Ionizing Radiation Changes the Electronic Properties of Melanin and Enhances the Growth of Melanized Fungi
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{"title"=>"Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi", "type"=>"journal", "authors"=>[{"first_name"=>"Ekaterina", "last_name"=>"Dadachova", "scopus_author_id"=>"7003945571"}, {"first_name"=>"Ruth A.", "last_name"=>"Bryan", "scopus_author_id"=>"7402594274"}, {"first_name"=>"Xianchun", "last_name"=>"Huang", "scopus_author_id"=>"13404235500"}, {"first_name"=>"Tiffany", "last_name"=>"Moadel", "scopus_author_id"=>"57194733832"}, {"first_name"=>"Andrew D.", "last_name"=>"Schweitzer", "scopus_author_id"=>"7005720391"}, {"first_name"=>"Philip", "last_name"=>"Aisen", "scopus_author_id"=>"7103155105"}, {"first_name"=>"Joshua D.", "last_name"=>"Nosanchuk", "scopus_author_id"=>"7005300850"}, {"first_name"=>"Arturo", "last_name"=>"Casadevall", "scopus_author_id"=>"35372929500"}], "year"=>2007, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"352646910", "sgr"=>"40549101984", "issn"=>"19326203", "pmid"=>"17520016", "scopus"=>"2-s2.0-40549101984", "doi"=>"10.1371/journal.pone.0000457", "isbn"=>"1932-6203"}, "id"=>"8d1f43d7-ecd6-35f3-8ab4-dec559d9c778", "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.\\n\\nMETHODOLOGY/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 (14)C-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.\\n\\nCONCLUSIONS/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.", "link"=>"http://www.mendeley.com/research/ionizing-radiation-changes-electronic-properties-melanin-enhances-growth-melanized-fungi", "reader_count"=>331, "reader_count_by_academic_status"=>{"Unspecified"=>9, "Professor > Associate Professor"=>16, "Researcher"=>74, "Student > Doctoral Student"=>19, "Student > Ph. D. Student"=>85, "Student > Postgraduate"=>14, "Student > Master"=>41, "Other"=>10, "Student > Bachelor"=>49, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>9}, "reader_count_by_user_role"=>{"Unspecified"=>9, "Professor > Associate Professor"=>16, "Researcher"=>74, "Student > Doctoral Student"=>19, "Student > Ph. D. Student"=>85, "Student > Postgraduate"=>14, "Student > Master"=>41, "Other"=>10, "Student > Bachelor"=>49, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>9}, "reader_count_by_subject_area"=>{"Unspecified"=>18, "Agricultural and Biological Sciences"=>180, "Arts and Humanities"=>3, "Chemistry"=>23, "Computer Science"=>3, "Earth and Planetary Sciences"=>8, "Engineering"=>14, "Environmental Science"=>15, "Biochemistry, Genetics and Molecular Biology"=>29, "Nursing and Health Professions"=>2, "Materials Science"=>4, "Mathematics"=>1, "Medicine and Dentistry"=>10, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Sports and Recreations"=>1, "Physics and Astronomy"=>10, "Social Sciences"=>1, "Immunology and Microbiology"=>7}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Social Sciences"=>{"Social Sciences"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>10}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>18}, "Environmental Science"=>{"Environmental Science"=>15}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}, "Arts and Humanities"=>{"Arts and Humanities"=>3}, "Engineering"=>{"Engineering"=>14}, "Chemistry"=>{"Chemistry"=>23}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>8}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>180}, "Computer Science"=>{"Computer Science"=>3}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>29}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>19, "Philippines"=>1, "Japan"=>2, "United Kingdom"=>2, "Kenya"=>1, "Belarus"=>1, "Portugal"=>1, "Canada"=>3, "Netherlands"=>1, "Belgium"=>2, "Finland"=>1, "Brazil"=>1, "Poland"=>2, "Italy"=>2, "Mexico"=>1, "South Africa"=>1, "France"=>2, "Nigeria"=>1, "Chile"=>1, "Germany"=>2}, "group_count"=>14}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/950301"], "description"=>"<p>rad - irradiated, ctrl - control, mel - melanized, suc- sucrose added. The volume of half-sphere was calculated as V/2 = π/12 d<sup>3</sup>. Radial linear growth rate of <i>C. sphaerospermum</i> colonies was calculated as K = (R<sub>t</sub>−R<sub>o</sub>)/(t−t<sub>o</sub>), where K is radial linear growth rate, mm/hr; R<sub>t</sub> and R<sub>o</sub> - colony radii at time t and time t<sub>o</sub>, respectively.</p>", "links"=>[], "tags"=>["non-melanized", "melanized", "sphaerospermum", "cells", "gamma", "radial", "melanin-deficient", "colonies", "grown", "agar", "plates", "sucrose"], "article_id"=>620608, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g007", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Survival_of_non_melanized_and_melanized_C_sphaerospermum_cells_following_exposure_to_external_gamma_rays_average_volume_left_side_plates_and_radial_growth_rate_right_side_plates_of_melanized_and_melanin_deficient_C_sphaerospermum_colonies_grown_on_agar_p/620608", "title"=>"Survival of non-melanized and melanized C. sphaerospermum cells following exposure to external gamma rays: average volume (left side plates) and radial growth rate (right side plates) of melanized and melanin-deficient <i>C. sphaerospermum</i> colonies grown on agar plates with (top panels) or without (bottom panels) sucrose in a radiation field of 0.05 mGy/hr or at background radiation level (control).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:31:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/950499"], "description"=>"<p>50 µg of <i>C. neoformans</i> melanin was used in the reactions; melanin was subjected to 40 min treatment, placed into dry ice following treatments and taken up in the ferricyanide solution immediately before measurements. To exclude contribution of heat component during irradiation of melanin with 250 W light, the samples were placed in 25°C water bath.</p>", "links"=>[], "tags"=>["electron-transfer", "melanin", "coupled", "forms", "electromagnetic"], "article_id"=>620807, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.t002", "stats"=>{"downloads"=>4, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increase_in_electron_transfer_properties_of_melanin_in_NADH_ferricyanide_coupled_reaction_after_exposure_to_different_forms_of_electromagnetic_radiation_/620807", "title"=>"Increase in electron-transfer properties of melanin in NADH/ferricyanide coupled reaction after exposure to different forms of electromagnetic radiation", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:32:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/950460"], "description"=>"1<p>V - initial velocity is expressed in nanomoles of ferricyanide reduced per min.</p>", "links"=>[], "tags"=>["untreated", "irradiated"], "article_id"=>620776, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.t001", "stats"=>{"downloads"=>1, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NADH_ferricyanide_melanin_reaction_in_presence_of_untreated_and_irradiated_C_neoformans_melanin_/620776", "title"=>"NADH-ferricyanide-melanin reaction in presence of untreated and irradiated <i>C. neoformans</i> melanin", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:32:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/950183"], "description"=>"<p>a) growth of melanized H99 cells; b) growth of non-melanized Lac(-) H99 cells; c) incorporation of <sup>14</sup>C-acetate into melanized H99 cells; d) incorporation of <sup>14</sup>C-acetate into non-melanized Lac(-) H99 cells; e) ratio of irradiated to non-irradiated cells CFUs and cpms ratios (normalized CFUs and cpms) for melanized H99 and non-melanized Lac(-) H99 cells.</p>", "links"=>[], "tags"=>["incorporation", "melanized", "neoformans", "h99", "cells", "non-melanized", "lacking", "laccase", "enzyme", "nutrients"], "article_id"=>620489, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g006", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Growth_and_incorporation_of_14_C_acetate_by_melanized_C_neoformans_H99_cells_and_non_melanized_Lac_H99_cells_lacking_the_laccase_enzyme_under_conditions_of_limited_nutrients_supply_in_a_radiation_field_of_0_05_mGy_hr_or_at_background_radiation_level_/620489", "title"=>"Growth and incorporation of <sup>14</sup>C-acetate by melanized C. neoformans H99 cells and non-melanized Lac(-) H99 cells lacking the laccase enzyme under conditions of limited nutrients supply in a radiation field of 0.05 mGy/hr or at background radiation level.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:30:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/949791"], "description"=>"<p>PDCA - pyrrole-2,3-dicarboxylic acid; PTCA - pyrrole-2,3,5-tricarboxylic acid; TTCA - 1,3-thiazole-2,4,5-tricarboxylic acid; TDCA - 1,3-thiazole-4,5-dicarboxylic acid. Absorption was monitored at 255 nm and displayed on a linear scale. Cs - <i>C. sphaerospermum</i>.</p>", "links"=>[], "tags"=>["melanin", "derived", "grown", "dextrose", "sabaroud", "agar"], "article_id"=>620106, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g003", "stats"=>{"downloads"=>3, "page_views"=>65, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HPLC_of_melanin_derived_from_C_sphaerospermum_grown_on_different_substrates_a_potato_dextrose_agar_b_Sabaroud_dextrose_agar_c_water_agar_with_casein_d_water_agar_with_dextrose_/620106", "title"=>"HPLC of melanin derived from <i>C. sphaerospermum</i> grown on different substrates: a) potato dextrose agar; b) Sabaroud dextrose agar; c) water agar with casein; d) water agar with dextrose.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:28:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/949962"], "description"=>"<p>Differences in <i>C. sphaerospermum</i> ESR spectra in comparison with <i>C. neoformans</i> are marked with arrows. ESR spectra were obtained by suspending “ghosts” in water. Ordinate is the derivative of the ESR absorption in arbitrary units. Cs - <i>C. sphaerospermum.</i></p>", "links"=>[], "tags"=>["spectra", "melanin", "derived", "grown", "dextrose", "sabaroud", "agar", "impregnated", "25"], "article_id"=>620268, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g004", "stats"=>{"downloads"=>4, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ESR_spectra_of_melanin_derived_from_C_sphaerospermum_grown_on_different_substrates_a_potato_dextrose_agar_b_Sabaroud_dextrose_agar_c_potato_dextrose_agar_impregnated_with_25_g_mL_tricyclazole_/620268", "title"=>"ESR spectra of melanin derived from <i>C. sphaerospermum</i> grown on different substrates: a) potato dextrose agar; b) Sabaroud dextrose agar; c) potato dextrose agar impregnated with 25 µg/mL tricyclazole.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:29:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/949661"], "description"=>"<p>a) structure of eumelanin oligomer; b) structure of pheomelanin oligomer; (c – f) HPLC of permanganate-oxidized melanins: c) chromatogram of background solution; d) <i>C. neoformans;</i> e) <i>C. sphaerospermum</i> grown on Sabaroud dextrose agar; f) <i>W. dermatitidis</i> isolate 8656 (wild type); (g–i) ESR spectra: g) <i>W. dermatitidis</i> isolate 8656; h) <i>C. neoformans</i> before irradiation; i) <i>C. neoformans</i> after irradiation with 0.3 kGy dose. PDCA - pyrrole-2,3-dicarboxylic acid; PTCA - pyrrole-2,3,5-tricarboxylic acid; TTCA - 1,3-thiazole-2,4,5-tricarboxylic acid; TDCA - 1,3-thiazole-4,5-dicarboxylic acid. Absorption was monitored at 255 nm and displayed on a linear scale. ESR spectra were obtained by suspending “ghosts” in water except for (h) which was performed in dry state. Ordinate in g–i is the derivative of the ESR absorption in arbitrary units.</p>", "links"=>[], "tags"=>["paramagnetic"], "article_id"=>619981, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g002", "stats"=>{"downloads"=>5, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_composition_and_paramagnetic_properties_of_melanin_/619981", "title"=>"Chemical composition and paramagnetic properties of melanin:", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:27:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/950536"], "description"=>"*<p>Wilcoxon non-parametric test for unpaired data was performed for each strain to compare doubling times for irradiated and control samples. Doubling time = ln 2/((ln(A/A<sub>o</sub>)/t), where A-amount of cells at time t, A<sub>o</sub> – amount of cells at time 0.</p>", "links"=>[], "tags"=>["times", "grown", "nutrient-deficient", "means", "sem", "experiments"], "article_id"=>620846, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.t003", "stats"=>{"downloads"=>7, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Doubling_times_for_W_dermatitidis_grown_in_nutrient_deficient_medium_with_and_without_radiation_The_means_and_SEM_of_4_experiments_are_presented_/620846", "title"=>"Doubling times for <i>W. dermatitidis</i> grown in nutrient-deficient medium with and without radiation. The means and SEM of 4 experiments are presented.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:33:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/950409"], "description"=>"<p>a) wild type 8656; b) albino mutant <i>wdpks1Δ-1</i> with a disrupted polyketide synthase gene; c) a strain complemented with wild type gene <i>wdpks1</i>. The cells were grown under conditions of limited nutrients in a radiation field of 0.05 mGy/hr or at background radiation level. The cells were exposed to radiation for various times and plated for CFUs on YPD.</p>", "links"=>[], "tags"=>["biophysics/membrane proteins and energy transduction", "chemical biology/chemical biology of the cell", "ecology/environmental microbiology", "microbiology/microbial physiology and metabolism"], "article_id"=>620724, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g008", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Growth_of_W_dermatitidis_/620724", "title"=>"Growth of <i>W. dermatitidis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:32:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/950098"], "description"=>"<p>a, b) irradiated and non-irradiated cells: a) XTT; b) MTT. c) XTT of cells grown at room temperature (22°C) or at 30°C. The cells were kept in the dark while being exposed to ionizing radiation or different temperatures. Following the exposure, XTT or MTT reagents were added to the samples and absorbance was measured at 492 or 550 nm for XTT and MTT, respectively.</p>", "links"=>[], "tags"=>["ionizing", "metabolic", "melanized", "non-melanized"], "article_id"=>620412, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g005", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_influence_of_ionizing_radiation_or_heat_on_the_metabolic_activity_of_melanized_and_non_melanized_C_neoformans_cells_/620412", "title"=>"The influence of ionizing radiation or heat on the metabolic activity of melanized and non-melanized <i>C. neoformans</i> cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:30:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/949520"], "description"=>"<p>a) light microscopy image of <i>C. neoformans</i> melanin “ghosts”; (b–e) TEM images of <i>C. sphaerospermum</i> “ghosts” derived from cells grown on nutrient rich or nutrient-deficient media: b) potato dextrose agar; c) Sabaroud dextrose agar; d) water agar with casein; e) water agar with dextrose. Original magnification: light microscopy image – X 1,000; TEM images – X 13,000.</p>", "links"=>[], "tags"=>["images", "melanized", "fungal"], "article_id"=>619839, "categories"=>["Medicine", "Ecology", "Microbiology", "Biophysics"], "users"=>["Ekaterina Dadachova", "Ruth A. Bryan", "Xianchun Huang", "Tiffany Moadel", "Andrew D. Schweitzer", "Philip Aisen", "Joshua D. Nosanchuk", "Arturo Casadevall"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000457.g001", "stats"=>{"downloads"=>2, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microscopic_images_of_melanized_fungal_cells_/619839", "title"=>"Microscopic images of melanized fungal cells:", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:26:45"}

PMC Usage Stats | Further Information

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Relative Metric

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