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.

Dehydration-induced tps gene transcripts from an anhydrobiotic nematode contain novel spliced leaders and encode atypical GT-20 family proteins

“…[1]). Although trehalose levels do not always correlate strongly with anhydrobiotic potential in a number of organisms [1,4,33,34], the prevailing hypotheses which attempt to explain anhydrobiosis all involve non-reducing disaccharides in some capacity. Despite this prominence, the current study is the first to examine the genetics of trehalose synthesis in an anhydrobiotic animal.…”

“…Members of three invertebrate taxa, bdelloid rotifers, tardigrades and nematodes, can undergo anhydrobiosis at all stages of the life cycle; other invertebrates have stage-specific anhydrobiotic forms (reviewed in Ref. [1]). The molecular mechanisms governing anhydrobiosis are not well understood, but there is considerable interest in the role of the non-reducing disaccharides trehalose (in animals and fungi) and sucrose (in plants).…”

“…For instance, when Aphelenchus avenae, a soildwelling fungivorous nematode amenable to laboratory culture, is dried slowly to induce anhydrobiosis, it converts up to 20% of its dry weight to trehalose and this correlates with acquisition of desiccation tolerance [2,3], albeit somewhat loosely [4]. Surprisingly, however, bdelloid rotifers seem unable to produce trehalose at all [5], although their anhydrobiotic capability is well established [1]. Nevertheless, the importance of non-reducing disaccharides has been stressed repeatedly, since it is well known that such sugars are able to stabilise dried proteins and membrane systems in vitro and it is widely assumed they have similar stabilising properties in vivo [6].…”

Improved tolerance to salt and water stress in Drosophila melanogaster cells conferred by late embryogenesis abundant protein

“…A recurring strategy in animals to tolerate extreme water loss is the expression of LEA proteins with or without the concurrent accumulation of large amounts of the non-reducing disaccharide trehalose (Goyal et al, 2005;Hand et al, 2011;Oliver et al, 2001;Tunnacliffe and Lapinski, 2003;Watanabe et al, 2005). LEA proteins were first described about 30 years ago in desiccation tolerant cotton seeds at maturation (Dure and Galau, 1981;Galau, 1986) and were thought to be unique to plants.…”

Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses

“…Trehalose appears to be better than other biological sugars in forming a protective vitrified state (Crowe et al, 1998). Trehalose also is a nonreducing sugar, which, unlike glucose and some other monosaccharides, does not engage in 'browning' (Maillard) reactions that can damage proteins during drying (reviewed by Tunnacliffe and Lapinski, 2003).…”