The Alcohol Dehydrogenase System in the Xylose-Fermenting Yeast Candida maltosa
Publication Date
July 23, 2010
Journal
PLoS ONE
Authors
Yuping Lin, Peng He, Qinhong Wang, Dajun Lu, et al
Volume
5
Issue
7
Pages
e11752
DOI
https://dx.plos.org/10.1371/journal.pone.0011752
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0011752
Web of Science
000280243800022
Scopus
77955406115
Mendeley
http://www.mendeley.com/research/alcohol-dehydrogenase-system-xylosefermenting-yeast-candida-maltosa
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Mendeley | Further Information

{"title"=>"The alcohol dehydrogenase system in the xylose-fermenting yeast candida maltosa", "type"=>"journal", "authors"=>[{"first_name"=>"Yuping", "last_name"=>"Lin", "scopus_author_id"=>"19640414400"}, {"first_name"=>"Peng", "last_name"=>"He", "scopus_author_id"=>"56763290400"}, {"first_name"=>"Qinhong", "last_name"=>"Wang", "scopus_author_id"=>"9237077600"}, {"first_name"=>"Dajun", "last_name"=>"Lu", "scopus_author_id"=>"7403079595"}, {"first_name"=>"Zilong", "last_name"=>"Li", "scopus_author_id"=>"55787040600"}, {"first_name"=>"Changsheng", "last_name"=>"Wu", "scopus_author_id"=>"56132580400"}, {"first_name"=>"Ning", "last_name"=>"Jiang", "scopus_author_id"=>"55547127950"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77955406115", "pui"=>"359319263", "doi"=>"10.1371/journal.pone.0011752", "isbn"=>"1932-6203", "sgr"=>"77955406115", "pmid"=>"20668703"}, "id"=>"20d66c44-333f-3169-b8ad-f7f3c1a723a6", "abstract"=>"BACKGROUND: The alcohol dehydrogenase (ADH) system plays a critical role in sugar metabolism involving in not only ethanol formation and consumption but also the general \"cofactor balance\" mechanism. Candida maltosa is able to ferment glucose as well as xylose to produce a significant amount of ethanol. Here we report the ADH system in C. maltosa composed of three microbial group I ADH genes (CmADH1, CmADH2A and CmADH2B), mainly focusing on its metabolic regulation and physiological function.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Genetic analysis indicated that CmADH2A and CmADH2B tandemly located on the chromosome could be derived from tandem gene duplication. In vitro characterization of enzymatic properties revealed that all the three CmADHs had broad substrate specificities. Homo- and heterotetramers of CmADH1 and CmADH2A were demonstrated by zymogram analysis, and their expression profiles and physiological functions were different with respect to carbon sources and growth phases. Fermentation studies of ADH2A-deficient mutant showed that CmADH2A was directly related to NAD regeneration during xylose metabolism since CmADH2A deficiency resulted in a significant accumulation of glycerol.\\n\\nCONCLUSIONS/SIGNIFICANCE: Our results revealed that CmADH1 was responsible for ethanol formation during glucose metabolism, whereas CmADH2A was glucose-repressed and functioned to convert the accumulated ethanol to acetaldehyde. To our knowledge, this is the first demonstration of function separation and glucose repression of ADH genes in xylose-fermenting yeasts. On the other hand, CmADH1 and CmADH2A were both involved in ethanol formation with NAD regeneration to maintain NADH/NAD ratio in favor of producing xylitol from xylose. In contrast, CmADH2B was expressed at a much lower level than the other two CmADH genes, and its function is to be further confirmed.", "link"=>"http://www.mendeley.com/research/alcohol-dehydrogenase-system-xylosefermenting-yeast-candida-maltosa", "reader_count"=>37, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>10, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>10, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>3, "Nursing and Health Professions"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>26, "Medicine and Dentistry"=>1, "Sports and Recreations"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>26}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"South Africa"=>2, "Thailand"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/839380"], "description"=>"<p><i>C. maltosa</i> cells were grown in YP medium containing different carbon sources under aerobic conditions: 80 g/l glucose (D), 2% (V/V) ethanol (E), 2% (V/V) glycerol (G), and 80 g/l xylose (X). Cells were harvested in the mid-exponential phase (for 12 h in glucose medium, 16 h in ethanol or glycerol medium and 24 h in xylose medium) for quantitative real-time RT-PCR.</p>", "links"=>[], "tags"=>["levels", "cmadh", "genes", "xu316", "changes", "adh2a-deficient", "mutant", "m3-400"], "article_id"=>509824, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_mRNA_levels_of_three_CmADH_genes_in_wide_type_strain_Xu316_A_and_their_changes_in_ADH2A_deficient_mutant_M3_400_B_/509824", "title"=>"mRNA levels of three CmADH genes in wide type strain Xu316 (A) and their changes in ADH2A-deficient mutant M3-400 (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:43:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/838849"], "description"=>"<p>ADH duplication events are shown in gray boxes. The topology of the phylogenetic relationships was a composite drawn from several sources <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Butler1\" target=\"_blank\">[15]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Fitzpatrick1\" target=\"_blank\">[46]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Gordon1\" target=\"_blank\">[47]</a>. Major clades were named, including the <i>Saccharomyces</i> complex, the CTG clade containing species that translate codon CTG as serine instead of leucine, the group of species that share the whole-genome duplication (WGD) and the <i>Saccharomyces sensu stricto</i> group. The ADH gene duplication and gene loss events in the CTG clade were deduced based on comparative analysis of the genomic contexts of ADH homologs from species of this clade (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752.s005\" target=\"_blank\">Figure S3</a>). The ADH duplication events in the <i>Saccharomyces</i> complex were reported previously <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Thomson1\" target=\"_blank\">[6]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Shain1\" target=\"_blank\">[18]</a>, and confirmed with the genomic contexts of ADH homologs from the Yeast Gene Order Browser (YGOB), an online tool for visualizing comparative genomics of yeasts <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011752#pone.0011752-Gordon1\" target=\"_blank\">[47]</a>. ADH1/ADH5 ortholog pair was retained in <i>S. cerevisiae</i> and one copy has been lost in <i>Candida glabrata</i>. <i>K. lactis</i>, a pre-WGD yeast, has duplicated the ADH genes independently more than once after separating from the post-WGD yeast species.</p>", "links"=>[], "tags"=>["events", "adh", "genes", "saccharomycotina"], "article_id"=>509296, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g001", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Minimum_number_of_events_required_to_explain_evolution_of_ADH_genes_in_some_Saccharomycotina_species_/509296", "title"=>"Minimum number of events required to explain evolution of ADH genes in some Saccharomycotina species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:34:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/839426"], "description"=>"<p>Shown are mean and S.E. (<i>n</i> = 3).</p>", "links"=>[], "tags"=>["properties", "cmadh2a"], "article_id"=>509883, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetic_properties_of_CmADH1_CmADH2A_and_CmADH2B_/509883", "title"=>"Kinetic properties of CmADH1, CmADH2A and CmADH2B.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-23 02:44:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/839297"], "description"=>"<p>Glucose or xylose (<i>open cycles</i>) concentration, ethanol (<i>open triangles</i>) and xylitol (<i>open squares</i>) concentrations, and cell density (<i>open diamonds</i>) were determined at various times after inoculation. Crude extracts were prepared from cells at various times for zymogram analysis. Amounts of each gel were 100 µg or 10 µg.</p>", "links"=>[], "tags"=>["cmadh", "isozymes", "xu316", "glucose", "xylose", "metabolism", "aerobic"], "article_id"=>509744, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expressions_of_CmADH_isozymes_of_C_maltosa_Xu316_during_glucose_A_or_xylose_B_metabolism_under_aerobic_conditions_/509744", "title"=>"Expressions of CmADH isozymes of <i>C. maltosa</i> Xu316 during glucose (A) or xylose (B) metabolism under aerobic conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:42:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/417942", "https://ndownloader.figshare.com/files/417977", "https://ndownloader.figshare.com/files/418015", "https://ndownloader.figshare.com/files/418101", "https://ndownloader.figshare.com/files/418140", "https://ndownloader.figshare.com/files/418188"], "description"=>"<div><h3>Background</h3><p>The alcohol dehydrogenase (ADH) system plays a critical role in sugar metabolism involving in not only ethanol formation and consumption but also the general “cofactor balance” mechanism. <em>Candida maltosa</em> is able to ferment glucose as well as xylose to produce a significant amount of ethanol. Here we report the ADH system in <em>C. maltosa</em> composed of three microbial group I ADH genes (<em>CmADH1</em>, <em>CmADH2A</em> and <em>CmADH2B</em>), mainly focusing on its metabolic regulation and physiological function.</p><h3>Methodology/Principal Findings</h3><p>Genetic analysis indicated that <em>CmADH2A</em> and <em>CmADH2B</em> tandemly located on the chromosome could be derived from tandem gene duplication. <em>In vitro</em> characterization of enzymatic properties revealed that all the three CmADHs had broad substrate specificities. Homo- and heterotetramers of CmADH1 and CmADH2A were demonstrated by zymogram analysis, and their expression profiles and physiological functions were different with respect to carbon sources and growth phases. Fermentation studies of ADH2A-deficient mutant showed that <em>CmADH2A</em> was directly related to NAD regeneration during xylose metabolism since CmADH2A deficiency resulted in a significant accumulation of glycerol.</p><h3>Conclusions/Significance</h3><p>Our results revealed that <em>CmADH1</em> was responsible for ethanol formation during glucose metabolism, whereas <em>CmADH2A</em> was glucose-repressed and functioned to convert the accumulated ethanol to acetaldehyde. To our knowledge, this is the first demonstration of function separation and glucose repression of ADH genes in xylose-fermenting yeasts. On the other hand, <em>CmADH1</em> and <em>CmADH2A</em> were both involved in ethanol formation with NAD regeneration to maintain NADH/NAD ratio in favor of producing xylitol from xylose. In contrast, <em>CmADH2B</em> was expressed at a much lower level than the other two CmADH genes, and its function is to be further confirmed.</p></div>", "links"=>[], "tags"=>["dehydrogenase", "xylose-fermenting", "yeast"], "article_id"=>142525, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011752.s001", "https://dx.doi.org/10.1371/journal.pone.0011752.s002", "https://dx.doi.org/10.1371/journal.pone.0011752.s003", "https://dx.doi.org/10.1371/journal.pone.0011752.s004", "https://dx.doi.org/10.1371/journal.pone.0011752.s005", "https://dx.doi.org/10.1371/journal.pone.0011752.s006"], "stats"=>{"downloads"=>10, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Alcohol_Dehydrogenase_System_in_the_Xylose_Fermenting_Yeast_Candida_maltosa_/142525", "title"=>"The Alcohol Dehydrogenase System in the Xylose-Fermenting Yeast <em>Candida maltosa</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-07-23 00:42:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/838997"], "description"=>"<p>The standard proteins were applied to lane M.</p>", "links"=>[], "tags"=>["purified", "recombinant", "cmadh1", "cmadh2a", "cmadh2b", "10"], "article_id"=>509436, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SDS_PAGE_of_purified_recombinant_CmADH1_lane_1_5_181_g_CmADH2A_lane_2_5_181_g_and_CmADH2B_lane_3_10_181_g_/509436", "title"=>"SDS-PAGE of purified recombinant CmADH1 (lane 1, 5 µg), CmADH2A (lane 2, 5 µg) and CmADH2B (lane 3, 10 µg).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:37:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/839055"], "description"=>"<p>Relative specific activities of 100% corresponded to the specific activity on ethanol. The values were expressed as percent of the rate obtained with ethanol as substrates. Shown are mean ± S.E. (n = 3). <i>ND</i>, no detectable activity.</p>", "links"=>[], "tags"=>["cmadh2a", "cmadh2b"], "article_id"=>509509, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g003", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_specific_activity_of_CmADH1_CmADH2A_and_CmADH2B_on_various_alcohols_/509509", "title"=>"Relative specific activity of CmADH1, CmADH2A and CmADH2B on various alcohols.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:38:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/839167"], "description"=>"<p>Lane 1 in all figures and lane 2 in <b>A</b> and <b>D</b>: crude extracts from Xu316 cells grown for 18 h in YP medium containing 80 g/l xylose. Lane 3 in <b>A</b>, lane 2 and 3 in <b>B</b>, and lane 2 in <b>C</b>: crude extracts from <i>E. coli</i> BL21(DE3) overexpressing the recombinant CmADH1 (<b>A</b>), CmADH2A (<b>B</b>) and CmADH2B (<b>C</b>) without His-tags, respectively. <b>D.</b> Mixed crude extracts of the recombinant CmADH1 and CmADH2A. Amounts of proteins were given on the bottom of the lanes. Hypothetical isozyme composition of the major ADH bands in the electrophoretic pattern of <i>C. maltosa</i> was shown on the right of the lanes.</p>", "links"=>[], "tags"=>["adh", "isozymes", "xu316", "recombinant"], "article_id"=>509619, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Zymogram_analysis_of_ADH_isozymes_from_C_maltosa_Xu316_and_recombinant_E_coli_BL21_DE3_/509619", "title"=>"Zymogram analysis of ADH isozymes from <i>C. maltosa</i> Xu316 and recombinant <i>E. coli</i> BL21(DE3).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:40:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/839465"], "description"=>"<p>NA, not applicable; ND, not detected.</p>", "links"=>[], "tags"=>["fermentative", "parameters", "adh2a-deficient", "mutant"], "article_id"=>509921, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.t002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_fermentative_parameters_of_wild_type_strain_Xu316_and_ADH2A_deficient_mutant_M3_400_of_C_maltosa_/509921", "title"=>"Comparison of fermentative parameters of wild type strain (Xu316) and ADH2A-deficient mutant (M3-400) of <i>C. maltosa</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-23 02:45:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/839234"], "description"=>"<p><i>C. maltosa</i> cells were grown in YP medium containing different carbon sources: 80 g/l glucose (D), 2% (V/V) ethanol (E), 2% (V/V) glycerol (G), 80 g/l glucose and 2% (V/V) ethanol (D•E), 80 g/l glucose and 2% (V/V) glycerol (D•G), 80 g/l xylose (X), 80 g/l xylose and 2% (V/V) ethanol (X•E), and 80 g/l xylose and 2% (V/V) glycerol (X•G). Crude extracts (110 µg protein) were prepared from cells in the mid-exponential phase (for 12 h) for zymogram analysis.</p>", "links"=>[], "tags"=>["cmadh", "isozymes", "xu316", "carbon"], "article_id"=>509682, "categories"=>["Biotechnology", "Microbiology", "Molecular Biology"], "users"=>["Yuping Lin", "Peng He", "Qinhong Wang", "Dajun Lu", "Zilong Li", "Changsheng Wu", "Ning Jiang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011752.g005", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_CmADH_isozymes_of_C_maltosa_Xu316_on_different_carbon_sources_/509682", "title"=>"Expression of CmADH isozymes of <i>C. maltosa</i> Xu316 on different carbon sources.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-23 02:41:22"}

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  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"8", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2014", "month"=>"11"}
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  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
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  • {"unique-ip"=>"14", "full-text"=>"26", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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Relative Metric

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