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      Iron Ladies – How Desiccated Asexual Rotifer Adineta vaga Deal With X-Rays and Heavy Ions?

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          Abstract

          Space exposure experiments from the last 15 years have unexpectedly shown that several terrestrial organisms, including some multi-cellular species, are able to survive in open space without protection. The robustness of bdelloid rotifers suggests that these tiny creatures can possibly be added to the still restricted list of animals that can deal with the exposure to harsh condition of space. Bdelloids are one of the smallest animals on Earth. Living all over the world, mostly in semi-terrestrial environments, they appear to be extremely stress tolerant. Their desiccation tolerance at any stage of their life cycle is known to confer tolerance to a variety of stresses including high doses of radiation and freezing. In addition, they constitute a major scandal in evolutionary biology due to the putative absence of sexual reproduction for at least 60 million years. Adineta vaga, with its unique characteristics and a draft genome available, was selected by ESA (European Space Agency) as a model system to study extreme resistance of organisms exposed to space environment. In this manuscript, we documented the resistance of desiccated A. vaga individuals exposed to increasing doses of X-ray, protons and Fe ions. Consequences of exposure to different sources of radiation were investigated in regard to the cellular type including somatic (survival assay) and germinal cells (fertility assay). Then, the capacity of A. vaga individuals to repair DNA DSB induced by different source of radiation was investigated. Bdelloid rotifers represent a promising model in order to investigate damage induced by high or low LET radiation. The possibility of exposure both on hydrated or desiccated specimens may help to decipher contribution of direct and indirect radiation damage on biological processes. Results achieved through this study consolidate our knowledge about the radioresistance of A. vaga and improve our capacity to compare extreme resistance against radiation among living organisms including metazoan.

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          Most cited references40

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          Cancer risk from exposure to galactic cosmic rays: implications for space exploration by human beings.

          Space programmes are shifting toward planetary exploration, and in particular towards missions by human beings to the moon and Mars. However, exposure to space radiation is an important barrier to exploration of the solar system by human beings because of the biological effects of high-energy heavy ions. These ions have a high charge and energy, are the main contributors to radiation risk in deep space, and their biological effects are understood poorly. Predictions of the nature and magnitude of risks posed by exposure to radiation in space are subject to many uncertainties. In recent years, worldwide efforts have focussed on an increased understanding of the oncogenic potential of galactic cosmic rays. A review of the new results in this specialty will be presented here.
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            Free Radicals in Biology: Oxidative Stress and the Effects of Ionizing Radiation

            P.A. Riley (2009)
            The most important electron acceptor in the biosphere is molecular oxygen which, by virtue of its bi-radical nature, readily accepts unpaired electrons to give rise to a series of partially reduced species collectively known as reduced (or 'reactive') oxygen species (ROS). These include superoxide (O.2-), hydrogen peroxide (H2O2), hydroxyl radical (HO.) and peroxyl (ROO.) and alkoxyl (RO.) radicals which may be involved in the initiation and propagation of free radical chain reactions and which are potentially highly damaging to cells. Mechanisms have evolved to restrict and control such processes, partly by compartmentation, and partly by antioxidant defences such as chain-breaking antioxidant compounds capable forming stable free radicals (e.g. ascorbate, alpha-tocopherol) and the evolution of enzyme systems (e.g. superoxide dismutase, catalase, peroxidases) that diminish the intracellular concentration of the ROS. Although some ROS perform useful functions, the production of ROS exceeding the ability of the organism to mount an antioxidant defence results in oxidative stress and the ensuing tissue damage may be involved in certain disease processes. Evidence that ROS are involved in primary pathological mechanisms is a feature mainly of extraneous physical or chemical perturbations of which radiation is perhaps the major contributor. One of the important radiation-induced free-radical species is the hydroxyl radical which indiscriminately attacks neighbouring molecules often at near diffusion-controlled rates. Hydroxyl radicals are generated by ionizing radiation either directly by oxidation of water, or indirectly by the formation of secondary partially ROS. These may be subsequently converted to hydroxyl radicals by further reduction ('activation') by metabolic processes in the cell. Secondary radiation injury is therefore influenced by the cellular antioxidant status and the amount and availability of activating mechanisms. The biological response to radiation may be modulated by alterations in factors affecting these secondary mechanisms of cellular injury.
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              Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation.

              Forty-one ionizing radiation-sensitive strains of Deinococcus radiodurans were evaluated for their ability to survive 6 weeks of desiccation. All exhibited a substantial loss of viability upon rehydration compared with wild-type D. radiodurans. Examination of chromosomal DNA from desiccated cultures revealed a time-dependent increase in DNA damage, as measured by an increase in DNA double-strand breaks. The evidence presented suggests that D. radiodurans' ionizing radiation resistance is incidental, a consequence of this organism's adaptation to a common physiological stress, dehydration.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                31 July 2020
                2020
                : 11
                : 1792
                Affiliations
                [1] 1Research Unit in Environmental and Evolutionary Biology (URBE), Laboratory of Evolutionary Genetics and Ecology (LEGE), NAmur Research Institute for Life Sciences (NARILIS), University of Namur , Namur, Belgium
                [2] 2Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth & Environment (ILEE), University of Namur , Namur, Belgium
                [3] 3Laboratory of Analysis by Nuclear Reaction (LARN), NAmur Research Institute for Life Sciences (NARILIS), University of Namur , Namur, Belgium
                [4] 4Space Microbiology Research Group, Radiation Biology Department, Institute of Aerospace Medicine, German Aerospace Center (DLR) , Cologne, Germany
                [5] 5Department of Natural Sciences, University of Applied Sciences Bonn-Rhein-Sieg (BRSU) , Rheinbach, Germany
                [6] 6Department of Basic Medical Sciences for Radiation Damages, National Institute of Radiological Sciences (NIRS) , Chiba, Japan
                Author notes

                Edited by: Rakesh Mogul, California State Polytechnic University, Pomona, United States

                Reviewed by: Tim Barraclough, University of Oxford, United Kingdom; Fernando Rodriguez, Marine Biological Laboratory (MBL), United States; Dinakar Challabathula, Central University of Tamil Nadu, India

                *Correspondence: Boris Hespeels, boris.hespeels@ 123456unamur.be

                These authors have contributed equally to this work

                This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.01792
                7412981
                32849408
                b0e3ec09-ba75-42e5-93f5-7587afd15d18
                Copyright © 2020 Hespeels, Penninckx, Cornet, Bruneau, Bopp, Baumlé, Redivo, Heuskin, Moeller, Fujimori, Lucas and Van Doninck.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 25 February 2020
                : 09 July 2020
                Page count
                Figures: 5, Tables: 0, Equations: 2, References: 52, Pages: 14, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                bdelloid rotifer,let,dna damage,extremophile,astrobiology,panspermia
                Microbiology & Virology
                bdelloid rotifer, let, dna damage, extremophile, astrobiology, panspermia

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