Slow desiccation improves dehydration tolerance and accumulation of compatible osmolytes in earthworm cocoons (Dendrobaena octaedra Savigny)

Christina Rask Petersen, Martin Holmstrup, Anders Malmendal, Mark Bayley, Johannes Overgaard

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

The earthworm, Dendrobaena octaedra, is a common species in temperate and subarctic regions of the northern hemisphere. The egg capsules ('cocoons') of D. octaedra are deposited in the upper soil layers where they may be exposed to desiccation. Many previous studies on desiccation tolerance in soil invertebrates have examined acute exposure to harsh desiccating conditions, however, these animals are often more likely to be exposed to a gradually increasing drought stress. In the present study we slowly desiccated D. octaedra cocoons to simulate ecologically realistic drought conditions and the results clearly demonstrate that gradually dehydrated cocoons show an increased tolerance of extreme drought compared with acutely dehydrated cocoons. NMR spectroscopic analysis of compatible osmolytes revealed the presence of sorbitol, glucose, betaine, alanine and mannitol in dehydrated embryos. The superior drought survival of gradually desiccated embryos could partly be attributed to a higher accumulation of osmolytes (especially sorbitol). Thus, gradually and acutely desiccated embryos accumulated approximately 2 mol l(-1) and 1 mol l(-1) total osmolytes, respectively. However, in addition to osmolyte accumulation, the gradually desiccated cocoons also tolerated a higher degree of water loss, demonstrating that gradually dehydrated D. octaedra cocoons are able to survive loss of approximately 95% of the original water content. Although D. octaedra embryos can probably not be categorized as a truly anhydrobiotic organism we propose that they belong in a transition zone between the desiccation sensitive and the truly anhydrobiotic organisms. Clearly, these earthworm embryos share many physiological traits with anhydrobiotic organisms.
OriginalsprogEngelsk
TidsskriftJournal of Experimental Biology
Vol/bind211
Udgave nummerPt 12
Sider (fra-til)1903-10
Antal sider8
ISSN0022-0949
DOI
StatusUdgivet - 1 jun. 2008
Udgivet eksterntJa

Citer dette

Petersen, Christina Rask ; Holmstrup, Martin ; Malmendal, Anders ; Bayley, Mark ; Overgaard, Johannes. / Slow desiccation improves dehydration tolerance and accumulation of compatible osmolytes in earthworm cocoons (Dendrobaena octaedra Savigny). I: Journal of Experimental Biology. 2008 ; Bind 211, Nr. Pt 12. s. 1903-10.
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abstract = "The earthworm, Dendrobaena octaedra, is a common species in temperate and subarctic regions of the northern hemisphere. The egg capsules ('cocoons') of D. octaedra are deposited in the upper soil layers where they may be exposed to desiccation. Many previous studies on desiccation tolerance in soil invertebrates have examined acute exposure to harsh desiccating conditions, however, these animals are often more likely to be exposed to a gradually increasing drought stress. In the present study we slowly desiccated D. octaedra cocoons to simulate ecologically realistic drought conditions and the results clearly demonstrate that gradually dehydrated cocoons show an increased tolerance of extreme drought compared with acutely dehydrated cocoons. NMR spectroscopic analysis of compatible osmolytes revealed the presence of sorbitol, glucose, betaine, alanine and mannitol in dehydrated embryos. The superior drought survival of gradually desiccated embryos could partly be attributed to a higher accumulation of osmolytes (especially sorbitol). Thus, gradually and acutely desiccated embryos accumulated approximately 2 mol l(-1) and 1 mol l(-1) total osmolytes, respectively. However, in addition to osmolyte accumulation, the gradually desiccated cocoons also tolerated a higher degree of water loss, demonstrating that gradually dehydrated D. octaedra cocoons are able to survive loss of approximately 95{\%} of the original water content. Although D. octaedra embryos can probably not be categorized as a truly anhydrobiotic organism we propose that they belong in a transition zone between the desiccation sensitive and the truly anhydrobiotic organisms. Clearly, these earthworm embryos share many physiological traits with anhydrobiotic organisms.",
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Slow desiccation improves dehydration tolerance and accumulation of compatible osmolytes in earthworm cocoons (Dendrobaena octaedra Savigny). / Petersen, Christina Rask; Holmstrup, Martin; Malmendal, Anders; Bayley, Mark; Overgaard, Johannes.

I: Journal of Experimental Biology, Bind 211, Nr. Pt 12, 01.06.2008, s. 1903-10.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Slow desiccation improves dehydration tolerance and accumulation of compatible osmolytes in earthworm cocoons (Dendrobaena octaedra Savigny)

AU - Petersen, Christina Rask

AU - Holmstrup, Martin

AU - Malmendal, Anders

AU - Bayley, Mark

AU - Overgaard, Johannes

PY - 2008/6/1

Y1 - 2008/6/1

N2 - The earthworm, Dendrobaena octaedra, is a common species in temperate and subarctic regions of the northern hemisphere. The egg capsules ('cocoons') of D. octaedra are deposited in the upper soil layers where they may be exposed to desiccation. Many previous studies on desiccation tolerance in soil invertebrates have examined acute exposure to harsh desiccating conditions, however, these animals are often more likely to be exposed to a gradually increasing drought stress. In the present study we slowly desiccated D. octaedra cocoons to simulate ecologically realistic drought conditions and the results clearly demonstrate that gradually dehydrated cocoons show an increased tolerance of extreme drought compared with acutely dehydrated cocoons. NMR spectroscopic analysis of compatible osmolytes revealed the presence of sorbitol, glucose, betaine, alanine and mannitol in dehydrated embryos. The superior drought survival of gradually desiccated embryos could partly be attributed to a higher accumulation of osmolytes (especially sorbitol). Thus, gradually and acutely desiccated embryos accumulated approximately 2 mol l(-1) and 1 mol l(-1) total osmolytes, respectively. However, in addition to osmolyte accumulation, the gradually desiccated cocoons also tolerated a higher degree of water loss, demonstrating that gradually dehydrated D. octaedra cocoons are able to survive loss of approximately 95% of the original water content. Although D. octaedra embryos can probably not be categorized as a truly anhydrobiotic organism we propose that they belong in a transition zone between the desiccation sensitive and the truly anhydrobiotic organisms. Clearly, these earthworm embryos share many physiological traits with anhydrobiotic organisms.

AB - The earthworm, Dendrobaena octaedra, is a common species in temperate and subarctic regions of the northern hemisphere. The egg capsules ('cocoons') of D. octaedra are deposited in the upper soil layers where they may be exposed to desiccation. Many previous studies on desiccation tolerance in soil invertebrates have examined acute exposure to harsh desiccating conditions, however, these animals are often more likely to be exposed to a gradually increasing drought stress. In the present study we slowly desiccated D. octaedra cocoons to simulate ecologically realistic drought conditions and the results clearly demonstrate that gradually dehydrated cocoons show an increased tolerance of extreme drought compared with acutely dehydrated cocoons. NMR spectroscopic analysis of compatible osmolytes revealed the presence of sorbitol, glucose, betaine, alanine and mannitol in dehydrated embryos. The superior drought survival of gradually desiccated embryos could partly be attributed to a higher accumulation of osmolytes (especially sorbitol). Thus, gradually and acutely desiccated embryos accumulated approximately 2 mol l(-1) and 1 mol l(-1) total osmolytes, respectively. However, in addition to osmolyte accumulation, the gradually desiccated cocoons also tolerated a higher degree of water loss, demonstrating that gradually dehydrated D. octaedra cocoons are able to survive loss of approximately 95% of the original water content. Although D. octaedra embryos can probably not be categorized as a truly anhydrobiotic organism we propose that they belong in a transition zone between the desiccation sensitive and the truly anhydrobiotic organisms. Clearly, these earthworm embryos share many physiological traits with anhydrobiotic organisms.

U2 - 10.1242/jeb.017558

DO - 10.1242/jeb.017558

M3 - Journal article

VL - 211

SP - 1903

EP - 1910

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - Pt 12

ER -