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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

View larger version (7K): [in this window] [in a new window]   Fig. 1. Soil temperature at 5 cm depth, Disko Island, Greenland (July 2006–June 2007). Several adult worms survived the entire experimental period in field containers placed next to the temperature loggers. The brief increase to 0°C in late January is uncommon at Disko where the soil usually remains frozen for nearly 6 months.

View larger version (4K): [in this window] [in a new window]   Fig. 2. Freeze mortality rate (%) of D. octaedra during exposure to frost for 3–47 days. Points represent average mortality at the individual time points (N=13–20). The line shows the linear regression of the entire data set.

View larger version (14K): [in this window] [in a new window]   Fig. 3. Glucose (A) and glycogen (B) content in surviving D. octaedra during frost (solid line, white circles) and untreated control (dashed line and grey triangles). Dead worms were not included. Worms were frozen at –2°C for up to 47 days. Lines show the linear regression (slope and statistical significance are presented in the top right corner).

View larger version (18K): [in this window] [in a new window]   Fig. 4. Lactate (A), alanine (B) and succinate (C) in surviving D. octaedra during frost (solid line, white circles) and untreated control (dashed line and grey triangles). Dead worms were not included. Worms were frozen at –2°C for up to 47 days. Lines show the linear regression (slope and statistical significance are presented in the top right corner).

View larger version (27K): [in this window] [in a new window]   Fig. 5. Metabolic rate of frozen and unfrozen D. octaedra estimated from respirometry and production of anaerobic metabolites or from heat production. (A) ATP consumption rates at 10 and 5°C were calculated from previously published measurements of oxygen consumption rates (Uvarov, 1998) using the assumption that each mole of O2 generates 6 ATP. The hatched bar depicts ATP consumption rate of unfrozen and aerobic worms at –2°C as estimated using a Q10 of 2.43 (from Uvarov's data). ATP consumption rate of frozen D. octaedra at –2°C are calculated from the temporal decrease in glucose shown in Fig. 3 using different assumptions regarding the proportion of anaerobic/aerobic metabolism and different assumptions of ATP yield per glucose molecule (see text for further explanation). (B) Metabolic rate of frozen and unfrozen D. octaedra measured directly by calorimetry. The hatched bar depicts ATP consumption rate of unfrozen and aerobic worms at –2°C as estimated using a Q10 of 3.76 (from calorimetric data).

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