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First published online February 27, 2009
Journal of Experimental Biology 212, 859-866 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.026864

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Dual roles of glucose in the freeze-tolerant earthworm Dendrobaena octaedra: cryoprotection and fuel for metabolism

Sofia Calderon^1,2, Martin Holmstrup¹, Peter Westh³ and Johannes Overgaard^1,2,*

¹ National Environmental Research Institute, University of Aarhus, Department of Terrestrial Ecology, Vejlsøvej 25, PO Box 314, DK-8600 Silkeborg, Denmark
² Department of Zoophysiology, Institute of Biological Sciences, University of Aarhus, Building 540, DK-8000 Aarhus, Denmark
³ NSM, Research Unit for Functional Biomaterials, Roskilde University, Roskilde, Denmark

^* Author for correspondence (e-mail: biojo{at}biology.au.dk)

Accepted 7 January 2009

Ectothermic animals inhabiting the subarctic and temperate regions have evolved strategies to deal with periods of continuous frost during winter. The earthworm Dendrobaena octaedra is freeze tolerant and accumulates large concentrations of glucose upon freezing. The present study investigates the roles of glucose accumulation for long-term freeze tolerance in worms kept frozen at –2°C for 47 days. During this period, worms were sampled periodically for determination of survival and for measurements of glucose, glycogen, lactate, alanine and succinate. In addition we performed calorimetric measurements to assess metabolic rate of frozen and unfrozen worms. Long-term freezing was associated with a gradual depletion of glucose and worms that succumbed during this period were always characterised by low glucose and glycogen levels. The anaerobic waste products lactate and alanine increased slightly whereas succinate levels remained constant. However, it is argued that other waste products (particularly propionate) could be the primary end product of a continued anaerobic metabolism. Calorimetric measures of the metabolic rate of frozen worms were in accord with values calculated from the reduction in glucose assuming that most (90%) glucose was metabolised anaerobically. Both estimates of metabolic rate demonstrated a 10-fold metabolic depression associated with freezing. Thus, in addition to the suspected role of glucose as cryoprotectant, the present study demonstrates that glucose accumulation is vital to ensure substrate for long-term anaerobic metabolism in frozen worms. On the basis of the estimated metabolite levels, we calculate that the combined effect of metabolic depression and large glucose stores enables a projected 3 months survival of freezing at –2°C of the `average' D. octaedra. Such conditions are very likely to occur in the northern distribution ranges of this stress-tolerant earthworm.

Key words: cryoprotectant, glucose, anoxia, anaerobic metabolism, freeze survival

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