Constraints of tolerance: why are desiccation-tolerant organisms so small or rare?

Abstract

Drying to equilibrium with the air kills nearly all animals and flowering plants, including livestock and crops. This makes drought a key ecological problem for terrestrial life and a major cause of human famine. However, the ability to tolerate complete desiccation is widespread in organisms that are either <5·mm long or found mainly where desiccation-sensitive organisms are scarce. This suggests that there is a trade-off between desiccation tolerance and growth. Recent molecular and biochemical research shows that organisms tolerate desiccation through a set of mechanisms, including sugars that replace water and form glasses, proteins that stabilize macromolecules and membranes, and anti-oxidants that counter damage by reactive oxygen species. These protections are often induced by drying, and some of the genes involved may be homologous in microbes, plants and animals. Understanding how mechanisms of desiccation tolerance may constrain growth might show how to undo the constraint in some economically important macroorganisms and elucidate the muchstudied but elusive relationship between tolerance of stress and productivity.Key words: animal, desiccation, drought, growth, microbe, plant, productivity, tolerance, trade-off. SummaryThe potential of -100·MPa. These thresholds also clearly separate desiccation-sensitive from -tolerant species (Alpert, 2005): there is a gap in the minimum water contents that different living things can survive. Except for a small proportion of seeds (Tweddle et al., 2003), almost all species tested either die if dried to 20% water content, and are thus desiccationsensitive, or survive drying to 10% water content and thus tolerate desiccation. It should be noted that 'desiccation tolerance' has sometimes been used to mean tolerance of partial desiccation by organisms that die if they desiccate completely, as in the literature on insects and intertidal algae. Here, the term will be used to mean tolerance of complete desiccation, defined as drying to equilibrium with moderately to very dry air, or to 10% water content or less.A prime secret of desiccation tolerance appears to be sugars (Alpert and Oliver, 2002). Certain sugars, mainly nonreducing disaccharides, may take the place of water in preventing the aggregation of macromolecules and the disintegration of membranes as cells dry. Many tolerant plants accumulate high concentrations of the familiar disaccharide sucrose (Vicre et al., 2004a). Many desiccation-tolerant animals and microbes and also some plants synthesize the disaccharide trehalose (Wingler, 2002;Breeuwer et al., 2003;Elbein et al., 2003;Crowe et al., 2005). In tandem with specific proteins (Goyal et al., 2005b), these sugars probably stabilize drying cells both by direct interaction with macromolecules and membranes and by reversibly immobilizing cytoplasm in an extremely slow-flowing liquid, a glass (Buitink and Leprince, 2004). Interestingly, sugar glasses also tend to form at the threshold of 10% water content, at least in seeds (Walters et al., 2005).Researchers ...

Ecophysiological performance of an urban strain of the aeroterrestrial green algaKlebsormidiumsp. (Klebsormidiales, Klebsormidiophyceae)

“…appears rather sensitive; this seems to be in agreement with the type of habitat where this strain and other strains with identical rbcL sequence were collected (urban walls and corners, mainly in northern European cities, at sites sheltered from direct sunlight most of the time; Rindi et al, 2008). Although some physiological data on desiccation in algae exist, the underlying mechanisms are not fully understood (Alpert, 2006). In contrast, the terrestrial cyanobacterium Nostoc commune has been developed as an excellent prokaryotic model system to understand desiccation and other stress tolerances at the biochemical and molecular level (Potts, 1999;Wright et al, 2005).…”

Physiological, cellular and molecular aspects of the desiccation tolerance in Anadenanthera colubrina seeds during germination

“…Water is essential for life, however, some structures, such as seeds, are known for their ability to tolerate dehydration to a low moisture content and retake metabolism after rehydration (Alpert, 2006). These seeds are called orthodox seeds and desiccation is a stage of their development.…”

Long-term experimental manipulation of moisture conditions and its impact on moss-living tardigrades

“…High densities of desiccation-tolerant organisms in dry habitats could reflect a trade-off between competitiveness and desiccation tolerance (Alpert 2006), such that desiccation tolerant populations are released from non-desiccation tolerant competitors in the dry habitats. Kinchin (1992Kinchin ( , 1994 discussed the possibility that drying out of the substrate may be positive for tardigrade populations by reducing the density of fungi in the substrate.…”