Desiccation Tolerance in the Tardigrade Richtersius coronifer Relies on Muscle Mediated Structural Reorganization (original) (raw)
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Anhydrobiosis: the extreme limit of desiccation tolerance
2007
Extreme habitats give rise to strong stressors that lead organisms to die or to possess specific adaptations to those stressors. One of the most widespread adaptations is quiescence, a common term for several strategies, including anhydrobiosis, a highly stable state of suspended animation due to complete desiccation pending recovery by rehydration. Anhydrobiosis is widespread in nature in a wide taxonomic variety among bacteria, protists, metazoans and plants. Using as model organisms, mainly tardigrades, micrometazoans able to enter anhydrobiosis in any phase of their life cycle from egg to adult, this review presents the response to desiccation from molecules to cells and organisms. Particular emphasis has been done with studies devoted to elucidate phenomena such as the longterm resistance in a desiccated state, the extraordinary resistance to chemical and physical extremes, the morphological, physiological, biochemical, and molecular constraints allowing organisms to enter and to survive anhydrobiosis, and the evolutionary meaning of life without water.
Biotechnology Advances, 2009
Certain organisms found across a range of taxa, including bacteria, yeasts, plants and many invertebrates such as nematodes and tardigrades are able to survive almost complete loss of body water. The dry organisms may remain in this state, which is known as anhydrobiosis, for decades without apparent damage. When water again becomes available, they rapidly rehydrate and resume active life. Research in anhydrobiosis has focused mainly on sugar metabolism and stress proteins. Despite the discovery of various molecules which are involved in desiccation and water stress, knowledge of the regulatory network governing the stability of the cellular architecture and the metabolic machinery during dehydration is still fragmentary and not well understood. A combination of transcriptional, proteomic and metabolic approaches with bioinformatics tools can provide a better understanding of gene regulation that underlie the biological functions and physiology related to anhydrobiosis. The development of this concept will raise exciting possibilities and techniques for the preservation and stabilization of biological materials in the dry state.
Dry and survive: Morphological changes during anhydrobiosis in a bdelloid rotifer
Journal of Structural Biology, 2010
a b s t r a c t Bdelloid rotifers are aquatic microinvertebrates able to cope with the loss of environmental water by entering dormancy, and are thus capable of living in temporary habitats. When water is evaporating, bdelloids contract into ''tuns", silence metabolism and lose water from the body, a condition known as anhydrobiosis. Under controlled conditions, a bdelloid species (Macrotrachela quadricornifera) was made anhydrobiotic, and its morphology was studied by light, confocal and electron microscopy. A compact anatomy characterizes the anhydrobiotic rotifer, resulting in a considerable reduction of its body volume: the internal organs, precisely packed together, occupy the body cavity almost completely and the lumen of hollow organs disappears. Remarkable ultrastructural changes characterize the anhydrobiotic condition. The mitochondria are wholly surrounded by a ring of electron-dense particles, and the epidermal pores, open in the hydrated specimens, become gradually closed by structures similar to epithelial junctions. The cilia are densely packed: microtubules are still identifiable, but the axonemal organization appears disrupted. This is the first extensive comparative study on the morphological changes associated with the anhydrobiosis process in a rotifer, providing the basis for an improved understanding of the processes involved in this extreme adaptation.
Is There a Single Biochemical Adaptation to Anhydrobiosis?
Integrative and Comparative Biology, 2002
SYNOPSIS. Even though water is required for the maintenance of biological integrity, numerous organisms are capable of surviving loss of virtually all their cellular water and existing in a state known as anhydrobiosis. Over the past three decades we and others have established that disaccharides such as trehalose and sucrose are almost certainly involved in stabilizing the dry cells. We discuss here some of the evidence behind the mechanism of this stabilization. Until the past few years this mechanism has been sufficiently appealing that a consensus has been developing that acquisition of these sugars in the cytoplasm may be both necessary and sufficient for anhydrobiosis. We show here that there are other routes to achieve the effects conferred by the sugars and that other adaptations are almost certainly required, at least in environmental conditions that are less than optimal. Under optimal storage conditions, the presence of the sugars alone may be sufficient to stabilize even mammalian cells in the dry state, findings that are already finding use in human clinical medicine. by guest on January 3, 2016 http://icb.oxfordjournals.org/ Downloaded from
2021
Tardigrades, also known as water bears, make up a phylum of small but extremely hardy animals, renowned for their ability to survive extreme stresses, including desiccation. How tardigrades survive desiccation is one of the enduring mysteries of animal physiology. Here we show that CAHS D, an intrinsically disordered protein belonging to a unique family of proteins possessed only by tardigrades, undergoes a liquid-to-gel phase transition in a concentration dependent manner. Unlike other gelling proteins, such as gelatin, our data support a mechanism in which gel formation of CAHS D is driven by intermolecular β-β interactions. We find that gel formation corresponds with strong coordination of water and slowing of water diffusion. The degree of water coordination correlates with the ability of CAHS D to protect lactate dehydrogenase from unfolding when dried. This implies that the mechanism for unfolding protection can be attributed to a combination of hydration and slowed molecular ...
Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance
IUBMB Life, 2018
In preparation for the onset of environmental challenges like overwintering, food limitation, anoxia, or water stress, many invertebrates and certain killifish enter diapause. Diapause is a developmentallyprogramed dormancy characterized by suppression of development and metabolism. For embryos of Artemia franciscana (brine shrimp), the metabolic arrest is profound. These gastrula-stage embryos depress oxidative metabolism by~99% during diapause and survive years of severe desiccation in a state termed anhydrobiosis. Trehalose is the sole fuel source for this developmental stage. Mitochondrial function during diapause is downregulated primarily by restricting substrate supply, as a result of inhibiting key enzymes of carbohydrate metabolism. Because proton conductance across the inner membrane is not decreased during diapause, the inference is that membrane potential must be compromised. In the absence of any intervention, the possibility exists that the F 1 F o ATP synthase and the adenine nucleotide translocator may reverse, leading to wholesale hydrolysis of cellular ATP. Studies with anhydrobiotes like A. franciscana are revealing multiple traits useful for improving desiccation tolerance that include the expression and accumulation late embryogenesis abundant (LEA) proteins and trehalose. LEA proteins are intrinsically disordered in aqueous solution but gain secondary structure (predominantly α-helix) as water is removed. These protective agents stabilize biological structures including lipid bilayers and mitochondria during severe water
Cells from an anhydrobiotic chironomid survive almost complete desiccation
Cryobiology, 2010
Dry-preservation of nucleated cells from multicellular animals represents a significant challenge in life science. As anhydrobionts can tolerate a desiccated state, their cells and organs are expected to show high desiccation tolerance in vitro. In the present study, we established cell lines derived from embryonic tissues of an anhydrobiotic chironomid, Polypedilum vanderplanki, designated as Pv11 and Pv210. Salinity stress induced the expression of a set of anhydrobiosis-related genes in both Pv11 and Pv210 cells, suggesting that at least a part of cells can autonomously control the physiological changes for the entry into anhydrobiosis. When desiccated with medium supplemented with 300 mM trehalose or sucrose and stored for 4 weeks in dry air (approximately 5% relative humidity), a small percentage of the cells was found to be viable upon rehydration, although surviving cells seemed not to be able to multiply. We also attempted dry-preservation of organs isolated from P. vanderplanki larvae, and found that a proportion of cells in some organs, including fat body, testis, nerve and dorsal vessel, tolerated in vitro desiccation.
Scientific Reports, 2018
The larvae of the African midge, Polypedilum vanderplanki, can enter an ametabolic state called anhydrobiosis to overcome fatal desiccation stress. The Pv11 cell line, derived from P. vanderplanki embryo, shows desiccation tolerance when treated with trehalose before desiccation and resumes proliferation after rehydration. However, the molecular mechanisms of this desiccation tolerance remain unknown. Here, we performed high-throughput CAGE-seq of mRNA and a differentially expressed gene analysis in trehalose-treated, desiccated, and rehydrated Pv11 cells, followed by gene ontology analysis of the identified differentially expressed genes. We detected differentially expressed genes after trehalose treatment involved in various stress responses, detoxification of harmful chemicals, and regulation of oxidoreduction that were upregulated. In the desiccation phase, L-isoaspartyl methyltransferase and heat shock proteins were upregulated and ribosomal proteins were downregulated. Analysis of differentially expressed genes during rehydration supported the notion that homologous recombination, nucleotide excision repair, and non-homologous recombination were involved in the recovery process. This study provides initial insights into the molecular mechanisms underlying the extreme desiccation tolerance of Pv11 cells. Desiccation stress, the loss of essential water, can be fatal. To tolerate desiccation stress, various organisms, such as rotifers, tardigrades, nematodes, plants, and larvae of the African midge Polypedilum vanderplanki, enter an ametabolic state called anhydrobiosis 1,2 and survive even if more than 99% of body water is lost 3. According to the water replacement hypothesis, a compatible solute, such as trehalose, protects phospholipid membranes and intracellular biological molecules and ensures their preservation under desiccation 3,4. Prolonged desiccation can lead to serious oxidative stress. For example, in the moss Fontinalis antipyretica an increase in the production of reactive oxygen species (ROS) is associated with dehydration 5,6. Protein oxidation in the dehydrated cells of the yeast Saccharomyces cerevisiae is 10 times that of hydrated cells 5,7. Thioredoxins (TRXs) remove harmful ROS and protect cells from ROS-induced damage 5,7. The genome of P. vanderplanki has a paralogous gene cluster for TRXs 8. These TRXs are upregulated by dehydration, and P. vanderplanki becomes tolerant to ROS-induced damage 8. Upon rehydration, the anhydrobiotes return to active life. In 2002, the Pv11 cell line was established as an embryonic cell culture from P. vanderplanki 9. Desiccation tolerance of Pv11 cells is induced by treatment with culture medium containing 600 mM trehalose for 48 h. Even after dehydration in a desiccator (<10% relative humidity) for 12 days and rehydration for 1 h, trehalose-treated Pv11 cells are able to resume proliferation 10 , whereas other insect cell lines (Sf9, BmN-4, AeAl-2, AnCu-35, and S2) do not. Pv11 cells are considered the only desiccation-tolerant insect cell line able to restore the regular cell