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      A biomimetic approach to shielding from ionizing radiation: The case of melanized fungi

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      PLoS ONE
      Public Library of Science

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          Abstract

          Melanized fungi have been shown to thrive in environments with high radionuclide concentrations, which led to the association of the pigment melanin with the protection against ionizing radiation. Several hypotheses regarding the function of melanin have been proposed. Yet, the exact mechanism behind the protective property of melanin is unclear and poorly explored. A better understanding of the mechanisms that are involved in increasing the tolerance of the organisms to ionizing radiation could lead to technology transfer to human-related applications. Effective protection from radiation is essential for human space flight in general and human missions beyond Low Earth Orbit specifically. In this paper, we follow a biomimetic approach: we test two of current hypotheses and discuss how they could be applied to radiation shield designs. First we focus on the interaction of melanin with high energy electrons, which has been suspected to reduce the kinetic energy of the electrons through a cascade of collisions, thus providing physical shielding. Second, we investigate if the spatial arrangement of melanin, organized as a thin film or a collection of hollow micro-spheres, affects its shielding properties. To this end, we measured experimentally and by numerical simulations the attenuation of β-radiation as pass through solutions and suspensions of melanin and contrasted the values to the ones of cellulose, a substance with similar elemental composition. Further, we investigate the spatial arrangement hypothesis using Monte Carlo simulations. In agreement with the simulations, our experiments indicated that melanin does not provide improved shielding in comparison to cellulose from β-radiation. However, our simulations suggest a substantial effect of the spatial arrangement on the shielding performance of melanin, a pathway that could be transferred to the design of composite radiation shields.

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          Ionizing Radiation Changes the Electronic Properties of Melanin and Enhances the Growth of Melanized Fungi

          Background Melanin pigments are ubiquitous in nature. Melanized microorganisms are often the dominating species in certain extreme environments, such as soils contaminated with radionuclides, suggesting that the presence of melanin is beneficial in their life cycle. We hypothesized that ionizing radiation could change the electronic properties of melanin and might enhance the growth of melanized microorganisms. Methodology/Principal Findings Ionizing irradiation changed the electron spin resonance (ESR) signal of melanin, consistent with changes in electronic structure. Irradiated melanin manifested a 4-fold increase in its capacity to reduce NADH relative to non-irradiated melanin. HPLC analysis of melanin from fungi grown on different substrates revealed chemical complexity, dependence of melanin composition on the growth substrate and possible influence of melanin composition on its interaction with ionizing radiation. XTT/MTT assays showed increased metabolic activity of melanized C. neoformans cells relative to non-melanized cells, and exposure to ionizing radiation enhanced the electron-transfer properties of melanin in melanized cells. Melanized Wangiella dermatitidis and Cryptococcus neoformans cells exposed to ionizing radiation approximately 500 times higher than background grew significantly faster as indicated by higher CFUs, more dry weight biomass and 3-fold greater incorporation of 14C-acetate than non-irradiated melanized cells or irradiated albino mutants. In addition, radiation enhanced the growth of melanized Cladosporium sphaerospermum cells under limited nutrients conditions. Conclusions/Significance Exposure of melanin to ionizing radiation, and possibly other forms of electromagnetic radiation, changes its electronic properties. Melanized fungal cells manifested increased growth relative to non-melanized cells after exposure to ionizing radiation, raising intriguing questions about a potential role for melanin in energy capture and utilization.
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            Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin.

            Life on Earth has always existed in the flux of ionizing radiation. However, fungi seem to interact with the ionizing radiation differently from other inhabitants of the Earth. Recent data show that melanized fungal species like those from Chernobyl's reactor respond to ionizing radiation with enhanced growth. Fungi colonize space stations and adapt morphologically to extreme conditions. Radiation exposure causes upregulation of many key genes, and an inducible microhomology-mediated recombination pathway could be a potential mechanism of adaptive evolution in eukaryotes. The discovery of melanized organisms in high radiation environments, the space stations, Antarctic mountains, and in the reactor cooling water combined with phenomenon of 'radiotropism' raises the tantalizing possibility that melanins have functions analogous to other energy harvesting pigments such as chlorophylls.
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              Humans in space.

              Many successful space missions over the past 40 years have highlighted the advantages and necessity of humans in the exploration of space. But as space travel becomes ever more feasible in the twenty-first century, the health and safety of future space explorers will be paramount. In particular, understanding the risks posed by exposure to radiation and extended weightlessness will be crucial if humans are to travel far from Earth.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: SoftwareRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Project administrationRole: Writing – original draft
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2020
                24 April 2020
                : 15
                : 4
                : e0229921
                Affiliations
                [001] ESA - Advanced Concepts Team, European Space Research and Technology Centre (ESTEC), NL-2200AG Noordwijk, Netherlands
                Helmholtz Zentrum München, GERMANY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-9342-7948
                Article
                PONE-D-19-27509
                10.1371/journal.pone.0229921
                7182175
                32330147
                7cfb6b19-ccf4-4499-a917-e948b59da363
                © 2020 Vasileiou, Summerer

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 October 2019
                : 18 February 2020
                Page count
                Figures: 4, Tables: 2, Pages: 16
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Physical Sciences
                Materials Science
                Materials
                Pigments
                Organic Pigments
                Melanin
                Physical Sciences
                Materials Science
                Materials
                Composite Materials
                Physical Sciences
                Physics
                Nuclear Physics
                Radiation
                Ionizing Radiation
                Biology and Life Sciences
                Organisms
                Eukaryota
                Fungi
                Research and analysis methods
                Mathematical and statistical techniques
                Statistical methods
                Monte Carlo method
                Physical sciences
                Mathematics
                Statistics
                Statistical methods
                Monte Carlo method
                Physical Sciences
                Physics
                Nuclear Physics
                Radiation
                Biology and Life Sciences
                Mycology
                Fungal Structure
                Physical Sciences
                Physics
                Particle Physics
                Elementary Particles
                Photons
                Custom metadata
                The data underlying the study is available on the public Zenodo repository (DOI: 10.5281/zenodo.3667494).

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                Uncategorized

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