Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats
Anhydrobiotic animals can survive the loss of both free and bound water from their cells. While in this state they are also resistant to freezing. This physiology adapts anhydrobiotes to harsh environments and it aids their dispersal. Panagrolaimus davidi, a bacterial feeding anhydrobiotic nematode...
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ftpubmed:oai:pubmedcentral.nih.gov:4352009 2023-05-15T13:56:01+02:00 Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats McGill, Lorraine M. Shannon, Adam J. Pisani, Davide Félix, Marie-Anne Ramløv, Hans Dix, Ilona Wharton, David A. Burnell, Ann M. 2015-03-06 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4352009 http://www.ncbi.nlm.nih.gov/pubmed/25747673 https://doi.org/10.1371/journal.pone.0116084 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC http://www.ncbi.nlm.nih.gov/pubmed/25747673 http://dx.doi.org/10.1371/journal.pone.0116084 http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited CC-BY Research Article Text 2015 ftpubmed https://doi.org/10.1371/journal.pone.0116084 2015-03-22T01:01:22Z Anhydrobiotic animals can survive the loss of both free and bound water from their cells. While in this state they are also resistant to freezing. This physiology adapts anhydrobiotes to harsh environments and it aids their dispersal. Panagrolaimus davidi, a bacterial feeding anhydrobiotic nematode isolated from Ross Island Antarctica, can survive intracellular ice formation when fully hydrated. A capacity to survive freezing while fully hydrated has also been observed in some other Antarctic nematodes. We experimentally determined the anhydrobiotic and freezing-tolerance phenotypes of 24 Panagrolaimus strains from tropical, temperate, continental and polar habitats and we analysed their phylogenetic relationships. We found that several other Panagrolaimus isolates can also survive freezing when fully hydrated and that tissue extracts from these freezing-tolerant nematodes can inhibit the growth of ice crystals. We show that P. davidi belongs to a clade of anhydrobiotic and freezing-tolerant panagrolaimids containing strains from temperate and continental regions and that P. superbus, an early colonizer at Surtsey island, Iceland after its volcanic formation, is closely related to a species from Pennsylvania, USA. Ancestral state reconstructions show that anhydrobiosis evolved deep in the phylogeny of Panagrolaimus. The early-diverging Panagrolaimus lineages are strongly anhydrobiotic but weakly freezing-tolerant, suggesting that freezing tolerance is most likely a derived trait. The common ancestors of the davidi and the superbus clades were anhydrobiotic and also possessed robust freezing tolerance, along with a capacity to inhibit the growth and recrystallization of ice crystals. Unlike other endemic Antarctic nematodes, the life history traits of P. davidi do not show evidence of an evolved response to polar conditions. Thus we suggest that the colonization of Antarctica by P. davidi and of Surtsey by P. superbus may be examples of recent “ecological fitting” of freezing-tolerant anhydrobiotic propagules to ... Text Antarc* Antarctic Antarctica Iceland Ross Island Surtsey PubMed Central (PMC) Antarctic Ross Island Surtsey ENVELOPE(-20.608,-20.608,63.301,63.301) PLOS ONE 10 3 e0116084 |
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Research Article |
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Research Article McGill, Lorraine M. Shannon, Adam J. Pisani, Davide Félix, Marie-Anne Ramløv, Hans Dix, Ilona Wharton, David A. Burnell, Ann M. Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
topic_facet |
Research Article |
description |
Anhydrobiotic animals can survive the loss of both free and bound water from their cells. While in this state they are also resistant to freezing. This physiology adapts anhydrobiotes to harsh environments and it aids their dispersal. Panagrolaimus davidi, a bacterial feeding anhydrobiotic nematode isolated from Ross Island Antarctica, can survive intracellular ice formation when fully hydrated. A capacity to survive freezing while fully hydrated has also been observed in some other Antarctic nematodes. We experimentally determined the anhydrobiotic and freezing-tolerance phenotypes of 24 Panagrolaimus strains from tropical, temperate, continental and polar habitats and we analysed their phylogenetic relationships. We found that several other Panagrolaimus isolates can also survive freezing when fully hydrated and that tissue extracts from these freezing-tolerant nematodes can inhibit the growth of ice crystals. We show that P. davidi belongs to a clade of anhydrobiotic and freezing-tolerant panagrolaimids containing strains from temperate and continental regions and that P. superbus, an early colonizer at Surtsey island, Iceland after its volcanic formation, is closely related to a species from Pennsylvania, USA. Ancestral state reconstructions show that anhydrobiosis evolved deep in the phylogeny of Panagrolaimus. The early-diverging Panagrolaimus lineages are strongly anhydrobiotic but weakly freezing-tolerant, suggesting that freezing tolerance is most likely a derived trait. The common ancestors of the davidi and the superbus clades were anhydrobiotic and also possessed robust freezing tolerance, along with a capacity to inhibit the growth and recrystallization of ice crystals. Unlike other endemic Antarctic nematodes, the life history traits of P. davidi do not show evidence of an evolved response to polar conditions. Thus we suggest that the colonization of Antarctica by P. davidi and of Surtsey by P. superbus may be examples of recent “ecological fitting” of freezing-tolerant anhydrobiotic propagules to ... |
format |
Text |
author |
McGill, Lorraine M. Shannon, Adam J. Pisani, Davide Félix, Marie-Anne Ramløv, Hans Dix, Ilona Wharton, David A. Burnell, Ann M. |
author_facet |
McGill, Lorraine M. Shannon, Adam J. Pisani, Davide Félix, Marie-Anne Ramløv, Hans Dix, Ilona Wharton, David A. Burnell, Ann M. |
author_sort |
McGill, Lorraine M. |
title |
Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
title_short |
Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
title_full |
Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
title_fullStr |
Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
title_full_unstemmed |
Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats |
title_sort |
anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of panagrolaimus nematodes in polar habitats |
publisher |
Public Library of Science |
publishDate |
2015 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4352009 http://www.ncbi.nlm.nih.gov/pubmed/25747673 https://doi.org/10.1371/journal.pone.0116084 |
long_lat |
ENVELOPE(-20.608,-20.608,63.301,63.301) |
geographic |
Antarctic Ross Island Surtsey |
geographic_facet |
Antarctic Ross Island Surtsey |
genre |
Antarc* Antarctic Antarctica Iceland Ross Island Surtsey |
genre_facet |
Antarc* Antarctic Antarctica Iceland Ross Island Surtsey |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC http://www.ncbi.nlm.nih.gov/pubmed/25747673 http://dx.doi.org/10.1371/journal.pone.0116084 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1371/journal.pone.0116084 |
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PLOS ONE |
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10 |
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3 |
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e0116084 |
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