Late embryogenesis abundant (LEA) proteins are associated with desiccation tolerance in resurrection plants and in plant seeds, and the recent discovery of a dehydration-induced Group 3 LEA-like gene in the nematode Aphelenchus avenae suggests a similar association in anhydrobiotic animals. Despite their importance, little is known about the structure of Group 3 LEA proteins, although computer modeling and secondary structure algorithms predict a largely ␣-helical monomer that forms coiled coil oligomers. We have therefore investigated the structure of the nematode protein, Aav-LEA1, in the first such analysis of a well characterized Group 3 LEA-like protein. Immunoblotting and subunit cross-linking experiments demonstrate limited oligomerization of AavLEA1, but analytical ultracentrifugation and gel filtration show that the vast majority of the protein is monomeric. Moreover, CD, fluorescence emission, and Fourier transform-infrared spectroscopy indicate an unstructured conformation for the nematode protein. Therefore, in solution, no evidence was found to support structure predictions; instead, Aav-LEA1 seems to be natively unfolded with a high degree of hydration and low compactness. Such proteins can, however, be induced to fold into more rigid structures by partner molecules or by altered physiological conditions. Because AavLEA1 is associated with desiccation stress, its Fourier transform-infrared spectrum in the dehydrated state was examined. A dramatic but reversible increase in ␣-helix and, possibly, coiled coil formation was observed on drying, indicating that computer predictions of secondary structure may be correct for the solid state. This unusual finding offers the possibility that structural shifts in Group 3 LEA proteins occur on dehydration, perhaps consistent with their role in anhydrobiosis.
When subjected to drought conditions, some organisms enter a state of suspended animation known as anhydrobiosis, surviving for indefinite periods until rehydration allows them to resume normal metabolism. We have identified a gene in the anhydrobiotic nematode Aphelenchus avenae that is upregulated in response to desiccation stress and whose encoded protein shares sequence similarity with a late-embryonic gene that is induced in many plants when they are deprived of water. This finding suggests that animals and plants that undergo anhydrobiosis may use common protective strategies against dehydration, and provides a unifying insight into the mechanism of anhydrobiosis.
When environmental conditions are unsuitable to support nematode reproduction, Caenorhabditis elegans arrests development before the onset of sexual maturity and specialised 'dauer' larvae, adapted for dispersal, and extended diapause are formed. Dauer larvae do not feed and their metabolism is dependent on internal food reserves. Adult worms which express defects in the insulin/insulin-like growth factor receptor DAF-2 also display enhanced longevity. Whole genome mRNA expression profiling has demonstrated that C. elegans dauer larvae and daf-2 adults have similar transcription profiles for a cohort of longevity genes. Important components of this enhanced longevity system are the a-crystallin family of small heat shock proteins, anti-ROS defence systems, increased activity of cellular detoxification processes and possibly also increased chromatin stability and decreased protein turnover. Anaerobic fermentation pathways are upregulated in dauer larvae, while long-lived daf-2 adults appear to have normal oxidative metabolism. Anabolic pathways are down regulated in dauer larvae (and possibly in daf-2 adults as well), and energy consumption appears to be diverted to enhanced cellular maintenance and detoxification processes in both systems. q
Summary -The entomopathogenic nematodes (EPN) Heterorhabditis and Steinernema together with their symbiont bacteriaPhotorhabdus and Xenorhabdus, respectively, are obligate and lethal parasites of insects. EPN can provide effective biological control of some important lepidopteran, dipteran and coleopteran pests of commercial crops and they are amenable to large-scale culture in liquid fermentors. They are unique among rhabditids in having a symbiotic relationship with an enteric bacterium species. The bacterial symbiont is required to kill the insect host and to digest the host tissues, thereby providing suitable nutrient conditions for nematode growth and development. This review describes the general biology of EPN and their symbionts and gives an overview of studies to date on EPN biodiversity, biogeography and phylogeny. The impetus for research in EPN and their symbionts has come about because of their biological control potential, with much of the focus in EPN research having been on applied aspects relating to pest control. However EPN and their symbionts are increasingly being viewed as exciting subjects for basic research in the areas of ecology, biodiversity, evolution, biochemistry, symbiosis and molecular genetics. Much progress has been made over the past 20 years in our understanding of the basic biology and genetics of EPN and their symbionts. We are now entering a new phase in which the tools of molecular genetics are being increasingly used to address a range of biological questions in EPN research. The knowledge gained from this endeavour should ensure that EPN will become even more effective biopesticides and should also ensure that EPN and their symbionts gain prominence as unique and intrinsically interesting biological systems.Résumé -Heterorhabditis, Steinernema et leurs symbiotes bactériens -Pathogènes mortels des insectes -Les nématodes entomopathogènes (EPN) Heterorhabditis et Steinernema, avec leur bactéries symbiotes Photorhabdus et Xenorhabdus, respectivement, sont des parasites obligés et mortels des insectes. Les EPN peuvent servir à un contrôle biologique de quelques lépidoptères, diptères et coléoptères importants pour les cultures commerciales et ils sont élevables à grande échelle dans des fermenteurs liquides. Ils sont uniques chez les rhabditides par leur relation symbiotique avec une espèce de bactérie entérique. La bactérie symbiote est nécessaire pour tuer l'insecte hôte et pour digérer les tissus de l'hôte, permettant ainsi des conditons de nutrition favorables à la croissance et au développement du nématode. La présente revue décrit la biologie générale des EPN et de leur symbiotes et donne un état des études actuelles sur la biodiversité, la biogéographie et la phylogénie des EPN. L'impulsion donnée aux recherches sur les EPN et leur symbiotes provient de leur potentialités pour le contrôle biologique, une grande partie des recherches sur les EPN ayant trait à des aspects appliqués en relation avec ce contrôle des parasites. Cependant, les EPN et leur symbiotes bactérie...
SUMMARY Members of the genus Panagrolaimus are bacterial-feeding nematodes that occupy a diversity of niches ranging from Antarctic and temperate soils to terrestrial mosses. Some members of this genus are able to survive extreme desiccation by entering into a state of suspended animation known as anhydrobiosis. We have assembled a collection of Panagrolaimusspecies and strains and have investigated their anhydrobiotic phenotypes. Our data show that within the genus Panagrolaimus there is a continuum of strains ranging from those unable to survive exposure to low relative humidity(RH) without prior preconditioning at high RH (slow desiccation strategists),through strains that have limited ability to survive rapid desiccation but whose anhydrobiotic ability improves upon preconditioning, to strains such as P. superbus that can readily survive immediate exposure to severe desiccation (fast desiccation strategists). Using this panel of nematodes we investigated the effect of preincubation at high RH on the accumulation of trehalose and on the nematodes' anhydrobiotic potential. We found that there is a strong correlation between trehalose induction and anhydrobiotic survival in Panagrolaimus. Furthermore, the high trehalose levels observed in fully hydrated P. superbus (10% dry mass) suggest that constitutive expression of trehalose pre-adapts this fast dehydration strategist to combat desiccation. All the strains observed, regardless of survival rates, undertook both coiling and clumping, which has the effect of reducing surface area and slowing the rate of water loss during desiccation. Phylogenetic analyses were carried out to investigate whether the observed anhydrobiotic phenotypes were the result of convergent evolution or represented a single phylogenetic lineage. These analyses, derived from alignments of the rDNA ITS and D3 sequences, indicate that the strongly anhydrobiotic strains of Panagrolaimus form a single phylogenetic lineage, which is separate from the weakly anhydrobiotic strains. The weakly anhydrobiotic strains are also phylogenetically divergent from each other. Our data indicate that Panagrolaimus has the potential to be an excellent model system for the investigation of molecular aspects of nematode anhydrobiosis.
Some organisms can survive exposure to extreme desiccation by entering a state of suspended animation known as anhydrobiosis. The free-living nematode Aphelenchus avenae can be induced to enter the anhydrobiotic state by exposure to a moderate reduction in relative humidity. During this preconditioning period, the nematode accumulates large amounts of the disaccharide trehalose, which is thought to be necessary, but not sufficient, for successful anhydrobiosis. To identify other adaptations that are required for anhydrobiosis, we developed a novel SL1-based mRNA differential display technique to clone genes that are upregulated by dehydration in A. avenae. Three such genes, Aav-lea-1, Aav-ahn-1, and Aav-glx-1, encode, respectively, a late embryogenesis abundant (LEA) group 3 protein, a novel protein that we named anhydrin, and the antioxidant enzyme glutaredoxin. Strikingly, the predicted LEA and anhydrin proteins are highly hydrophilic and lack significant secondary structure in the hydrated state. The dehydration-induced upregulation of Aav-lea-1 and Aav-ahn-1 was confirmed by Northern hybridization and quantitative PCR experiments. Both genes were also upregulated by an osmotic upshift, but not by cold, heat, or oxidative stress. Experiments to investigate the relationship between mRNA levels and protein expression for these genes are in progress. LEA proteins occur commonly in plants, accumulating during seed maturation and desiccation stress; the presence of a gene encoding an LEA protein in an anhydrobiotic nematode suggests that some mechanisms of coping with water loss are conserved between plants and animals.
SummaryMost animal species reproduce sexually and fully parthenogenetic lineages are usually short lived in evolution. Still, parthenogenesis may be advantageous as it avoids the cost of sex and permits colonization by single individuals. Panagrolaimid nematodes have colonized environments ranging from arid deserts to Arctic and Antarctic biomes. Many are obligatory meiotic parthenogens, and most have cryptobiotic abilities, being able to survive repeated cycles of complete desiccation and freezing. To identify systems that may contribute to these striking abilities, we sequenced and compared the genomes and transcriptomes of parthenogenetic and outcrossing panagrolaimid species, including cryptobionts and non-cryptobionts. The parthenogens are triploids, most likely originating through hybridization. Adaptation to cryptobiosis shaped the genomes of panagrolaimid nematodes and is associated with the expansion of gene families and signatures of selection on genes involved in cryptobiosis. All panagrolaimids have acquired genes through horizontal gene transfer, some of which are likely to contribute to cryptobiosis.
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.
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