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

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          Abstract

          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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          Most cited references42

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          The contribution of melanin to microbial pathogenesis.

          Melanins are enigmatic pigments that are produced by a wide variety of microorganisms including several species of pathogenic bacteria, fungi and helminths. The study of melanin is difficult because these pigments defy complete biochemical and structural analysis. Nevertheless, the availability of new reagents in the form of monoclonal antibodies and melanin-binding peptides, combined with the application of various physical techniques, has provided insights into the process of melanization. Melanization is important in microbial pathogenesis because it has been associated with virulence in many microorganisms. Melanin appears to contribute to virulence by reducing the susceptibility of melanized microbes to host defence mechanisms. However, the interaction of melanized microbes and the host is complex and includes immune responses to melanin-related antigens. Production of melanin has also been linked to protection against environmental insults. Interference with melanization is a potential strategy for antimicrobial drug and pesticide development. The process of melanization poses fascinating problems in cell biology and provides a type of pathogenic strategy that is common to highly diverse pathogens.
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            Thermotolerance generated by plant/fungal symbiosis.

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              Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages.

              Cryptococcus neoformans (Cn) is a soil fungus that causes life-threatening meningitis in immunocompromised patients and is a facultative intracellular pathogen capable of replication inside macrophages. The mechanism by which environmental fungi acquire and maintain virulence for mammalian hosts is unknown. We hypothesized that the survival strategies for Cn after ingestion by macrophages and amoebae were similar. Microscopy, fungal and amoebae killing assays, and phagocytosis assays revealed that Cn is phagocytosed by and replicates in Acanthamoeba castellanii, which leads to death of amoebae. An acapsular strain of Cn did not survive when incubated with amoebae, but melanization protected these cells against killing by amoebae. A phospholipase mutant had a decreased replication rate in amoebae compared with isogenic strains. These observations suggest that cryptococcal characteristics that contribute to mammalian virulence also promote fungal survival in amoebae. Intracellular replication was accompanied by the accumulation of polysaccharide containing vesicles similar to those described in Cn-infected macrophages. The results suggest that the virulence of Cn for mammalian cells is a consequence of adaptations that have evolved for protection against environmental predators such as amoebae and provide an explanation for the broad host range of this pathogenic fungus.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS ONE
                plos
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2007
                23 May 2007
                : 2
                : 5
                : e457
                Affiliations
                [1 ]Department of Nuclear Medicine, Albert Einstein College of Medicine, Bronx, New York, United States of America
                [2 ]Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, United States of America
                [3 ]Physiology and Biophysics, Albert Einstein College of Medicine, Bronx, New York, United States of America
                [4 ]Medicine, Albert Einstein College of Medicine, Albert Einstein College of Medicine, Bronx, New York, United States of America
                Newcastle University, United Kingdom
                Author notes
                * To whom correspondence should be addressed. E-mail: edadacho@ 123456aecom.yu.edu

                Conceived and designed the experiments: AC ED RB. Performed the experiments: RB AS PA JN XH TM. Analyzed the data: AC ED RB XH. Contributed reagents/materials/analysis tools: PA JN. Wrote the paper: AC ED. Other: Suggested the idea for the study: AC.

                Article
                07-PONE-RA-00646R2
                10.1371/journal.pone.0000457
                1866175
                17520016
                eb4bdb5c-63a5-415d-a421-abb7a5180686
                Dadachova et al. 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
                : 21 January 2007
                : 24 April 2007
                Page count
                Pages: 13
                Categories
                Research Article
                Biophysics/Membrane Proteins and Energy Transduction
                Chemical Biology/Chemical Biology of the Cell
                Ecology/Environmental Microbiology
                Microbiology/Microbial Physiology and Metabolism

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                Uncategorized

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