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Nagwani, A.K.;  Kaczmarek, �.;  Kmita, H. Anhydrobiosis. Encyclopedia. Available online: https://encyclopedia.pub/entry/26347 (accessed on 24 June 2024).
Nagwani AK,  Kaczmarek �,  Kmita H. Anhydrobiosis. Encyclopedia. Available at: https://encyclopedia.pub/entry/26347. Accessed June 24, 2024.
Nagwani, Amit Kumar, Łukasz Kaczmarek, Hanna Kmita. "Anhydrobiosis" Encyclopedia, https://encyclopedia.pub/entry/26347 (accessed June 24, 2024).
Nagwani, A.K.,  Kaczmarek, �., & Kmita, H. (2022, August 22). Anhydrobiosis. In Encyclopedia. https://encyclopedia.pub/entry/26347
Nagwani, Amit Kumar, et al. "Anhydrobiosis." Encyclopedia. Web. 22 August, 2022.
Anhydrobiosis
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Anhydrobiosis is induced by loss of water and indicates dehydration tolerance. Survival of dehydration is possible through changes at different levels of organism organization, including a remarkable reduction in metabolic activity at the cellular level. Thus, anhydrobiosis may be regarded as an anti-aging strategy.

tardigrades anhydrobiosis aging

1. Introduction

Tardigrades (water bears) are microinvertebrates found in marine, freshwater, and limno-terrestrial habitats [1]. The number of known tardigrade species has been steadily increasing over the past decades. Currently, 1019 freshwater and 217 marine species are reported in the World Register of Marine Species (WoRMS) database, and ca. 1400 species are described in the Actual Checklist of Tardigrada Species (41st edition: 16 May 2022) [2][3]. The phylum is divided into two classes, Eutardigrada and Heterotardigrada, distinguished mainly on the basis of claws, dorsal and cephalic cuticles, body appendages, and reproductive structures [4].
Tardigrades differ in reproduction modes; they can be dioecious, parthenogenetic, or hermaphroditic [5]. The known life-history traits of tardigrades, including total lifespan, number of molts, hatching time, and hatching success, do not appear to be strictly correlated with a certain reproduction mode and vary between species [6]. A total lifespan ranging from several weeks to several years has been observed in different tardigrade species with similar reproductive modes [7]. Food preferences are also diverse in tardigrades, including plant cells, algae, bacteria, nematodes, rotifers, or other tardigrades [8][9][10]. Tardigrades differ in their ability to survive in extreme environmental conditions through cryptobiosis [11]. Several types of cryptobiosis are distinguished according to the triggering factor: anhydrobiosis (lack of water), cryobiosis (low temperature), anoxybiosis (lack of oxygen), and osmobiosis (high or low osmotic pressure) [12][13][14][15]. During cryptobiosis, tardigrades reduce their metabolic activity, restoring it when conditions again become favorable [16]. Thus, cryptobiosis may extend their lifespan by many years [17][18].
One of the most important impacts of cryptobiosis on tardigrade lifespan is its impact on aging. For anhydrobiosis, the prevalent form of cryptobiosis [19], two hypotheses, denoted as “Sleeping Beauty” and “The Picture of Dorian Gray”, were proposed [20][21] to explain its effect on aging. The “Sleeping Beauty” hypothesis assumes complete exclusion of the time spent in anhydrobiosis; aging does not occur. The “The Picture of Dorian Gray” hypothesis predicts that the anhydrobiotic organism ages, at least in the initial stages of anhydrobiosis, such that aging proceeds or is slowed down [19]. Thus, the time spent in anhydrobiosis increases (“Sleeping Beauty”) or does not increase (“The Picture of Dorian Gray”) the lifespan of anhydrobiotic animals compared with non-dehydrated (active) animals, possibly due to differences in metabolic rate and protection against aging-imposed damages, although this has not been analyzed. Predictions of these hypotheses have rarely been tested. The lifespan of active specimens is currently the main parameter used to verify the hypotheses; total or age-specific fecundity, specimen vitality, and—rarely—morphology are also used [22]. The “Sleeping Beauty” hypothesis seems to apply to the bdelloid rotifers Macrotrachela quadricornifera Milne, 1886 [22] and Adineta ricciae Segers & Shiel, 2005 [20]; the free-living nematode Panagrolaimus rigidus Schneider, 1866 appears to follow “The Picture of Dorian Gray” [19]. For tardigrades, only one species (Milnesium tardigradum Doyere, 1840) [17] has been studied in this context; it was shown to follow the “Sleeping Beauty” hypothesis. The “Sleeping Beauty” hypothesis, in relation to the effect of anhydrobiosis on aging, seems to support complete suspension of metabolism [23]. However, respiration-based metabolism was detectable in anhydrobiotic animals at a low level for the tardigrade Macrobiotus hufelandi C.A.S. Schultze, 1834 [24] and the stem nematode Ditylenchus dipsaci (Kühn, 1857) [25][26]. Moreover, the activity of a mitochondrial protein known as alternative oxidase (AOX) during dehydration likely contributes to anhydrobiosis survival of Milnesium inceptum Morek, Suzuki, Schill, Georgiev, Yankova, Marley, & Michalczyk, 2019 [27]. Considering the available data, verification of these hypotheses remains an intriguing possibility. More research is required to determine the effect of anhydrobiosis on animal aging. However, markers that can verify these aging hypotheses are limited. The life-history traits could be used, but understanding the impact of anhydrobiosis on aging also requires study at the cellular level.

2. Anhydrobiosis

Anhydrobiosis indicates “life without water” and is also known as “dehydration tolerance”. Anhydrobiosis is induced by loss of water. As with other invertebrates, such as nematodes and rotifers, tardigrades exhibit a remarkable ability to enter and survive in an anhydrobiotic state at any stage of life [12][28]. The apparent decrease in metabolism with low water content is the most challenging aspect of anhydrobiosis. The relationship between hydration and metabolic rate, and whether anhydrobiotic animals should be classified as living (metabolically active) or dead (ametabolic), has been debated. However, despite years of research on anhydrobiotic invertebrates (e.g., [23][28][29][30]), the metabolic status and preservation of molecular integrity with low water content are not completely understood.
During anhydrobiosis, tardigrades form a tun-shaped structure to reduce their evaporation surface [16]. This ability is present in all tardigrade lineages, including marine echiniscoideans and arthrotardigrades, indicating that it is an ancient and homologous trait and a morphological and behavioral adaption to dehydration [16][31][32]. The process of tun formation is generally accompanied by contraction of the longitudinal intersegmental cuticle and invagination of the legs [33][34]. Intracellular lipids may be responsible for reduced transpiration rates and decreased cuticle permeability [35]. Tun formation is an active process requiring energy supply; thus, only active animals with functional mitochondria can achieve it [16][35]. Species inhabiting different microenvironments often exhibit differences in tun formation. For instance, limno-terrestrial species usually form tuns within half an hour; marine-tidal species may accomplish it in seconds [36]. A study of Echiniscoides sigismundi (M. Schultze, 1865), a marine tardigrade species, revealed that tun formation is not a prerequisite for dehydration tolerance in all tardigrade species and may be an adaptation to elevated external pressure rather than desiccation [32]. Moreover, it was reported that marine and true freshwater tardigrades cannot survive dehydration and undergo anhydrobiosis [7].
Dehydration generally causes severe damage to cellular structures, resulting in cell death; tardigrades have the ability to withstand such extremes. Available data indicate that tardigrade resistance to dehydration is based on mechanisms highly conserved within eukaryotes and mechanisms specific to the animals [37][38]. These mechanisms are mediated by oxidative stress response proteins (superoxide dismutase glutathione peroxidase, glutathione reductase, glutathione transferase, and catalase), chaperones (heat shock proteins), DNA repair enzymes (recombinases involved in DNA homologous recombination), water transporters (aquaporins), and intrinsically disordered proteins, such as late embryogenesis abundant proteins (LEA) and tardigrade-specific proteins, including tardigrade-specific intrinsically disordered proteins (TDP) and damage suppressor proteins (Dsup) [13][38][39][40]. Available data indicate that the mechanisms overlap, ensuring different molecule shielding and metabolic reprogramming and supporting glass formation by different molecules and water replacement. The latter is also assisted by non-protein molecules such as trehalose, although not all tardigrades rely on this disaccharide [16][29][41][42]. Further study of other non-protein protectants may provide additional useful information concerning dehydration tolerance in anhydrobiotic tardigrades. The same applies to TDP and Dsup; the results of multiomic studies indicate different numbers of paralogs for these proteins [37] and a lack of conservation of these proteins between Eutardigrada and Heterotardigrada but also a possibility of convergent evolution of anhydrobiosis machinery [38][43][44][45]. However, the role of highly conserved and ubiquitous heat shock proteins (HSPs) in managing different kinds of cellular stress and providing proteostasis is not consistent in the case of tardigrade anhydrobiosis [46][47][48]. With contradictory data, the role of these proteins in different anhydrobiotic tardigrades remains to be verified.
Damage caused by oxidative stress appears to be the most deleterious effect of water depletion, mediated by the formation of reactive oxygen species (ROS) [49][50]. ROS are involved in many pathological processes, including aging [51][52]. Genomic-, transcriptomic-, and proteomics-based studies have indicated the expression of a wide variety of known antioxidant enzymes in dehydrated tardigrades compared to active ones [38][53][54][55]. These enzymes can limit the availability of ROS and include superoxide dismutase (SOD), which transforms superoxide anions into hydrogen peroxide (H2O2); catalase (CAT) and glutathione peroxidase (GPx), which decompose H2O2 and glutathione transferase (GST), catalyzing the detoxification of endogenously derived ROS (and environmental pollutants) by glutathione conjunction; and glutathione reductase (GR), which recycles glutathione from glutathione disulfide [40][54][56]. Duplication of SOD-encoding genes was observed as a common characteristic of anhydrobiotic tardigrades [37][38]. Additionally, in Paramacrobiotus richtersi (Murray, 1911), increased SOD activity was reported in response to dehydration, suggesting its importance in the process [54]. Moreover, upregulation of catalase-encoding genes during anhydrobiosis was detected in the tardigrade Hypsibius exemplaris Gąsiorek, Stec, Morek, & Michalczyk, 2018 [43]. Glutathione peroxidase was reported to be crucial for successful anhydrobiosis in Pam. spatialis Guidetti, Cesari, Bertolani, Altiero, & Rebecchi, 2019 [40]. However, despite the available data concerning antioxidant systems in anhydrobiotic tardigrades, the molecular mechanism underlying anhydrobiosis is not completely understood. Further studies are necessary to understand the role of antioxidant systems in anhydrobiotic species.

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