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Lack of Correlation of Desiccation and Radiation Tolerance In FEMS Microbiology Letters, 365, 2018, fny044 doi: 10.1093/femsle/fny044 Advance Access Publication Date: 21 February 2018 Research Letter R E S E A RCH L E T T E R – Environmental Microbiology Lack of correlation of desiccation and radiation tolerance in microorganisms from diverse extreme environments tested under anoxic conditions Kristina Beblo-Vranesevic1,∗,†, Maria Bohmeier1, Alexandra K. Perras2,3, Petra Schwendner4, Elke Rabbow1, Christine Moissl-Eichinger2,5, Charles S. Cockell4, Pauline Vannier6, Viggo T. Marteinsson6,7, Euan P. Monaghan8, Pascale Ehrenfreund8,9, Laura Garcia-Descalzo10, Felipe Gomez´ 10, Moustafa Malki11, Ricardo Amils11,Fred´ eric´ Gaboyer12, Frances Westall12, Patricia Cabezas13, Nicolas Walter13 and Petra Rettberg1 1Radiation Biology Department, Institute of Aerospace Medicine, German Aerospace Center (DLR), Linder Hoehe, 51147 Cologne, Germany, 2Department of Internal Medicine, Medical University of Graz, Auerbruggerplatz 15, 8010 Graz, Austria, 3Department of Microbiology and Archaea, University of Regensburg, Universitatsstr.¨ 31, 93053 Regensburg, Germany, 4UK Center for Astrobiology, School of Physics and Astronomy, University of Edinburgh, Peter Guthrie Tait Road, EH9 3FD, Edinburgh, UK, 5BioTechMed Graz, Mozartgasse 12/II, 8010 Graz, Austria, 6MATISProkaria, Vinlandsleid 12, 113 Reykjav´ık, Iceland, 7Faculty of Food Science and Nutrition, University of Iceland, Vatnsmyrarvegur´ 16, 101 Reykjav´ık, Iceland, 8Leiden Observatory, Universiteit Leiden, Niels Bohrweg 2, 2333 Leiden, Netherland, 9Space Policy Institute, George Washington University, 1957 E Street, 20052 Washington DC, USA, 10Instituto Nacional de Tecnica´ Aeroespacial-Centro de Astrobiolog´ıa (INTA-CAB), Torrejon´ de Ardoz, 28850 Madrid, Spain, 11Centro de Biolog´ıa Molecular Severo Ochoa, Universidad Autonoma´ de Madrid (UAM), Calle Nicolas´ Cabrera 1, 28049 Madrid, Spain, 12Centre de Biophysique Moleculaire,´ Centre National de la Recherche Scientifique (CNRS), Rue Charles Sadron, 45071 Orleans,´ France and 13European Science Foundation (ESF), Quai Lezay-Marnesia,´ 67080 Strasbourg, France ∗Corresponding author: Radiation Biology Department, Institute of Aerospace Medicine, Radiation Biology Department, German Aerospace Center (DLR), Linder Hohe,¨ 51147 Cologne, Germany. Tel: +49-2203-6012194; Fax: +49-2203-61970; E-mail: [email protected] One sentence summary: 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. Editor: Hermann Heipieper †Kristina Beblo-Vranesevic, http://orcid.org/0000-0002-4834-7121 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 Received: 14 December 2017; Accepted: 19 February 2018 C 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 [email protected] 1 2 FEMS Microbiology Letters, 2018, Vol. 365, No. 6 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. Keywords: correlation; desiccation; radiation; survival; anaerobes; extreme environment INTRODUCTION breaks can occur (Bieger-Dose et al. 1992; Dose et al. 1992). Addi- tionally, the DNA can change from the B to the A-conformation Anaerobic microorganisms are widely distributed in Earth’s ex- resulting in DNA single- and double-strand breaks. Dehydra- treme environments, yet we still know little about their physi- tion for 6 weeks caused approximately 60 DNA double-strand ology and their capacity to adapt to extreme conditions. In par- breaks per genome in D. radiodurans (Fredrickson et al. 2008). ticular, there is a paucity of studies whereby different anaerobic Nevertheless, the survival of the microorganisms after 6 weeks microorganisms from extreme environments are investigated to of desiccation was not even reduced by one order of magni- understand their diverse physiological and metabolic capabili- tude (Mattimore and Battista 1996). Another form of damaging ties. In this study, the two stressors of interest were the toler- stress that occurs during desiccation is the formation of reactive ance to periods of water loss and the exposure to ionizing radia- oxygen species (ROS), which, in turn, leads to oxidative stress tion. These stressors also occur in other extreme environments (Franc¸a, Panek and Eleutherio 2007). The ROS are mainly su- but their combination is rare. Microorganisms frequently expe- r r peroxide anions ( O −) and hydroxyl radicals ( OH) affecting all rience periodic desiccation in subaerial environments or during 2 macromolecular cellular components (Cabiscol, Tamarit and Ros dispersal. Although most natural environments do not experi- 2000). However, the exact origin of the radicals during rehydra- ence ionizing radiation beyond the level of naturally occurring tion is unknown, but a possible source could be the metabolism background radiation (Thorne 2003), this stress can be explored itself (e.g. respiratory chain) when the cells were growing aer- as a proxy for an organisms’ ability to repair general cell dam- obically (Gonzalez-Flecha´ and Demple 1995;Franc¸a, Panek and age. Furthermore, there has often been a claimed correlation be- Eleutherio 2007).They are also formed by indirect effects through tween desiccation and ionizing radiation resistance, which is of the radiation-induced radiolysis of intracellular water and sur- interest to explore further. It is suggested that the physiological rounding water and account for approximately 80% of intro- basis and repair mechanisms to counteract the stress-induced duced DNA damages (Michaels and Hunt 1978;Joneset al. 1994; damage by radiation or desiccation might be linked or might Riley 1994). After exposure to ionizing radiation of 5 kGy, approx- even be the same (Mattimore and Battista 1996). imately 200 double-strand breaks were detected in D. radiodurans While there are several studies investigating the survivability (Cox and Battista 2005). However, the survivability of D. radio- of model microorganisms, such as Escherichia coli and Deinococcus durans was not reduced (Battista, Earl and Park 1999). In addi- radiodurans, after desiccation and after exposure to ionizing ra- tion, ionizing radiation also affects proteins through oxidation diation tested under oxic conditions (Clavero et al. 1994; Welsh processes, lipids through lipid peroxidation and disturbance of and Herbert 1999;Daly2009; Bauermeister et al. 2011), there are membrane permeability in eukaryotic and prokaryotic systems only a few examples where facultative and strict anaerobic mi- (Leyko and Bartosz 1985;Dalyet al. 2007; Krisko and Radman croorganisms were tested against these stressors under anoxic 2010). conditions. The survival capacity after exposure to one stres- MASE (Mars Analogues for Space Exploration), a project sor in form of ionizing radiation was described for the hyper- funded by the European Union, was initiated to investigate thermophilic anaerobic microorganisms, Pyrococcus furiosus and anaerobic microorganisms in terrestrial extreme environments Thermococcus gammatolerans (DiRuggiero et al. 1997;Jolivetet al. and their physiological adaptations to these extreme environ- 2003). However, there are only very few studies about the tol- mental conditions (Cockell et al. 2017). In this article, we describe erance in terms of sensitivity of anaerobic microorganisms to the survivability after prolonged desiccation of up to 4 weeks desiccation (Fetzer, Bak and Conrad 1993;Bebloet al. 2009). and exposure to ionizing radiation (up to 3 kGy) of four facul- The application of both of these stressors gives insights into tative anaerobic and two strict anaerobic microorganisms iso- the abilities that microorganisms have evolved to survive dam- lated from different extreme environments in the frame of this age to macromolecules such as proteins, membranes and nu- project. cleic acids. During desiccation, initially the free intracellular water and subsequently the hydration
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