Molecular Anhydrobiology: Identifying Molecules Implicated in Invertebrate Anhydrobiosis

Abstract

Studies in anhydrobiotic plants have defined many genes which are upregulated during desiccation, but comparable studies in invertebrates are at an early stage. To develop a better understanding of invertebrate anhydrobiosis, we have begun to characterise dehydration-inducible genes and their proteins in anhydrobiotic nematodes and bdelloid rotifers; this review emphasises recent findings with a hydrophilic nematode protein. Initial work with the fungivorous nematode Aphelenchus avenae led to the identification of two genes, both of which were markedly induced on slow drying (90-98% relative humidity, 24 hr) and also by osmotic stress, but not by heat or cold or oxidative stresses. The first of these genes encodes a novel protein we have named anhydrin; it is a small, basic polypeptide, with no counterparts in sequence databases, which is predicted to be natively unstructured and highly hydrophilic. The second is a member of the Group 3 LEA protein family; this and other families of LEA proteins are widely described in plants, where they are most commonly associated with the acquisition of desiccation tolerance in maturing seeds. Like anhydrin, the nematode LEA protein, Aav-LEA-1, is highly hydrophilic and a recombinant form has been shown to be unstructured in solution. In vitro functional studies suggest that Aav-LEA-1 is able to stabilise other proteins against desiccation-induced aggregation, which is in keeping with a role of LEA proteins in anhydrobiosis. In vivo, however, Aav-LEA-1 is apparently processed into smaller forms during desiccation. A processing activity was found in protein extracts of dehydrated, but not hydrated, nematodes; these shorter polypeptides are also active anti-aggregants and we hypothesise that processing LEA protein serves to increase the number of active molecules available to the dehydrating animal. Other LEA-like proteins are being identified in nematodes and it seems likely therefore that they will play a major role in the molecular anhydrobiology of invertebrates, as they are thought to do in plants.

The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon

“…The effectiveness of LEA-protein may be increased by its greater tertiary structure at the high solute concentrations in airdry tissue (Goyal et al 2005a(Goyal et al , 2005b. A LEA-like protein in Craterostigma plantagineum binds to two enzymes, stabilising their activity after repeated cycles of dehydration (Petersen et al 2012).…”

Genetic Analysis of Desiccation Tolerance inSaccharomyces cerevisiae

“…Indeed, several potential stress-response molecules and pathways appear to be induced in the desiccation-tolerant state of desiccation-tolerant seeds and extremophiles (Goyal et al 2005). One class of induced molecules consists of nonreducing disaccharides such as trehalose and sucrose.…”

Identification of the trehalose-6-phosphate synthase (tps) gene in desiccation tolerant and intolerant tardigrades

“…By using a modified protocol of Lapinski and Tunnacliffe (2003), we sequenced a 574 bp portion coding for a glycosyltransferase, similar to genes responsible for trehalose-6-phosphate synthase (TPS) present in GenBank and the literature (Leloir & Cabib 1953;Cabib & Leloir 1958;Candy & Kilby 1958;Murphy & Wyatt 1965;Blàzquez et al 1998;Zentella et al 1999;Pellerone et al 2003;Goyal et al 2005b;Chung 2008).…”

“…As it has become more and more evident in several desiccation tolerant organisms, the anhydrobiotic ability is bound to a complex system that involves many different molecular components working together as bioprotectants, such as disaccharides, heat shock proteins and late embryogenesis abundant proteins (Goyal et al 2005b). One of the widespread molecules that is claimed to be involved in anhydrobiosis is the non-reducing disaccharide trehalose (Clegg 2001).…”