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 deg...

Full description

Bibliographic Details
Main Authors: Berthelot, Camille, Clarke, Jane, Desvignes, Thomas, William Detrich, H, Flicek, Paul, Peck, Lloyd S, Peters, Michael, Postlethwait, John H, Clark, Melody S
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2019
Subjects:
Online Access:https://www.repository.cam.ac.uk/handle/1810/289437
https://doi.org/10.17863/CAM.36686
id ftunivcam:oai:www.repository.cam.ac.uk:1810/289437
record_format openpolar
spelling ftunivcam:oai:www.repository.cam.ac.uk:1810/289437 2024-02-04T09:54:03+01:00 Adaptation of Proteins to the Cold in Antarctic Fish: A Role for Methionine? Berthelot, Camille Clarke, Jane Desvignes, Thomas William Detrich, H Flicek, Paul Peck, Lloyd S Peters, Michael Postlethwait, John H Clark, Melody S 2019-01-01 application/pdf https://www.repository.cam.ac.uk/handle/1810/289437 https://doi.org/10.17863/CAM.36686 eng eng Oxford University Press (OUP) https://academic.oup.com/gbe/article/11/1/220/5215157 Genome Biol Evol https://www.repository.cam.ac.uk/handle/1810/289437 doi:10.17863/CAM.36686 Attribution 4.0 International http://creativecommons.org/licenses/by/4.0/ Acclimatization Animals Antarctic Regions Evolution Molecular Fish Proteins Freezing Methionine Perciformes Protein Folding Transcriptome Article 2019 ftunivcam https://doi.org/10.17863/CAM.36686 2024-01-11T23:20:30Z 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 proteins with temperate teleost proteins, 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 Apollo - University of Cambridge Repository Antarctic Southern Ocean
institution Open Polar
collection Apollo - University of Cambridge Repository
op_collection_id ftunivcam
language English
topic Acclimatization
Animals
Antarctic Regions
Evolution
Molecular
Fish Proteins
Freezing
Methionine
Perciformes
Protein Folding
Transcriptome
spellingShingle Acclimatization
Animals
Antarctic Regions
Evolution
Molecular
Fish Proteins
Freezing
Methionine
Perciformes
Protein Folding
Transcriptome
Berthelot, Camille
Clarke, Jane
Desvignes, Thomas
William Detrich, H
Flicek, Paul
Peck, Lloyd S
Peters, Michael
Postlethwait, John H
Clark, Melody S
Adaptation of Proteins to the Cold in Antarctic Fish: A Role for Methionine?
topic_facet Acclimatization
Animals
Antarctic Regions
Evolution
Molecular
Fish Proteins
Freezing
Methionine
Perciformes
Protein Folding
Transcriptome
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 proteins with temperate teleost proteins, 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
William Detrich, H
Flicek, Paul
Peck, Lloyd S
Peters, Michael
Postlethwait, John H
Clark, Melody S
author_facet Berthelot, Camille
Clarke, Jane
Desvignes, Thomas
William Detrich, H
Flicek, Paul
Peck, Lloyd S
Peters, Michael
Postlethwait, John H
Clark, Melody S
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 University Press (OUP)
publishDate 2019
url https://www.repository.cam.ac.uk/handle/1810/289437
https://doi.org/10.17863/CAM.36686
geographic Antarctic
Southern Ocean
geographic_facet Antarctic
Southern Ocean
genre Antarc*
Antarctic
Southern Ocean
genre_facet Antarc*
Antarctic
Southern Ocean
op_relation https://www.repository.cam.ac.uk/handle/1810/289437
doi:10.17863/CAM.36686
op_rights Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.17863/CAM.36686
_version_ 1789970280371716096