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Trehalose in Bdelloids

Trehalose chromatogram
Carbohydrate analysis by gas chromatography. (a) Dried nematode A. avenae extract containing glucose and accumulated trehalose. (b) Dried rotifer P. roseola extract containing glucose, but no trehalose or other disaccharide. Glucose is represented by the doublet of peaks emerging at 7 min, while trehalose gives a single peak at 13 min. From Lapinski & Tunnacliffe (2003); Caprioli et al. (2004) and McGee (2006) have similar findings with other bdelloid species.
The accumulation of non-reducing disaccharides such as trehalose (in nematodes and yeast) and sucrose (in plants) is thought to be crucial in some organisms for survival of desiccation (Crowe et al. 1998; Clegg 2001). However, three strands of evidence from our laboratory suggest that non-reducing disaccharides might not be essential for anhydrobiosis.

First, in yeast, trehalose biosynthesis can be abolished with only a limited effect on desiccation tolerance (Ratnakumar & Tunnacliffe 2006).

Second, in three species of bdelloid rotifer, no trehalose is produced during drying (see figure); furthermore, no copies of the tps genes which govern trehalose biosynthesis in other eukaryotes have been found (Lapinski & Tunnacliffe 2003; McGee 2006). Similar results have been reported by Caprioli et al. (2004) in a fourth species. This suggests that bdelloids employ desiccation tolerance mechanisms which do not include trehalose accumulation.

Third, genetically engineered human cells which produce trehalose show no improvement in desiccation tolerance, although they are better able to cope with osmotic stress (García de Castro & Tunnacliffe 2000).

Thus, although non-reducing disaccharides may be present in large quantities in some anhydro-organisms – up to 20% dry weight in some nematodes, for example – they probably only represent part of the toolkit used to resist desiccation and in some organisms they seem not to be needed at all.

The desiccome:

One conclusion of this work might be that there are a number of different strategies used in nature to ensure desiccation tolerance. Malcolm Potts coined the term “desiccome” to describe those adaptations needed for anhydrobiosis (Potts et al. 2005). Although different organisms seem to employ different strategies, we might nevertheless ask whether there is a “minimal desiccome”, i.e. a set of adaptations which all anhydro-organisms use. Work in several laboratories around the world is now focused on identifying components of the desiccome in various organisms.


Bdelloid Rotifer Research Topics:


References:

Caprioli, M., Krabbe Katholm, A., Melone, G., Ramløv, H., Ricci, C. and Santo, N. (2004) Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species. Comp Biochem Physiol A Mol Integr Physiol. 139: 527-532

Clegg, J. S. (2001) Cryptobiosis--a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol. 128: 613-624.

Crowe, J. H., Carpenter, J. F. and Crowe, L. M.(1998) The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60: 73-103.

García de Castro, A. and Tunnacliffe, A.(2000) Intracellular trehalose improves osmotolerance but not desiccation tolerance in mammalian cells. FEBS Lett. 487: 199-202.

Lapinski, J. and Tunnacliffe, A.(2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett. 553: 387-390.

McGee, B., K. (2006) Hydrophillic proteins in the anhydrobiosis of bdelloid rotifers. Ph.D. thesis, Institute of Biotechnology, University of Cambridge.

Potts M., Slaughter S. M., Hunneke F.-U., Garst J. F. and Helm R. F. (2005) Desiccation tolerance of prokaryotes: application of principles to human cells. Integr. Comp. Biol. 45: 800-809.

Ratnakumar, S. and Tunnacliffe, A. (2006) Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast. FEMS Yeast Res 6: 902-913.