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      Lack of correlation of desiccation and radiation tolerance in microorganisms from diverse extreme environments tested under anoxic conditions

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          Abstract

          Four facultative anaerobic and two obligate anaerobic bacteria were isolated from extreme environments (deep subsurface halite mine, sulfidic anoxic spring, mineral-rich river) in the frame MASE (Mars Analogues for Space Exploration) project. The isolates were investigated under anoxic conditions for their survivability after desiccation up to 6 months and their tolerance to ionizing radiation up to 3000 Gy. The results indicated that tolerances to both stresses are strain-specific features. Yersinia intermedia MASE-LG-1 showed a high desiccation tolerance but its radiation tolerance was very low. The most radiation-tolerant strains were Buttiauxella sp. MASE-IM-9 and Halanaerobium sp. MASE-BB-1. In both cases, cultivable cells were detectable after an exposure to 3 kGy of ionizing radiation, but cells only survived desiccation for 90 and 30 days, respectively. Although a correlation between desiccation and ionizing radiation resistance has been hypothesized for some aerobic microorganisms, our data showed that there was no correlation between tolerance to desiccation and ionizing radiation, suggesting that the physiological basis of both forms of tolerances is not necessarily linked. In addition, these results indicated that facultative and obligate anaerobic organisms living in extreme environments possess varied species-specific tolerances to extremes.

          Abstract

          The survival after desiccation and after exposure to ionizing radiation of microorganisms from different extreme environments refutes the previously reported correlation between desiccation tolerance and radiation tolerance.

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          Most cited references72

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          Hydroxyl radical scavenging activity of compatible solutes

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            Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments.

            All microorganisms possess a positive turgor, and maintenance of this outward-directed pressure is essential since it is generally considered as the driving force for cell expansion. Exposure of microorganisms to high-osmolality environments triggers rapid fluxes of cell water along the osmotic gradient out of the cell, thus causing a reduction in turgor and dehydration of the cytoplasm. To counteract the outflow of water, microorganisms increase their intracellular solute pool by amassing large amounts of organic osmolytes, the so-called compatible solutes. These osmoprotectants are highly congruous with the physiology of the cell and comprise a limited number of substances including the disaccharide trehalose, the amino acid proline, and the trimethylammonium compound glycine betaine. The intracellular amassing of compatible solutes as an adaptive strategy to high-osmolality environments is evolutionarily well-conserved in Bacteria, Archaea, and Eukarya. Furthermore, the nature of the osmolytes that are accumulated during water stress is maintained across the kingdoms, reflecting fundamental constraints on the kind of solutes that are compatible with macromolecular and cellular functions. Generally, compatible solutes can be amassed by microorganisms through uptake and synthesis. Here we summarise the molecular mechanisms of compatible solute accumulation in Escherichia coli and Bacillus subtilis, model organisms for the gram-negative and gram-positive branches of bacteria.
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              Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli.

              Hydrogen peroxide is generated during aerobic metabolism and is capable of damaging critical biomolecules. However, mutants of Escherichia coli that are devoid of catalase typically exhibit no adverse phenotypes during growth in aerobic media. We discovered that catalase mutants retain the ability to rapidly scavenge H(2)O(2) whether it is formed internally or provided exogenously. Analysis of candidate genes revealed that the residual activity is due to alkyl hydroperoxide reductase (Ahp). Mutants that lack both Ahp and catalase could not scavenge H(2)O(2). These mutants excreted substantial amounts of H(2)O(2), and they grew poorly in air. Ahp is kinetically a more efficient scavenger of trace H(2)O(2) than is catalase and therefore is likely to be the primary scavenger of endogenous H(2)O(2). Accordingly, mutants that lack Ahp accumulated sufficient hydrogen peroxide to induce the OxyR regulon, whereas the OxyR regulon remained off in catalase mutants. Catalase still has an important role in wild-type cells, because the activity of Ahp is saturated at a low (10(-5) M) concentration of H(2)O(2). In contrast, catalase has a high K(m), and it therefore becomes the predominant scavenger when H(2)O(2) concentrations are high. This arrangement is reasonable because the cell cannot provide enough NADH for Ahp to rapidly degrade large amounts of H(2)O(2). In sum, E. coli does indeed generate substantial H(2)O(2), but damage is averted by the scavenging activity of Ahp.
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                Author and article information

                Journal
                FEMS Microbiol Lett
                FEMS Microbiol. Lett
                femsle
                FEMS Microbiology Letters
                Oxford University Press
                0378-1097
                1574-6968
                21 February 2018
                March 2018
                21 February 2018
                : 365
                : 6
                : fny044
                Affiliations
                [1 ]Radiation Biology Department, Institute of Aerospace Medicine, German Aerospace Center (DLR), Linder Hoehe, 51147 Cologne, Germany
                [2 ]Department of Internal Medicine, Medical University of Graz, Auerbruggerplatz 15, 8010 Graz, Austria
                [3 ]Department of Microbiology and Archaea, University of Regensburg, Universitätsstr. 31, 93053 Regensburg, Germany
                [4 ]UK Center for Astrobiology, School of Physics and Astronomy, University of Edinburgh, Peter Guthrie Tait Road, EH9 3FD, Edinburgh, UK
                [5 ]BioTechMed Graz, Mozartgasse 12/II, 8010 Graz, Austria
                [6 ]MATISProkaria, Vinlandsleid 12, 113 Reykjavík, Iceland
                [7 ]Faculty of Food Science and Nutrition, University of Iceland, Vatnsmýrarvegur 16, 101 Reykjavík, Iceland
                [8 ]Leiden Observatory, Universiteit Leiden, Niels Bohrweg 2, 2333 Leiden, Netherland
                [9 ]Space Policy Institute, George Washington University, 1957 E Street, 20052 Washington DC, USA
                [10 ]Instituto Nacional de Técnica Aeroespacial-Centro de Astrobiología (INTA-CAB), Torrejón de Ardoz, 28850 Madrid, Spain
                [11 ]Centro de Biología Molecular Severo Ochoa, Universidad Autónoma de Madrid (UAM), Calle Nicolás Cabrera 1, 28049 Madrid, Spain
                [12 ]Centre de Biophysique Moléculaire, Centre National de la Recherche Scientifique (CNRS), Rue Charles Sadron, 45071 Orléans, France
                [13 ]European Science Foundation (ESF), Quai Lezay-Marnésia, 67080 Strasbourg, France
                Author notes
                Corresponding author: Radiation Biology Department, Institute of Aerospace Medicine, Radiation Biology Department, German Aerospace Center (DLR), Linder Höhe, 51147 Cologne, Germany. Tel: +49-2203-6012194; Fax: +49-2203-61970; E-mail: kristina.beblo@ 123456dlr.de
                Author information
                http://orcid.org/0000-0002-4834-7121
                Article
                fny044
                10.1093/femsle/fny044
                5939664
                29474542
                ac3034e9-3a2b-4890-bfc3-121ea18b3d67
                © FEMS 2018.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                : 19 February 2018
                : 14 December 2017
                Page count
                Pages: 9
                Funding
                Funded by: European Community's Seventh Framework Program
                Award ID: FP7/2007-2013
                Categories
                Research Letter
                Environmental Microbiology

                Microbiology & Virology
                correlation,desiccation,radiation,survival,anaerobes,extreme environment
                Microbiology & Virology
                correlation, desiccation, radiation, survival, anaerobes, extreme environment

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