Anhydrobiosis in nematodes: Biosynthesis of trehalose

Loomis, Stephen H.; Madin, K. A. C.; Crowe, John H.

doi:10.1002/jez.1402110308

Cited by 26 publications

(16 citation statements)

References 21 publications

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“…This phenomenon is widespread, occurring in nearly all the major taxa of the plant, animal, and microbial worlds . Almost all desiccation-tolerant organisms synthesize large amounts of disaccharides (particularly sucrose and trehalose) during dehydration (Drennan et al, 1993;Gadd et al, 1987;Loomis et al, 1980;Hoekstra et al, 1989;Koster and Leopold, 1988;Clegg, 1965), and their survival is correlated with the presence of these sugars (Madin and Crowe, 1975;Womersley et al, 1986) . Studies in vitro have shown that these sugars are capable of preserving structure and function in biomolecules and molecular assemblages, such as membranes, during drying (Crowe et al, 1987a).…”

Section: Introductionmentioning

confidence: 99%

Trehalose Maintains Phase Separation in an Air-Dried Binary Lipid Mixture

Ricker

Tsvetkova

Wolkers

et al. 2003

Biophysical Journal

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Mixing and thermal behavior of hydrated and air-dried mixtures of 1,2-dilauroyl-sn-glycero-3-phosphocholine (DLPC) and 1,2-distearoyl-d70-sn-glycero-3-phosphocholine (DSPCd-70) in the absence and presence of trehalose were investigated by Fourier transform infrared spectroscopy. Mixtures of DLPC:DSPCd-70 (1:1) that were air-dried at 25 degrees C show multiple phase transitions and mixed phases in the dry state. After annealing at high temperatures, however, only one transition is seen during cooling scans. When dried in the presence of trehalose, the DLPC component shows two phase transitions at -22 degrees C and 75 degrees C and is not fully solidified at -22 degrees C. The DSPCd-70 component, however, shows a single phase transition at 78 degrees C. The temperatures of these transitions are dramatically reduced after annealing at high temperatures with trehalose. The data suggest that the sugar has a fluidizing effect on the DLPC component during drying and that this effect becomes stronger for both components with heating. Examination of infrared bands arising from the lipid phosphate and sugar hydroxyl groups suggests that the strong effect of trehalose results from direct interactions between lipid headgroups and the sugar and that these interactions become stronger after heating. The findings are discussed in terms of the protective effect of trehalose on dry membranes.

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Section: Introductionmentioning

confidence: 99%

Trehalose Maintains Phase Separation in an Air-Dried Binary Lipid Mixture

Ricker

Tsvetkova

Wolkers

et al. 2003

Biophysical Journal

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“…An ultimate strategy for the survival of drought is anhydrobiosis, in which an organism loses virtually all of its free intracellular water and ceases metabolism but remains capable of revival after rehydration (1). Anhydrobiosis has been found in various unicellular organisms, invertebrates, and plants (2)(3)(4)(5)(6)(7)(8)(9). Based on studies on plant seeds and in vitro experiments, two mutually compatible hypotheses have been proposed.…”

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confidence: 99%

“…Concurrently, late embryonic abundant (LEA) proteins increase in quantity (23). Trehalose and a highly hydrophilic LEA protein are found in many anhydrobiotic microbes and animals (1)(2)(3)(4)(5)(6)(7)(8)(24)(25)(26)(27) and are assumed to be involved in desiccation tolerance. Combination of these factors may contribute to the building of stable intracellular glasses (28)(29)(30)(31).…”

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confidence: 99%

Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki

Sakurai

Furuki

Akao³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

229

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Anhydrobiosis is an extremely dehydrated state in which organisms show no detectable metabolism but retain the ability to revive after rehydration. Thus far, two hypotheses have been proposed to explain how cells are protected during dehydration: (i) water replacement by compatible solutes and (ii) vitrification. The present study provides direct physiological and physicochemical evidence for these hypotheses in an African chironomid, Polypedilum vanderplanki, which is the largest multicellular animal capable of anhydrobiosis. Differential scanning calorimetry measurements and Fourier-transform infrared (FTIR) analyses indicated that the anhydrobiotic larvae were in a glassy state up to as high as 65°C. Changing from the glassy to the rubbery state by either heating or allowing slight moisture uptake greatly decreased the survival rate of dehydrated larvae. In addition, FTIR spectra showed that sugars formed hydrogen bonds with phospholipids and that membranes remained in the liquid-crystalline state in the anhydrobiotic larvae. These results indicate that larvae of P. vanderplanki survive extreme dehydration by replacing the normal intracellular medium with a biological glass. When entering anhydrobiosis, P. vanderplanki accumulated nonreducing disaccharide trehalose that was uniformly distributed throughout the dehydrated body by FTIR microscopic mapping image. Therefore, we assume that trehalose plays important roles in water replacement and intracellular glass formation, although other compounds are surely involved in these phenomena.trehalose ͉ water replacement ͉ Fourier-transform infrared microspectroscopy ͉ biological glass ͉ cryptobiosis

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“…2 B), although individual actins and myosins were slightly enriched among genes with a significant down-regulation in embryos although one small HPS showed an inverse pattern). Although not significantly enriched (due to the low number of protein in the pathway), the trehalose metabolism genes all show differential expression in the ephippium, three alpha-alspha-trehalose-6-phosphate synthases (that catalyze the rate-limiting step in trehalose synthesis pathway [35], are up-regulated in the ephippium (Fig.2 D; FDR<0.01), while the trehalose hydrolase is down-regulated (FDR<0.01).…”

Section: A Priori Expected Enrichment Of Molecular Functions Across Lmentioning

confidence: 99%

Quantitative proteomics reveals remodeling of protein repertoire across life phases ofDaphnia pulex

Peshkin

Boukhali

Haas

et al. 2019

Preprint

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The microcrustacean Daphnia is becoming an organism of choice for genomic and proteomic studies of the effects of environmental stressors. However, the changes in protein expression across the life cycle have not been fully characterized. We analyzed the proteomes of adult females, juveniles, asexually produced embryos, and the ephippia -resting stages containing two sexually produced diapausing freezing-and desiccation-resistant embryos.Overall, we were significantly more likely to detect proteins with known molecular functions than proteins with no detectable orthology. Similarly we could detect those with stronger gene model support, as judged by mutual best BLAST hits between two independent genome assemblies than those without such support. This suggests that we could apply our proteomics pipeline to verify hypothesized proteins, even given less-than-perfect reference gene models. In particular, we observed up-regulation of vitellogenins and down-regulation of actins and myosins in embryos of both types, as compared to juveniles and adults and overrepresentation of cell-cycle related proteins in the developing embryos, as compared to both diapausing embryos and adults. We found upregulation of small heat-shock proteins and redox peroxidases, as well as overrepresentation of stress-response proteins in the ephippium relative to the asexually produced non-diapausing embryos. The ephippium also showed upregulation of three trehalose-synthesis proteins and down-regulation of a trehalose hydrolase, consistent with the role of trehalose in protection against freezing and desiccation. Statement of significance of the studyFreshwater plankton crustacean Daphnia is rapidly becoming a model organism of choice for ecological and developmental genomics. While there have been several advances towards establishing the protocols and reference datasets for proteomics, a detailed dataset covering several main steps of asexual and sexual phases of Daphnia life cycle is not yet available. Moreover, different versions of D. pulex genome differ in the number of proteincoding genes identified; it is unclear whether these differences are caused by differences between sequenced genotypes or between gene model methodology used. In this study we report LC-MS2/MS3 proteomes of whole body adult females, juvenile females, asexually produces embryos and diapausing eggs capable of surviving freezing and desiccation.

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Anhydrobiosis in nematodes: Biosynthesis of trehalose

Cited by 26 publications

References 21 publications

Trehalose Maintains Phase Separation in an Air-Dried Binary Lipid Mixture

Trehalose Maintains Phase Separation in an Air-Dried Binary Lipid Mixture

Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki

Quantitative proteomics reveals remodeling of protein repertoire across life phases ofDaphnia pulex

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