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      Thermotolerance experiments on active and desiccated states of Ramazzottius varieornatus emphasize that tardigrades are sensitive to high temperatures

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          Abstract

          Global warming is already having harmful effects on habitats worldwide and it is therefore important to gain an understanding of how rising temperatures may affect extant animals. Here, we investigate the tolerance to high temperatures of Ramazzottius varieornatus, a tardigrade frequently found in transient freshwater habitats. Using logistic modelling on activity we evaluate the effect of 24 hour temperature exposures on active tardigrades, with or without a short acclimation period, compared to exposures of desiccated tardigrades. We estimate that the 50% mortality temperature for non-acclimated active tardigrades is 37.1 °C, with a small but significant increase to 37.6 °C following acclimation. Desiccated specimens tolerate much higher temperatures, with an estimated 50% mortality temperature of 82.7 °C following 1 hour exposures, but with a significant decrease to 63.1 °C following 24 hour exposures. Our results show that metabolically active tardigrades are vulnerable to high temperatures, yet acclimatization could provide a tolerance increase. Desiccated specimens show a much higher resilience—exposure-time is, however, a limiting factor giving tardigrades a restricted window of high temperature tolerance. Tardigrades are renowned for their ability to tolerate extreme conditions, but their endurance towards high temperatures clearly has an upper limit—high temperatures thus seem to be their Achilles heel.

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          Life in extreme environments.

          Each recent report of liquid water existing elsewhere in the Solar System has reverberated through the international press and excited the imagination of humankind. Why? Because in the past few decades we have come to realize that where there is liquid water on Earth, virtually no matter what the physical conditions, there is life. What we previously thought of as insurmountable physical and chemical barriers to life, we now see as yet another niche harbouring 'extremophiles'. This realization, coupled with new data on the survival of microbes in the space environment and modelling of the potential for transfer of life between celestial bodies, suggests that life could be more common than previously thought. Here we examine critically what it means to be an extremophile, and the implications of this for evolution, biotechnology and especially the search for life in the Universe.
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            The role of vitrification in anhydrobiosis.

            Numerous organisms are capable of surviving more or less complete dehydration. A common feature in their biochemistry is that they accumulate large amounts of disaccharides, the most common of which are sucrose and trehalose. Over the past 20 years, we have provided evidence that these sugars stabilize membranes and proteins in the dry state, most likely by hydrogen bonding to polar residues in the dry macromolecular assemblages. This direct interaction results in maintenance of dry proteins and membranes in a physical state similar to that seen in the presence of excess water. An alternative viewpoint has been proposed, based on the fact that both sucrose and trehalose form glasses in the dry state. It has been suggested that glass formation (vitrification) is in itself sufficient to stabilize dry biomaterials. In this review we present evidence that, although vitrification is indeed required, it is not in itself sufficient. Instead, both direct interaction and vitrification are required. Special properties have often been claimed for trehalose in this regard. In fact, trehalose has been shown by many workers to be remarkably (and sometimes uniquely) effective in stabilizing dry or frozen biomolecules, cells, and tissues. Others have not observed any such special properties. We review evidence here showing that trehalose has a remarkably high glass-transition temperature (Tg). It is not anomalous in this regard because it lies at the end of a continuum of sugars with increasing Tg. However, it is unusual in that addition of small amounts of water does not depress Tg, as in other sugars. Instead, a dihydrate crystal of trehalose forms, thereby shielding the remaining glassy trehalose from effects of the added water. Thus under less than ideal conditions such as high humidity and temperature, trehalose does indeed have special properties, which may explain the stability and longevity of anhydrobiotes that contain it. Further, it makes this sugar useful in stabilization of biomolecules of use in human welfare.
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              Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus

              Tardigrada, a phylum of meiofaunal organisms, have been at the center of discussions of the evolution of Metazoa, the biology of survival in extreme environments, and the role of horizontal gene transfer in animal evolution. Tardigrada are placed as sisters to Arthropoda and Onychophora (velvet worms) in the superphylum Panarthropoda by morphological analyses, but many molecular phylogenies fail to recover this relationship. This tension between molecular and morphological understanding may be very revealing of the mode and patterns of evolution of major groups. Limnoterrestrial tardigrades display extreme cryptobiotic abilities, including anhydrobiosis and cryobiosis, as do bdelloid rotifers, nematodes, and other animals of the water film. These extremophile behaviors challenge understanding of normal, aqueous physiology: how does a multicellular organism avoid lethal cellular collapse in the absence of liquid water? Meiofaunal species have been reported to have elevated levels of horizontal gene transfer (HGT) events, but how important this is in evolution, and particularly in the evolution of extremophile physiology, is unclear. To address these questions, we resequenced and reassembled the genome of H. dujardini, a limnoterrestrial tardigrade that can undergo anhydrobiosis only after extensive pre-exposure to drying conditions, and compared it to the genome of R. varieornatus, a related species with tolerance to rapid desiccation. The 2 species had contrasting gene expression responses to anhydrobiosis, with major transcriptional change in H. dujardini but limited regulation in R. varieornatus. We identified few horizontally transferred genes, but some of these were shown to be involved in entry into anhydrobiosis. Whole-genome molecular phylogenies supported a Tardigrada+Nematoda relationship over Tardigrada+Arthropoda, but rare genomic changes tended to support Tardigrada+Arthropoda.
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                Author and article information

                Contributors
                nmobjerg@bio.ku.dk
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                9 January 2020
                9 January 2020
                2020
                : 10
                : 94
                Affiliations
                [1 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Department of Biology, August Krogh Building, , University of Copenhagen, ; Copenhagen, Denmark
                [2 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Data Science Laboratory, Department of Mathematical Sciences, , University of Copenhagen, ; Copenhagen, Denmark
                Author information
                http://orcid.org/0000-0001-5482-9584
                http://orcid.org/0000-0002-5845-9047
                Article
                56965
                10.1038/s41598-019-56965-z
                6952461
                31919388
                a9c9dde0-e965-418c-9a8e-5e5dc439a3d7
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 June 2019
                : 19 December 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100004836, Det Frie Forskningsråd (Danish Council for Independent Research);
                Award ID: DFF – 4090-00145
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100002808, Carlsbergfondet (Carlsberg Foundation);
                Award ID: CF15-0570
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100008398, Villum Fonden (Villum Foundation);
                Award ID: 17522
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                ecology,evolution,zoology,environmental sciences
                Uncategorized
                ecology, evolution, zoology, environmental sciences

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