Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

Nicholas M. Teets, Justin T. Peyton, Herve Colinet, David Renault, Joanna L. Kelley, Yuta Kawarasaki, Richard E. Lee, David L. Denlinger

Research output: Contribution to journalArticlepeer-review

91 Scopus citations

Abstract

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 southernmost 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.

Original languageEnglish
Pages (from-to)20744-20749
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number50
DOIs
StatePublished - Dec 11 2012

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank the staff of Palmer Station for support during our field season. We also acknowledge Asela Wijeratne and members of the Ohio Agricultural Research and Development Center Molecular and Cellular Imaging Center for running the sequencing reactions. We appreciate input from Xiaodong Bai during the initial planning phase of this study, and we thank Martin Holmstrup (Aarhus University) and Melody Clark (British Antarctic Survey) for critically reading the paper. We acknowledge Vanessa Larvor for technical assistance in the GC-MS experiments. This work was supported by National Science Foundation OPP-ANT-0837613 and ANT-0837559. Funding for the metabolomics experiments was provided by the French Polar Institute (Institut Polaire Français Paul-Emile Victor 136) and is linked with the Scientific Committee on Antarctic Research Evolution and Biodiversity in the Antarctic research program.

Funding Information:
We thank the staff of Palmer Station for support during our field season. We also acknowledge Asela Wijeratne and members of the Ohio Agricultural Research and Development Center Molecular and Cellular Imaging Center for running the sequencing reactions. We appreciate input from Xiaodong Bai during the initial planning phase of this study, and we thank Martin Holmstrup (Aarhus University) and Melody Clark (British Antarctic Survey) for critically reading the paper. We acknowledge Vanessa Larvor for technical assistance in the GC-MS experiments. This work was supported by National Science Foundation OPP-ANT-0837613 and ANT-0837559. Funding for the metabolomics experiments was provided by the French Polar Institute (Institut Polaire Fran?ais Paul-Emile Victor 136) and is linked with the Scientific Committee on Antarctic Research Evolution and Biodiversity in the Antarctic research program.

Publisher Copyright:
© 2012, National Academy of Sciences. All rights reserved.

Keywords

  • Environmental stress
  • Physiological ecology

ASJC Scopus subject areas

  • General

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