Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

Utilisation du GC-MS de l'umr 6553 Ecobio; Aide technique de Vanessa Larvor International audience Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar...

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Published in:Proceedings of the National Academy of Sciences
Main Authors: Teets, Nicholas M., Peyton, Justin T., Colinet, Hervé, Renault, David, Kelley, Joanna L., Kawarasaki, Yuta, Lee, Richard E. Jr, Denlinger, David L.
Other Authors: Entomology, Ohio State University, Ohio State University Columbus (OSU), Evolution, Ecology and Organismal Biology, Ecosystèmes, biodiversité, évolution Rennes (ECOBIO), Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES), Department of Genetics Stanford, Stanford Medicine, Stanford University-Stanford University, Zoology and Program in Ecology, Evolution and Environmental Biology, Miami University Ohio (MU), NSF OPP-ANT-0837613 and ANT-0837559; IPEV Program 136; SCAREB of Antarctic research program
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2012
Subjects:
Online Access:https://hal.archives-ouvertes.fr/hal-00801357
https://doi.org/10.1073/pnas.1218661109
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record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic environmental stress
physiological ecology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle environmental stress
physiological ecology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Teets, Nicholas M.
Peyton, Justin T.
Colinet, Hervé
Renault, David
Kelley, Joanna L.
Kawarasaki, Yuta
Lee, Richard E. Jr
Denlinger, David L.
Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
topic_facet environmental stress
physiological ecology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description Utilisation du GC-MS de l'umr 6553 Ecobio; Aide technique de Vanessa Larvor International audience Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar arthropods that face near- constant desiccating conditions, as water is frozen and thus unavailable for much of the year. The molecular mechanisms that govern extreme dehydration tolerance in insects remain largely undefined. In this study, we used RNA sequencing to quantify transcriptional mechanisms of extreme dehydration tolerance in the Antarctic midge, Belgica antarctica, the world's southern most insect and only insect endemic to Antarctica. Larvae of B. antarctica are remarkably tolerant of dehydration, surviving losses up to 70% of their body water. Gene expression changes in response to dehydration indicated up-regulation of cellular recycling pathways including the ubiquitin-mediated proteasome and autophagy, with concurrent down-regulation of genes involved in general metabolism and ATP production. Metabolomics results revealed shifts in metabolite pools that correlated closely with changes in gene expression, indicating that coordinated changes in gene expression and metabolism are a critical component of the dehydration response. Finally, using comparative genomics, we compared our gene expression results with a transcriptomic dataset for the Arctic collembolan, Megaphorura arctica. Although B. antarctica and M. arctica are adapted to similar environments, our analysis indicated very little overlap in expression profiles between these two arthropods. Whereas several orthologous genes showed similar expression patterns, transcriptional changes were largely species specific, indicating these polar arthropods have developed distinct transcriptional mechanisms to cope with similar desiccating conditions.
author2 Entomology, Ohio State University
Ohio State University Columbus (OSU)
Evolution, Ecology and Organismal Biology
Ecosystèmes, biodiversité, évolution Rennes (ECOBIO)
Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Institut Ecologie et Environnement (INEE)
Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1)
Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)
Department of Genetics Stanford
Stanford Medicine
Stanford University-Stanford University
Zoology and Program in Ecology, Evolution and Environmental Biology
Miami University Ohio (MU)
NSF OPP-ANT-0837613 and ANT-0837559; IPEV Program 136; SCAREB of Antarctic research program
format Article in Journal/Newspaper
author Teets, Nicholas M.
Peyton, Justin T.
Colinet, Hervé
Renault, David
Kelley, Joanna L.
Kawarasaki, Yuta
Lee, Richard E. Jr
Denlinger, David L.
author_facet Teets, Nicholas M.
Peyton, Justin T.
Colinet, Hervé
Renault, David
Kelley, Joanna L.
Kawarasaki, Yuta
Lee, Richard E. Jr
Denlinger, David L.
author_sort Teets, Nicholas M.
title Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
title_short Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
title_full Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
title_fullStr Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
title_full_unstemmed Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
title_sort gene expression changes governing extreme dehydration tolerance in an antarctic insect
publisher HAL CCSD
publishDate 2012
url https://hal.archives-ouvertes.fr/hal-00801357
https://doi.org/10.1073/pnas.1218661109
geographic Antarctic
Arctic
The Antarctic
geographic_facet Antarctic
Arctic
The Antarctic
genre Antarc*
Antarctic
Antarctic midge
Antarctica
Arctic
Belgica antarctica
genre_facet Antarc*
Antarctic
Antarctic midge
Antarctica
Arctic
Belgica antarctica
op_source ISSN: 0027-8424
EISSN: 1091-6490
Proceedings of the National Academy of Sciences of the United States of America
https://hal.archives-ouvertes.fr/hal-00801357
Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2012, 109 (50), pp.20744-20749. ⟨10.1073/pnas.1218661109⟩
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op_doi https://doi.org/10.1073/pnas.1218661109
container_title Proceedings of the National Academy of Sciences
container_volume 109
container_issue 50
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spelling ftccsdartic:oai:HAL:hal-00801357v1 2023-05-15T14:04:01+02:00 Gene expression changes governing extreme dehydration tolerance in an Antarctic insect Teets, Nicholas M. Peyton, Justin T. Colinet, Hervé Renault, David Kelley, Joanna L. Kawarasaki, Yuta Lee, Richard E. Jr Denlinger, David L. Entomology, Ohio State University Ohio State University Columbus (OSU) Evolution, Ecology and Organismal Biology Ecosystèmes, biodiversité, évolution Rennes (ECOBIO) Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Institut Ecologie et Environnement (INEE) Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1) Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES) Department of Genetics Stanford Stanford Medicine Stanford University-Stanford University Zoology and Program in Ecology, Evolution and Environmental Biology Miami University Ohio (MU) NSF OPP-ANT-0837613 and ANT-0837559; IPEV Program 136; SCAREB of Antarctic research program 2012 https://hal.archives-ouvertes.fr/hal-00801357 https://doi.org/10.1073/pnas.1218661109 en eng HAL CCSD National Academy of Sciences info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1218661109 hal-00801357 https://hal.archives-ouvertes.fr/hal-00801357 doi:10.1073/pnas.1218661109 ISSN: 0027-8424 EISSN: 1091-6490 Proceedings of the National Academy of Sciences of the United States of America https://hal.archives-ouvertes.fr/hal-00801357 Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2012, 109 (50), pp.20744-20749. ⟨10.1073/pnas.1218661109⟩ environmental stress physiological ecology [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2012 ftccsdartic https://doi.org/10.1073/pnas.1218661109 2021-10-24T15:17:07Z Utilisation du GC-MS de l'umr 6553 Ecobio; Aide technique de Vanessa Larvor International audience Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar arthropods that face near- constant desiccating conditions, as water is frozen and thus unavailable for much of the year. The molecular mechanisms that govern extreme dehydration tolerance in insects remain largely undefined. In this study, we used RNA sequencing to quantify transcriptional mechanisms of extreme dehydration tolerance in the Antarctic midge, Belgica antarctica, the world's southern most insect and only insect endemic to Antarctica. Larvae of B. antarctica are remarkably tolerant of dehydration, surviving losses up to 70% of their body water. Gene expression changes in response to dehydration indicated up-regulation of cellular recycling pathways including the ubiquitin-mediated proteasome and autophagy, with concurrent down-regulation of genes involved in general metabolism and ATP production. Metabolomics results revealed shifts in metabolite pools that correlated closely with changes in gene expression, indicating that coordinated changes in gene expression and metabolism are a critical component of the dehydration response. Finally, using comparative genomics, we compared our gene expression results with a transcriptomic dataset for the Arctic collembolan, Megaphorura arctica. Although B. antarctica and M. arctica are adapted to similar environments, our analysis indicated very little overlap in expression profiles between these two arthropods. Whereas several orthologous genes showed similar expression patterns, transcriptional changes were largely species specific, indicating these polar arthropods have developed distinct transcriptional mechanisms to cope with similar desiccating conditions. Article in Journal/Newspaper Antarc* Antarctic Antarctic midge Antarctica Arctic Belgica antarctica Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Antarctic Arctic The Antarctic Proceedings of the National Academy of Sciences 109 50 20744 20749