the cold, paradoxically at the cellular level these stenothermal animals have problems producing, folding, and degr...

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Published in:Genome Biology and Evolution
Main Authors: Berthelot, Camille, Clarke, Jane, Desvignes, Thomas, Detrich III, H William, Flicek, Paul, Peck, Lloyd, Peters, Michael, Postlethwait, John H, Clark, Melody
Format: Article in Journal/Newspaper
Language:English
Published: Oxford Academic 2019
Subjects:
Online Access:http://nora.nerc.ac.uk/id/eprint/522308/
https://nora.nerc.ac.uk/id/eprint/522308/1/evy262.pdf
https://academic.oup.com/gbe/article/11/1/220/5215157
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spelling ftnerc:oai:nora.nerc.ac.uk:522308 2023-05-15T13:41:43+02:00 Adaptation of proteins to the cold in Antarctic fish: A role for Methionine? Berthelot, Camille Clarke, Jane Desvignes, Thomas Detrich III, H William Flicek, Paul Peck, Lloyd Peters, Michael Postlethwait, John H Clark, Melody 2019-01 text http://nora.nerc.ac.uk/id/eprint/522308/ https://nora.nerc.ac.uk/id/eprint/522308/1/evy262.pdf https://academic.oup.com/gbe/article/11/1/220/5215157 en eng Oxford Academic https://nora.nerc.ac.uk/id/eprint/522308/1/evy262.pdf Berthelot, Camille; Clarke, Jane; Desvignes, Thomas; Detrich III, H William; Flicek, Paul; Peck, Lloyd orcid:0000-0003-3479-6791 Peters, Michael; Postlethwait, John H; Clark, Melody orcid:0000-0002-3442-3824 . 2019 Adaptation of proteins to the cold in Antarctic fish: A role for Methionine? Genome Biology and Evolution, 11 (1). 220-231. https://doi.org/10.1093/gbe/evy262 <https://doi.org/10.1093/gbe/evy262> cc_by_4 CC-BY Publication - Article PeerReviewed 2019 ftnerc 2023-02-04T19:47:50Z The evolution of antifreeze glycoproteins has enabled notothenioid fish to flourish in the freezing waters of the Southern Ocean.Whereas successful at the biodiversity level to life in the cold, paradoxically at the cellular level these stenothermal animals have problems producing, folding, and degrading proteins at their ambient temperatures of –1.86 °C. In this first multi-species transcriptome comparison of the amino acid composition of notothenioid proteinswith temperate teleostproteins,we show that, unlike psychrophilic bacteria, Antarctic fish provide little evidence for the mass alteration of protein amino acid composition to enhance protein folding and reduce protein denaturation in the cold. The exception was the significant overrepresentation of positions where leucine in temperate fish proteins was replaced by methionine in the notothenioid orthologues. We hypothesize that these extra methionines have been preferentially assimilated into the genome to act as redox sensors in the highly oxygenated waters of the Southern Ocean. This redox hypothesis is supported by analyses of notothenioids showing enrichment of genes associated with responses to environmental stress, particularly reactive oxygen species. So overall, although notothenioid fish show cold-associated problems with protein homeostasis, they may have modified only a selected number of biochemical pathways to work efficiently below 0°C. Even a slight warming of the Southern Ocean might disrupt the critical functions of this handful of key pathways with considerable impacts for the functioning of this ecosystem in the future. Article in Journal/Newspaper Antarc* Antarctic Southern Ocean Natural Environment Research Council: NERC Open Research Archive Antarctic Southern Ocean Genome Biology and Evolution 11 1 220 231
institution Open Polar
collection Natural Environment Research Council: NERC Open Research Archive
op_collection_id ftnerc
language English
description The evolution of antifreeze glycoproteins has enabled notothenioid fish to flourish in the freezing waters of the Southern Ocean.Whereas successful at the biodiversity level to life in the cold, paradoxically at the cellular level these stenothermal animals have problems producing, folding, and degrading proteins at their ambient temperatures of –1.86 °C. In this first multi-species transcriptome comparison of the amino acid composition of notothenioid proteinswith temperate teleostproteins,we show that, unlike psychrophilic bacteria, Antarctic fish provide little evidence for the mass alteration of protein amino acid composition to enhance protein folding and reduce protein denaturation in the cold. The exception was the significant overrepresentation of positions where leucine in temperate fish proteins was replaced by methionine in the notothenioid orthologues. We hypothesize that these extra methionines have been preferentially assimilated into the genome to act as redox sensors in the highly oxygenated waters of the Southern Ocean. This redox hypothesis is supported by analyses of notothenioids showing enrichment of genes associated with responses to environmental stress, particularly reactive oxygen species. So overall, although notothenioid fish show cold-associated problems with protein homeostasis, they may have modified only a selected number of biochemical pathways to work efficiently below 0°C. Even a slight warming of the Southern Ocean might disrupt the critical functions of this handful of key pathways with considerable impacts for the functioning of this ecosystem in the future.
format Article in Journal/Newspaper
author Berthelot, Camille
Clarke, Jane
Desvignes, Thomas
Detrich III, H William
Flicek, Paul
Peck, Lloyd
Peters, Michael
Postlethwait, John H
Clark, Melody
spellingShingle Berthelot, Camille
Clarke, Jane
Desvignes, Thomas
Detrich III, H William
Flicek, Paul
Peck, Lloyd
Peters, Michael
Postlethwait, John H
Clark, Melody
Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
author_facet Berthelot, Camille
Clarke, Jane
Desvignes, Thomas
Detrich III, H William
Flicek, Paul
Peck, Lloyd
Peters, Michael
Postlethwait, John H
Clark, Melody
author_sort Berthelot, Camille
title Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
title_short Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
title_full Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
title_fullStr Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
title_full_unstemmed Adaptation of proteins to the cold in Antarctic fish: A role for Methionine?
title_sort adaptation of proteins to the cold in antarctic fish: a role for methionine?
publisher Oxford Academic
publishDate 2019
url http://nora.nerc.ac.uk/id/eprint/522308/
https://nora.nerc.ac.uk/id/eprint/522308/1/evy262.pdf
https://academic.oup.com/gbe/article/11/1/220/5215157
geographic Antarctic
Southern Ocean
geographic_facet Antarctic
Southern Ocean
genre Antarc*
Antarctic
Southern Ocean
genre_facet Antarc*
Antarctic
Southern Ocean
op_relation https://nora.nerc.ac.uk/id/eprint/522308/1/evy262.pdf
Berthelot, Camille; Clarke, Jane; Desvignes, Thomas; Detrich III, H William; Flicek, Paul; Peck, Lloyd orcid:0000-0003-3479-6791
Peters, Michael; Postlethwait, John H; Clark, Melody orcid:0000-0002-3442-3824 . 2019 Adaptation of proteins to the cold in Antarctic fish: A role for Methionine? Genome Biology and Evolution, 11 (1). 220-231. https://doi.org/10.1093/gbe/evy262 <https://doi.org/10.1093/gbe/evy262>
op_rights cc_by_4
op_rightsnorm CC-BY
container_title Genome Biology and Evolution
container_volume 11
container_issue 1
container_start_page 220
op_container_end_page 231
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