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The Society for Integrative and Comparative Biology
Sharing the Secrets of Life Without Water
1 University of Massachusetts–Amherst
Water and life are inseparable. No known living thing can function without water, and there is life wherever there is water on Earth (Rothschild and Mancinelli, 2001
). One of the greatest problems of living on land is thus that the air is almost always deadly dry. For example, at equilbrium with air of 50% relative humidity at 20°C, cells have a water content of about 0.1 g H2O g–1 dry mass. This is probably not enough water to surround the proteins and membranes in a cell (Billi and Potts, 2002) and so stops metabolism and kills almost all animals and plants.
However, a very few animals, a few plants, and an unknown proportion of microbes can be separated from water for a time. They can dry without dying, survive for hours to decades in a desiccated, ametabolic state, and then recover full function after rewetting. They are either small or found mainly where few other organisms can survive. Though still little-known even among biologists, this general taxonomic and ecological scope of desiccation tolerance was well-established a half-century ago (Alpert, 2000). What has awaited answer with more modern techniques are the twin puzzles raised by the prodigious survival yet modest distribution of desiccation-tolerant organisms: How do they tolerate desiccation? and Why are they not more common?
These were therefore the two central topics of the symposium on "the comparative mechanisms and evolution of desiccation tolerance in animals, microbes, and plants," held at the 2005 meeting of the Society for Integrative Biology. This was the first symposium since the advent of molecular genetics to compare all three groups of desiccation-tolerant organisms, and assembled researchers from four continents and from disciplines ranging from ecology to biophysics.
The first six papers consider the mechanisms of desiccation tolerance, how tolerance is achieved. Bartels (this issue) reviews evidence for the importance of sugars, protective proteins, and regulatory genes in stabilization in the desiccation-tolerant flowering plant, Craterostigma plantigineum.During desiccation, the nematode Aphelenchus avenae upregulates genes that encode some unique proteins but also some members of a protein family associated with tolerance in plants (Goyal et al., this issue). Kikawada et al. (this issue) note the importance of sugar synthesis during drying in inducing tolerance in the larva of the fly Polypedilum vanderplanki; in this species, a behavioral response that slows drying appears to help ensure time for synthesis. Clegg (this issue) reviews the biochemistry and biophysics associated with desiccation tolerance in the crustacean, Artemia franciscana, and presents new data on related tolerance of heat.
Negative correlation between the length of desiccation that seeds and spores can survive and the number of double bonds in the acyl chains of the lipids in their membranes indicates that deterioration of membranes limits the longevity of plants in the desiccated state and that lipid composition is important (Hoekstra, this issue). Kranner and Birti
(this issue) emphasize the importance of anti-oxidants as scavengers of free radicals that cause oxidation damage during desiccation; the major anti-oxidant glutathione may trigger programmed cell death if not itself re-reduced. These papers suggest that all desiccation tolerance relies mainly on a small set of mechanisms that stabilize macromolecules and membranes as cells dry and that protect cells from damage while dry. However, the details of the mechanisms differ between species.
The second six papers explore the evolution and ecology of desiccation-tolerant animals and plants: how does tolerance affect fitness and when is it selected for? Treonis and Wall (this issue) show that nematodes in the soil of Antarctica may have only rare, brief periods of activity when soil moisture is high. Walters et al. (this issue) report evidence that mild temperature and moderate humidity reduce the longevity of desiccated organisms. Ricci and Caprioli (this issue) find no obvious metabolic cost of desiccation cycles in rotifers, and present evidence that they do not age while desiccated, but note that terrestrial rotifers, in which tolerance is obligate, tend to have lower fecundity than aquatic ones. Jönsson (this issue) reports a similar link between low fecundity and tolerance in tardigrades, and a link with large egg size.
One reason why tolerance in plants may be more easily evolved than in animals is that genes necessary for tolerance are conserved through selection on seeds and spores. Comparison between the molecular biology and physiology of tolerance in seeds and vegetative tissues in angiosperms supports the hypothesis that the second is derived from the first (Illing et al., this issue). Tolerance in adult bryophytes may likewise be derived from tolerance in spores (Oliver et al., this issue). Together, these papers tend to support the general view that avoiding desiccation when possible may lead to greater productivity than tolerating it, causing tolerance to be lost through evolution when not essential.
Understanding the mechanisms and evolution of tolerance enables us to ask a third, more self-interested question: Can we engineer it? None of the animals or plants raised by humans for food can tolerate desiccation, and drought is probably the major environmental cause of famine worldwide. Supplies of blood and other human cells for medical use are strongly limited by their short storage life while fresh. Can we engineer tolerance in sensitive species or cells? The last three papers examine the prospects for creating desiccation tolerance. Crowe et al. (this issue) describe how the main sugar involved in tolerance in animals, trehalose, has been successfully used to induce tolerance in human blood platelets, and how borrowing a stress protein from Artemia has helped improve tolerance in nucleated cells. Based on a comparison between responses to drying in prokaryotic and eukaryotic cells, Potts et al. (this issue) propose that "a common set of structural, physiological and molecular mechanisms" for desiccation tolerance may lead us to the designs for extending tolerance to sensitive cells. Alpert (this issue) seconds this hopeful prognosis for single cells and calls for a further focus on trade-offs between tolerance and productivity.
The symposium was generously supported by the Society, the U.S. Department of Agriculture, the National Science Foundation, and grants to individual participants from their home institutions and other societies and agencies. Thanks to the symposium participants and to the editorial staff of ICB, the immediate result is this issue.
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Alpert, P. 2000. The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecology, 151:5-17.[CrossRef]
Billi, D., and M. Potts. 2002. Life and death of dried prokaryotes. Research in Microbiology, 153:7-12.[Medline]
Rothschild, L. J., and R. L. Mancinelli. 2001. Life in extreme environments. Nature, 409:1092-1101.[CrossRef][Medline]
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