• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of transbhomepageaboutsubmitalertseditorial board
Philos Trans R Soc Lond B Biol Sci. Oct 29, 2003; 358(1438): 1755–1771.
PMCID: PMC1693263

Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis.

Abstract

In 1702, Van Leeuwenhoek was the first to describe the phenomenon of anhydrobiosis in a species of bdelloid rotifer, Philodina roseola. It is the purpose of this review to examine what has been learned since then about the extreme desiccation tolerance in rotifers and how this compares with our understanding of anhydrobiosis in other organisms. Remarkably, much of what is known today about the requirements for successful anhydrobiosis, and the degree of biostability conferred by the dry state, was already determined in principle by the time of Spallanzani in the late 18th century. Most modern research on anhydrobiosis has emphasized the importance of the non-reducing disaccharides trehalose and sucrose, one or other sugar being present at high concentrations during desiccation of anhydrobiotic nematodes, brine shrimp cysts, bakers' yeast, resurrection plants and plant seeds. These sugars are proposed to act as water replacement molecules, and as thermodynamic and kinetic stabilizers of biomolecules and membranes. In apparent contradiction of the prevailing models, recent experiments from our laboratory show that bdelloid rotifers undergo anhydrobiosis without producing trehalose or any analogous molecule. This has prompted us to critically re-examine the association of disaccharides with anhydrobiosis in the literature. Surprisingly, current hypotheses are based almost entirely on in vitro data: there is very limited information which is more than simply correlative in the literature on living systems. In many species, disaccharide accumulation occurs at approximately the same time as desiccation tolerance is acquired. However, several studies indicate that these sugars are not sufficient for anhydrobiosis; furthermore, there is no conclusive evidence, through mutagenesis or functional knockout experiments, for example, that sugars are necessary for anhydrobiosis. Indeed, some plant seeds and micro-organisms, like the rotifer, exhibit excellent desiccation tolerance in the absence of high intracellular sugar concentrations. Accordingly, it seems appropriate to call for a re-evaluation of our understanding of anhydrobiosis and to embark on new experimental programmes to determine the key molecular mechanisms involved.

Full Text

The Full Text of this article is available as a PDF (571K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aguilera JM, Karel M. Preservation of biological materials under desiccation. Crit Rev Food Sci Nutr. 1997 Apr;37(3):287–309. [PubMed]
  • Arakawa T, Timasheff SN. Stabilization of protein structure by sugars. Biochemistry. 1982 Dec 7;21(25):6536–6544. [PubMed]
  • Argüelles JC. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol. 2000 Oct;174(4):217–224. [PubMed]
  • Bartels D, Salamini F. Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol. 2001 Dec;127(4):1346–1353. [PMC free article] [PubMed]
  • Battista JR, Park MJ, McLemore AE. Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology. 2001 Sep;43(2):133–139. [PubMed]
  • Blackman SA, Obendorf RL, Leopold AC. Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiol. 1992 Sep;100(1):225–230. [PMC free article] [PubMed]
  • Blázquez MA, Santos E, Flores CL, Martínez-Zapater JM, Salinas J, Gancedo C. Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J. 1998 Mar;13(5):685–689. [PubMed]
  • Bloom FR, Price P, Lao G, Xia JL, Crowe JH, Battista JR, Helm RF, Slaughter S, Potts M. Engineering mammalian cells for solid-state sensor applications. Biosens Bioelectron. 2001 Sep;16(7-8):603–608. [PubMed]
  • Bolen DW, Baskakov IV. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol. 2001 Jul 27;310(5):955–963. [PubMed]
  • Cerrutti P, Segovia de Huergo M, Galvagno M, Schebor C, del Pilar Buera M. Commercial baker's yeast stability as affected by intracellular content of trehalose, dehydration procedure and the physical properties of external matrices. Appl Microbiol Biotechnol. 2000 Oct;54(4):575–580. [PubMed]
  • Chen T, Acker JP, Eroglu A, Cheley S, Bayley H, Fowler A, Toner M. Beneficial effect of intracellular trehalose on the membrane integrity of dried mammalian cells. Cryobiology. 2001 Sep;43(2):168–181. [PubMed]
  • CLEGG JS. THE ORIGIN OF TREHALOSE AND ITS SIGNIFICANCE DURING THE FORMATION OF ENCYSTED DORMANT EMBRYOS OF ARTEMIA SALINA. Comp Biochem Physiol. 1965 Jan;14:135–143. [PubMed]
  • Clegg JS. Cryptobiosis--a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol. 2001 Apr;128(4):613–624. [PubMed]
  • Clegg JS, Seitz P, Seitz W, Hazlewood CF. Cellular responses to extreme water loss: the water-replacement hypothesis. Cryobiology. 1982 Jun;19(3):306–316. [PubMed]
  • Colaço C, Sen S, Thangavelu M, Pinder S, Roser B. Extraordinary stability of enzymes dried in trehalose: simplified molecular biology. Biotechnology (N Y) 1992 Sep;10(9):1007–1011. [PubMed]
  • Crowe JH, Hoekstra FA, Crowe LM. Anhydrobiosis. Annu Rev Physiol. 1992;54:579–599. [PubMed]
  • Crowe JH, Carpenter JF, Crowe LM. The role of vitrification in anhydrobiosis. Annu Rev Physiol. 1998;60:73–103. [PubMed]
  • Crowe JH, Crowe LM, Oliver AE, Tsvetkova N, Wolkers W, Tablin F. The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. Cryobiology. 2001 Sep;43(2):89–105. [PubMed]
  • Crowe LM, Crowe JH. Anhydrobiosis: a strategy for survival. Adv Space Res. 1992;12(4):239–247. [PubMed]
  • Eleutherio EC, Araujo PS, Panek AD. Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae. Biochim Biophys Acta. 1993 Mar 21;1156(3):263–266. [PubMed]
  • Eleutherio EC, Maia FM, Pereira MD, Degré R, Cameron D, Panek AD. Induction of desiccation tolerance by osmotic treatment in Saccharomyces uvarum var. carlsbergensis. Can J Microbiol. 1997 May;43(5):495–498. [PubMed]
  • Nockrashy AS El-, Frampton VL. Destruction of lysine by nonreducing sugars. Biochem Biophys Res Commun. 1967 Sep 7;28(5):675–681. [PubMed]
  • Estruch F. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev. 2000 Oct;24(4):469–486. [PubMed]
  • Ford BJ. The van Leeuwenhoek specimens. Notes Rec R Soc Lond. 1981;36(1):37–59. [PubMed]
  • Gaff DF. Desiccation-tolerant flowering plants in southern Africa. Science. 1971 Dec 3;174(4013):1033–1034. [PubMed]
  • García de Castro A, Tunnacliffe A. Intracellular trehalose improves osmotolerance but not desiccation tolerance in mammalian cells. FEBS Lett. 2000 Dec 29;487(2):199–202. [PubMed]
  • García De Castro A, Bredholt H, Strøm AR, Tunnacliffe A. Anhydrobiotic engineering of gram-negative bacteria. Appl Environ Microbiol. 2000 Sep;66(9):4142–4144. [PMC free article] [PubMed]
  • de Castro AG, Lapinski J, Tunnacliffe A. Anhydrobiotic engineering. Nat Biotechnol. 2000 May;18(5):473–473. [PubMed]
  • Gordon SL, Oppenheimer SR, Mackay AM, Brunnabend J, Puhlev I, Levine F. Recovery of human mesenchymal stem cells following dehydration and rehydration. Cryobiology. 2001 Sep;43(2):182–187. [PubMed]
  • Grably Melanie R, Stanhill Ariel, Tell Osnat, Engelberg David. HSF and Msn2/4p can exclusively or cooperatively activate the yeast HSP104 gene. Mol Microbiol. 2002 Apr;44(1):21–35. [PubMed]
  • Caiola MG, Ocampo-Friedmann R, Friedmann EI. Cytology of long-term desiccation in the desert cyanobacterium Chroococcidiopsis (Chroococcales). Phycologia. 1993;32(5):315–322. [PubMed]
  • Guo N, Puhlev I, Brown DR, Mansbridge J, Levine F. Trehalose expression confers desiccation tolerance on human cells. Nat Biotechnol. 2000 Feb;18(2):168–171. [PubMed]
  • Hengge-Aronis Regine. Recent insights into the general stress response regulatory network in Escherichia coli. J Mol Microbiol Biotechnol. 2002 May;4(3):341–346. [PubMed]
  • Hershkovitz N, Oren A, Cohen Y. Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl Environ Microbiol. 1991 Mar;57(3):645–648. [PMC free article] [PubMed]
  • Hoekstra FA, Golovina EA, Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 2001 Sep;6(9):431–438. [PubMed]
  • Hottiger T, Boller T, Wiemken A. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett. 1987 Aug 10;220(1):113–115. [PubMed]
  • Ingram J, Bartels D. THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):377–403. [PubMed]
  • KEILIN D. The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B Biol Sci. 1959 Mar 17;150(939):149–191. [PubMed]
  • Kleines M, Elster RC, Rodrigo MJ, Blervacq AS, Salamini F, Bartels D. Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum (Hochst.). Planta. 1999 Jul;209(1):13–24. [PubMed]
  • LEA CH, HANNAN RS, GREAVES RIN. The reaction between proteins and reducing sugars in the 'dry' state; dried human blood plasma. Biochem J. 1950 Nov-Dec;47(5):626–629. [PMC free article] [PubMed]
  • Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol. 1995 Oct;61(10):3592–3597. [PMC free article] [PubMed]
  • Linders LJ, Wolkers WF, Hoekstra FA, van 't Riet K. Effect of added carbohydrates on membrane phase behavior and survival of dried Lactobacillus plantarum. Cryobiology. 1997 Aug;35(1):31–40. [PubMed]
  • Mansell JL, Clegg JS. Cellular and molecular consequences of reduced cell water content. Cryobiology. 1983 Oct;20(5):591–612. [PubMed]
  • Manzanera M, García de Castro A, Tøndervik A, Rayner-Brandes M, Strøm AR, Tunnacliffe A. Hydroxyectoine is superior to trehalose for anhydrobiotic engineering of Pseudomonas putida KT2440. Appl Environ Microbiol. 2002 Sep;68(9):4328–4333. [PMC free article] [PubMed]
  • Mattimore V, Battista JR. Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol. 1996 Feb;178(3):633–637. [PMC free article] [PubMed]
  • Nickle David C, Learn Gerald H, Rain Matthew W, Mullins James I, Mittler John E. Curiously modern DNA for a "250 million-year-old" bacterium. J Mol Evol. 2002 Jan;54(1):134–137. [PubMed]
  • Oliver AE, Leprince O, Wolkers WF, Hincha DK, Heyer AG, Crowe JH. Non-disaccharide-based mechanisms of protection during drying. Cryobiology. 2001 Sep;43(2):151–167. [PubMed]
  • Ooms JJJ, Leon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM. Acquisition of Desiccation Tolerance and Longevity in Seeds of Arabidopsis thaliana (A Comparative Study Using Abscisic Acid-Insensitive abi3 Mutants). Plant Physiol. 1993 Aug;102(4):1185–1191. [PMC free article] [PubMed]
  • Ophir T, Gutnick DL. A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol. 1994 Feb;60(2):740–745. [PMC free article] [PubMed]
  • Perry RN. Desiccation survival of parasitic nematodes. Parasitology. 1999;119 (Suppl):S19–S30. [PubMed]
  • Potts M. Desiccation tolerance of prokaryotes. Microbiol Rev. 1994 Dec;58(4):755–805. [PMC free article] [PubMed]
  • Potts M. Desiccation tolerance: a simple process? Trends Microbiol. 2001 Nov;9(11):553–559. [PubMed]
  • Puhlev I, Guo N, Brown DR, Levine F. Desiccation tolerance in human cells. Cryobiology. 2001 May;42(3):207–217. [PubMed]
  • Ruis H, Schüller C. Stress signaling in yeast. Bioessays. 1995 Nov;17(11):959–965. [PubMed]
  • Sano F, Asakawa N, Inoue Y, Sakurai M. A dual role for intracellular trehalose in the resistance of yeast cells to water stress. Cryobiology. 1999 Aug;39(1):80–87. [PubMed]
  • Schebor C, Galvagno M, del Pilar Buera M, Chirife J. Glass transition temperatures and fermentative activity of heat-treated commercial active dry yeasts. Biotechnol Prog. 2000 Mar-Apr;16(2):163–168. [PubMed]
  • Singer MA, Lindquist S. Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell. 1998 Apr;1(5):639–648. [PubMed]
  • Timasheff SN. Water as ligand: preferential binding and exclusion of denaturants in protein unfolding. Biochemistry. 1992 Oct 20;31(41):9857–9864. [PubMed]
  • Tunnacliffe A, García de Castro A, Manzanera M. Anhydrobiotic engineering of bacterial and mammalian cells: is intracellular trehalose sufficient? Cryobiology. 2001 Sep;43(2):124–132. [PubMed]
  • Vogel G, Aeschbacher RA, Müller J, Boller T, Wiemken A. Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J. 1998 Mar;13(5):673–683. [PubMed]
  • Vreeland RH, Rosenzweig WD, Powers DW. Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature. 2000 Oct 19;407(6806):897–900. [PubMed]
  • White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, Haft DH, Gwinn ML, Nelson WC, Richardson DL, et al. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science. 1999 Nov 19;286(5444):1571–1577. [PubMed]
  • Winderickx J, de Winde JH, Crauwels M, Hino A, Hohmann S, Van Dijck P, Thevelein JM. Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Mol Gen Genet. 1996 Sep 25;252(4):470–482. [PubMed]
  • Wolkers WF, Walker NJ, Tablin F, Crowe JH. Human platelets loaded with trehalose survive freeze-drying. Cryobiology. 2001 Mar;42(2):79–87. [PubMed]
  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. Living with water stress: evolution of osmolyte systems. Science. 1982 Sep 24;217(4566):1214–1222. [PubMed]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...