Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
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 a...
Published in: | Proceedings of the National Academy of Sciences |
---|---|
Main Authors: | , , , , , , , |
Other Authors: | , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2012
|
Subjects: | |
Online Access: | https://doi.org/10.1073/pnas.1218661109 https://hal.archives-ouvertes.fr/hal-00801357 |
id |
fttriple:oai:gotriple.eu:10670/1.s31cki |
---|---|
record_format |
openpolar |
spelling |
fttriple:oai:gotriple.eu:10670/1.s31cki 2023-05-15T13:58:50+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 2012-01-01 https://doi.org/10.1073/pnas.1218661109 https://hal.archives-ouvertes.fr/hal-00801357 en eng HAL CCSD National Academy of Sciences hal-00801357 doi:10.1073/pnas.1218661109 10670/1.s31cki https://hal.archives-ouvertes.fr/hal-00801357 undefined Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 0027-8424 EISSN: 1091-6490 Proceedings of the National Academy of Sciences of the United States of America 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 geo envir Journal Article https://vocabularies.coar-repositories.org/resource_types/c_6501/ 2012 fttriple https://doi.org/10.1073/pnas.1218661109 2023-01-22T17:37:37Z 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. Utilisation du GC-MS de l'umr 6553 Ecobio; Aide technique de Vanessa Larvor Article in Journal/Newspaper Antarc* Antarctic Antarctic midge Antarctica Arctic Belgica antarctica Unknown Antarctic Arctic The Antarctic Proceedings of the National Academy of Sciences 109 50 20744 20749 |
institution |
Open Polar |
collection |
Unknown |
op_collection_id |
fttriple |
language |
English |
topic |
environmental stress physiological ecology geo envir |
spellingShingle |
environmental stress physiological ecology geo envir 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 geo envir |
description |
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. Utilisation du GC-MS de l'umr 6553 Ecobio; Aide technique de Vanessa Larvor |
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://doi.org/10.1073/pnas.1218661109 https://hal.archives-ouvertes.fr/hal-00801357 |
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 |
Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 0027-8424 EISSN: 1091-6490 Proceedings of the National Academy of Sciences of the United States of America 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⟩ |
op_relation |
hal-00801357 doi:10.1073/pnas.1218661109 10670/1.s31cki https://hal.archives-ouvertes.fr/hal-00801357 |
op_rights |
undefined |
op_doi |
https://doi.org/10.1073/pnas.1218661109 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
109 |
container_issue |
50 |
container_start_page |
20744 |
op_container_end_page |
20749 |
_version_ |
1766267198924390400 |