Extreme stress tolerance in tardigrades: surviving space conditions in low earth orbit. J Zool System Evolut Res

Journal of Zoological Systematics and Evolutionary Research (Impact Factor: 1.68). 05/2011; 49(special issue):90-97. DOI: 10.1111/j.1439-0469.2010.00605.x


Most terrestrial tardigrade species possess the ability to enter a reversible ametabolic state termed anhydrobiosis in response to desiccation. In the anhydrobiotic state, tardigrades display an incredible capacity to tolerate extreme environmental stress, not necessarily encountered in their natural habitat. In this study, we determine the effect of different extreme stresses on initial survival, long-term survival and fecundity of selected species of limno-terrestrial tardigrades. The primary focus was to assess the effect of cosmic radiation. This was achieved through the RoTaRad (Rotifers, Tardigrades and Radiation) project on the BIOPAN 6 mission, funded by Agenzia Spaziale Italiana under the European Space Agency. To test their tolerance of space environment, tardigrades were sent into low earth orbit, and exposed to cosmic radiation and a microgravity environment. Experiments on Whatman-3 filters show an effect of cosmic radiation on the survival of the eutardigrade Richtersius coronifer just after returning to Earth; however, after 2 years of desiccation on Whatman-3 filters, none of the tardigrades previously exposed to cosmic radiation could be revived. In a microcosmos experiment, the tardigrades R. coronifer, Ramazzottius oberhauseri and Echiniscus testudo were desiccated on a moss substrate together with rotifers and nematodes. Very low survival rates were observed in this experiment, likely due to the applied desiccation protocol. Embryos of the tardigrade Milnesium tardigradum were also exposed to cosmic radiation; they all hatched in the laboratory after the flight. In addition, experiments testing extreme cold and vacuum tolerance in R. coronifer show that tardigrades in anhydrobiosis are unaffected by these conditions.
Molti dei tardigradi che vivono in ambiente terrestre sono capaci di sopravvivere alla disidratazione del loro ambiente ricorrendo a una particolare forma di dormienza detta anidrobiosi. Durante l’anidrobiosi, è noto che i tardigradi tollerano stress che possono andare ben oltre quelli tipici del loro ambiente naturale. Seguendo questa linea di indagine, in questo studio abbiamo valutato la risposta di tardigradi a condizioni estreme in termini della loro capacità di ripresa, e della successiva sopravvivenza e fertilità. L’esperimento RoTaRad, che ha avuto luogo nella’facility’ BIOPAN6 (di ESA) all’esterno del vettore Foton 3, ed ha volato intorno alla Terra per 10 giorni esposto alle condizioni dello spazio, ha dato l’opportunità di valutare l’effetto di radiazioni cosmiche e di ‘microgravità’ su tre specie di tardigradi. Gli animali sono stati disidratati in condizioni controllate su due substrati: filtri Whatman 3 (Richtersius coronifer), e muschio (microcosmo: Richtersius coronifer, Echiniscus testudo, Ramazzotius oberhauseri, insieme a nematodi e rotiferi bdelloidei). I risultati ottenuti dalla reidratazione dei filtri, con R. coronifer, suggeriscono che le radiazioni cosmiche non hanno inficiato la sua capacità di ripresa dopo l’esposizione, ma filtri paralleli tenuti disidratati per due anni non hanno registrato alcuna ripresa. Nel microcosmo le specie di tardigradi hanno mostrato una bassa ripresa, forse a causa del protocollo di disidratazione seguito nella preparazione dei campioni che ha dovuto essere lo stesso per tutti i taxa. Un ulteriore set di campioni esposti alle radiazioni cosmiche era rappresentato da embrioni di Milnesium tardigradum: tutti hanno completato lo sviluppo e sono nati in laboratorio. Ulteriori esperimenti sono anche stati condotti presso l’Università di Copenhagen esponendo R. coronifer disidratato al freddo e al vuoto: la ripresa è stata molto elevata.

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Available from: Kenneth Halberg
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    • "Tardigrades (Fig. 1) are best known for their ability to undergo cryptobiosis (anhydrobiosis), slowing their metabolism (by a factor of 10,000). Tardigrades have become an interesting invertebrate model species due to their extreme capacities for withstanding not only desiccation and freezing, but also for being able to survive interplanetary vacuum, ionizing solar and galactic radiation, extreme temperatures (-150 ºC to 150 ºC), and large changes in osmolarity (e.g., Persson et al. 2011; Welnicz et al. 2011). Understanding the genomes of tardigrades is important not only to understand anhydrobiosis, miniaturization and DNA repair (Förster et al. 2012), but also to obtain insights into the evolution of the clade that leads to the enormous diversity of arthropods. "

    Full-text · Dataset · Feb 2014
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    • "Tardigrades are microscopic metazoans, known for their ability to tolerate physical stress, and to survive in some of the most extreme environments (Renaud-Mornant, 1975; Dastych and Kristensen, 1995; Pugh and McInnes, 1998; Wright, 2001; Møbjerg et al., 2007; Rebecchi et al., 2007; J€ onsson et al., 2008; Halberg et al., 2009b; McInnes, 2010; Schill, 2010; Møbjerg et al., 2011; Persson et al., 2011; Halberg et al., 2013). Another area, which has received much attention, is their phylogenetic position in the animal tree of life (Dujardin, 1851; Plate, 1889; Marcus, 1929; Crowe et al., 1970; Baccetti and Rosati, 1971; Bussers and Jeuniaux, 1973; Dewel and Clark, 1973; Ramsk€ old and Hou, 1991; Mallatt et al., 2004; Dunn et al., 2008; Rota-Stabelli et al., 2010). "
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    ABSTRACT: Knowledge of tardigrade brain structure is important for resolving the phylogenetic relationships of Tardigrada. Here, we present new insight into the morphology of the brain in a marine arthrotardigrade, Actinarctus doryphorus, based on transmission electron microscopy, supported by scanning electron microscopy, conventional light microscopy as well as confocal laser scanning microscopy. Arthrotardigrades contain a large number of plesiomorphic characters and likely represent ancestral tardigrades. They often have segmented body outlines and each trunk segment, with its paired set of legs, may have up to five sensory appendages. Noticeably, the head carries numerous cephalic appendages that are structurally equivalent to the sensory appendages of the trunk segments. Our data reveal that the brain of A. doryphorus is partitioned into three paired lobes, and that these lobes exhibit a more pronounced separation as compared to that of eutardigrades. The first brain lobe in A. doryphorus is located anteriodorsally, with the second lobe just below it in an anterioventral position. Both of these two paired lobes are located anterior to the buccal tube. The third pair of brain lobes are situated posterioventrally to the first two lobes, and flank the buccal tube. In addition, A. doryphorus possesses a subpharyngeal ganglion, which is connected with the first of the four ventral trunk ganglia. The first and second brain lobes in A. doryphorus innervate the clavae and cirri of the head. The innervations of these structures indicate a homology between, respectively, the clavae and cirri of A. doryphorus and the temporalia and papilla cephalica of eutardigrades. The third brain lobes innervate the buccal lamella and the stylets as described for eutardigrades. Collectively, these findings suggest that the head region of extant tardigrades is the result of cephalization of multiple segments. Our results on the brain anatomy of Actinarctus doryphorus support the monophyly of Panarthropoda. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.
    Full-text · Article · Feb 2014 · Journal of Morphology
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    • "Here, we investigate the anatomical changes that occur during anhydrobiosis in the tardigrade Richtersius coronifer (Richters, 1903), a species well known for its ability to enter anhydrobiosis [10,28,29]. We show that mitochondrial energy production and a functional musculature are prerequisites for the formation of the tun state. "
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    ABSTRACT: Life unfolds within a framework of constraining abiotic factors, yet some organisms are adapted to handle large fluctuations in physical and chemical parameters. Tardigrades are microscopic ecdysozoans well known for their ability to endure hostile conditions, such as complete desiccation - a phenomenon called anhydrobiosis. During dehydration, anhydrobiotic animals undergo a series of anatomical changes. Whether this reorganization is an essential regulated event mediated by active controlled processes, or merely a passive result of the dehydration process, has not been clearly determined. Here, we investigate parameters pivotal to the formation of the so-called "tun", a state that in tardigrades and rotifers marks the entrance into anhydrobiosis. Estimation of body volume in the eutardigrade Richtersius coronifer reveals an 87 % reduction in volume from the hydrated active state to the dehydrated tun state, underlining the structural stress associated with entering anhydrobiosis. Survival experiments with pharmacological inhibitors of mitochondrial energy production and muscle contractions show that i) mitochondrial energy production is a prerequisite for surviving desiccation, ii) uncoupling the mitochondria abolishes tun formation, and iii) inhibiting the musculature impairs the ability to form viable tuns. We moreover provide a comparative analysis of the structural changes involved in tun formation, using a combination of cytochemistry, confocal laser scanning microscopy and 3D reconstructions as well as scanning electron microscopy. Our data reveal that the musculature mediates a structural reorganization vital for anhydrobiotic survival, and furthermore that maintaining structural integrity is essential for resumption of life following rehydration.
    Full-text · Article · Dec 2013 · PLoS ONE
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