The Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose
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{"title"=>"The putative endoglucanase pcGH61D from phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose", "type"=>"journal", "authors"=>[{"first_name"=>"Bjørge", "last_name"=>"Westereng", "scopus_author_id"=>"23135999100"}, {"first_name"=>"Takuya", "last_name"=>"Ishida", "scopus_author_id"=>"7403961709"}, {"first_name"=>"Gustav", "last_name"=>"Vaaje-Kolstad", "scopus_author_id"=>"8702321200"}, {"first_name"=>"Miao", "last_name"=>"Wu", "scopus_author_id"=>"55510461400"}, {"first_name"=>"Vincent G H", "last_name"=>"Eijsink", "scopus_author_id"=>"7006656581"}, {"first_name"=>"Kiyohiko", "last_name"=>"Igarashi", "scopus_author_id"=>"7402350297"}, {"first_name"=>"Masahiro", "last_name"=>"Samejima", "scopus_author_id"=>"7006742999"}, {"first_name"=>"Jerry", "last_name"=>"Ståhlberg", "scopus_author_id"=>"7003490209"}, {"first_name"=>"Svein J.", "last_name"=>"Horn", "scopus_author_id"=>"7103259928"}, {"first_name"=>"Mats", "last_name"=>"Sandgren", "scopus_author_id"=>"6701754824"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"362967357", "sgr"=>"81755166559", "issn"=>"19326203", "pmid"=>"22132148", "scopus"=>"2-s2.0-81755166559", "doi"=>"10.1371/journal.pone.0027807", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"842a16a8-0701-3e05-b54f-213792b34371", "abstract"=>"Many fungi growing on plant biomass produce proteins currently classified as glycoside hydrolase family 61 (GH61), some of which are known to act synergistically with cellulases. In this study we show that PcGH61D, the gene product of an open reading frame in the genome of Phanerochaete chrysosporium, is an enzyme that cleaves cellulose using a metal-dependent oxidative mechanism that leads to generation of aldonic acids. The activity of this enzyme and its beneficial effect on the efficiency of classical cellulases are stimulated by the presence of electron donors. Experiments with reduced cellulose confirmed the oxidative nature of the reaction catalyzed by PcGH61D and indicated that the enzyme may be capable of penetrating into the substrate. Considering the abundance of GH61-encoding genes in fungi and genes encoding their functional bacterial homologues currently classified as carbohydrate binding modules family 33 (CBM33), this enzyme activity is likely to turn out as a major determinant of microbial biomass-degrading efficiency.", "link"=>"http://www.mendeley.com/research/putative-endoglucanase-pcgh61d-phanerochaete-chrysosporium-metaldependent-oxidative-enzyme-cleaves-c", "reader_count"=>178, "reader_count_by_academic_status"=>{"Unspecified"=>6, "Professor > Associate Professor"=>11, "Researcher"=>43, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>55, "Student > Postgraduate"=>3, "Student > Master"=>30, "Other"=>7, "Student > Bachelor"=>10, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>9}, "reader_count_by_user_role"=>{"Unspecified"=>6, "Professor > Associate Professor"=>11, "Researcher"=>43, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>55, "Student > Postgraduate"=>3, "Student > Master"=>30, "Other"=>7, "Student > Bachelor"=>10, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>9}, "reader_count_by_subject_area"=>{"Unspecified"=>17, "Engineering"=>7, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>29, "Materials Science"=>1, "Agricultural and Biological Sciences"=>106, "Medicine and Dentistry"=>3, "Chemical Engineering"=>2, "Physics and Astronomy"=>1, "Chemistry"=>11}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>7}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>11}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>106}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>29}, "Unspecified"=>{"Unspecified"=>17}, "Environmental Science"=>{"Environmental Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>2}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "Norway"=>3, "Finland"=>1, "Brazil"=>1, "United Kingdom"=>1, "Italy"=>1, "Mexico"=>1, "Thailand"=>1}, "group_count"=>7}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/710027"], "description"=>"<p>Panel <b>A</b> displays a MALDI-TOF-MS spectrum of reduced PASC, showing peak series differing by <i>m/z</i> 162-repeats, typical for hexose oligosaccharides, up to <i>m/z</i> 4000. Note that the reduction is not complete; the close-up to the right shows that the 1177, 1339 and 1501 peaks, corresponding the reduced heptamer, octamer and nonamer, respectively, are accompanied by a peak corresponding to the native oligosaccharides with <i>m/z</i> -2 (two protons less). The reduced PASC (0.1%) was incubated with 40 µg/mL <i>Pc</i>GH61D in 20mM Tris buffer pH 6.5, 1.0 mM ascorbic acid, at 50°C, and samples were taken at 90 minutes, 4 and 20 hours. The MALDI-TOF-mass spectrum of the 4 hour sample (Panel <b>B</b>) and clearly shows reduced products (their <i>m/z</i> values are indicated). The close-up to the right shows the various pentameric products (sodium adducts are marked): the DP5 lactone, <i>m/z</i> = 849; DP5, <i>m/z</i> = 851 (minor amount, not labelled); reduced DP5, <i>m/z</i> = 853.3; DP5<sub>ox</sub>, <i>m/z</i> = 867.3; sodium salt of DP5<sub>ox</sub> (-H<sup>+</sup>, +Na<sup>+</sup>), <i>m/z</i> = 889.2).</p>", "links"=>[], "tags"=>["reduced"], "article_id"=>380382, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g007", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_Pc_GH61D_on_reduced_cellulose_/380382", "title"=>"Effect of <i>Pc</i>GH61D on reduced cellulose.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:26:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/709685"], "description"=>"<p>Panel <b>A</b> shows a typical HPAEC chromatogram of products obtained upon incubation of 0.1% PASC with 40 µg/mL <i>Pc</i>GH61D in 25mM Tris (not MES which is not good for MALDI) pH 6.5, 1mM ascorbic acid (not reduced glutathione which is not good for MALDI), overnight at 50°C. The chromatogram shows a range of oxidized oligosaccharides (DP 4-10) as well as native oligosaccharides (for information on chromatographic standards, see Forsberg <i>et al</i>. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#pone.0027807-Forsberg1\" target=\"_blank\">[7]</a>). Panel <b>B</b> shows the MALDI spectrum of the same sample as in Panel <b>A</b> focusing on the most prominent masses in the spectrum. All ion clusters for oxidized products had a similar distribution, the most abundant peak being the Na-adduct of the aldonic acid, which is annotated with DPn<sub>ox</sub> and its <i>m/z</i>. Panel <b>C</b> displays the MALDI-TOF-mass spectrum of the same sample as in panel <b>B</b> after saturation with lithium (20 mM) to obtain lithium adducts only. This was done to eliminate the possibility that the compound annotated as the aldonic acid in fact was a K-adduct of the native oligosaccharide (which would give the same mass as the Na-adduct of the oxidized oligosaccharide). Indeed Li-adducts ([M+Li]) and the corresponding lithium salt of the lithium adduct [M+2Li-H]) occur in pairs throughout the spectrum replacing completely the more complex cluster of Na- and K-adducts/salts (<i>m/z</i> -16 relative to the sodium adducts of panel <b>B</b>; only the lithium adducts of the aldonic acids are annotated). This confirms the presence of aldonic acids. For further clarification a detailed view of the ion cluster for DP6<sub>ox</sub> (Glc<sub>5</sub>GlcA) from Panel <b>B</b> is shown in Panel <b>D</b>. The cluster contains the Na-adducts of the gluconolacton (DP6<sub>La</sub>, <i>m/z</i> 1011), cellohexaose (DP6, <i>m/z</i> 1013) and oxidized cellohexaose (DP6<sub>ox</sub>; <i>m/z</i> 1029). In addition, the spectrum shows the Na-salt of the Na-adduct of DP6<sub>ox</sub> (<i>m/z</i> 1051), the K-adduct of DP6<sub>ox</sub> (<i>m/z</i> 1045) and the Na-salt of the K-adduct of DP6<sub>ox</sub> (<i>m/z</i> 1067). To verify the presence and position of the acid group, MS<sup>2</sup> experiments were done for several ions. Panel <b>E</b> displays fragments obtained for DP6<sub>ox</sub> (<i>m/z</i> 1029) with fragment ions named according to the Domon and Costello nomenclature <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#pone.0027807-Domon1\" target=\"_blank\">[34]</a>. The spectrum corresponds to that of a cello-oligosaccharide with an aldonic acid in the reducing end, and repeating hexose units towards the non-reducing end. The nomenclature used for products throughout this report is: DPn, cello-oligosaccharide with n glucose residues; DPn<sub>ox</sub>, cello-oligosaccharides with n-1 glucose residues + one gluconic acid [Glc<sub>(n-1)</sub>GlcA]; DPn<sub>LA</sub>, cello-oligosaccharides with n-1 glucose residues + one gluconolactone [Glc<sub>(n-1)</sub>GlcLA].</p>", "links"=>[], "tags"=>["generated", "cellulose"], "article_id"=>380038, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g003", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Products_generated_from_cellulose_by_Pc_GH61D_/380038", "title"=>"Products generated from cellulose by <i>Pc</i>GH61D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:24:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/709422"], "description"=>"<p>Lanes: 1 & 5, marker (Precision Plus Protein™ Dual Color Standards; BioRad); lane 2, culture medium of the <i>P. pastoris</i> strain; lane 3, EndoH treated culture medium; lane 4, EndoH treated culture medium after enterokinase treatment. Lane 6 & 7, protein bands with Mw of 25 and 27 kDa, respectively. The protein band used for N-terminal sequencing is indicated by an arrow.</p>", "links"=>[], "tags"=>["recombinantly"], "article_id"=>379764, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g001", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SDS_PAGE_analysis_of_recombinantly_expressed_Pc_GH61D_/379764", "title"=>"SDS-PAGE analysis of recombinantly expressed <i>Pc</i>GH61D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:23:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/709575"], "description"=>"<p>Panel <b>A</b> shows a structure-based sequence alignment of <i>Pc</i>GH61D and GH61A from <i>Thermoascus aurantiacus</i> with GH61s with known crystal structures, <i>Tt</i>GH61E and <i>Hj</i>Cel61B. Residues in the metal ion-binding site of the proteins are indicated by triangles in the sequence alignment. The position of a large insertion in the <i>Hj</i>Cel61B structure and corresponding region in <i>Ta</i>GH61A is marked with a red box. Panel <b>B</b> shows surface representations of <i>Tt</i>GH61E (left), <i>Pc</i>GH61D (middle), and <i>Hj</i>Cel61B (right). The metal ion binding sites are coloured blue. The red surface in <i>Hj</i>Cel61B corresponds to the red box in panel A. Panel <b>C</b> shows a superposition of the metal binding sites of <i>Tt</i>GH61E (PDB code: 3EII, coloured green), <i>Hj</i>Cel61B (PDB code: 2VTC, coloured light-blue), and the <i>Pc</i>GH61D homology model (coloured orange). The light blue and green spheres indicate the nickel ion found bound in the <i>Hj</i>Cel61B structure and the zinc ion bound in the <i>Tt</i>GH61E structure, respectively. Red spheres indicate water molecules in the two structures <i>Hj</i>Cel61B and <i>Tt</i>GH61E. Grey dashed lines indicate interactions with the bound metals.</p>", "links"=>[], "tags"=>["chemistry", "microbiology", "plant biology", "biotechnology", "biophysics", "Biochemistry"], "article_id"=>379919, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g002", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_and_structural_analysis_/379919", "title"=>"Sequence and structural analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:24:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/709836"], "description"=>"<p>The figure shows superposition of chromatograms as in the top panel of <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#pone-0027807-g003\" target=\"_blank\">figure 3</a> for: PASC + <i>Pc</i>GH61D (black), Avicel + <i>Pc</i>GH61D (red), Cellulose nanofibrils + <i>Pc</i>GH61D (magenta), and Avicel + CelS2 (blue). Note the alternating intensities in the latter sample. All reactions were run in the presence of 1 mM ascorbic acid and at pH 6.5. Since these HPLC analyses were run over an extended time period the original chromatograms showed slight variations in elution times; this has been manually changed to obtain an optimum superposition. Standards were always run as part of each series of HPAEC experiments to secure correct peak annotation. Nb. Experiments with filter paper, which has a much higher DP (estimated to be ∼2000 pp. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#pone.0027807-Zang1\" target=\"_blank\">[35]</a>, did not yield detectable amounts of soluble products. However, when a cellulase was added, short oxidized products were detected in chromatograms that looked approximately as the chromatogram obtained in the synergy experiment including GH61 in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#pone-0027807-g008\" target=\"_blank\">Figure 8B</a>.</p>", "links"=>[], "tags"=>["substrate", "enzyme"], "article_id"=>380189, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_substrate_and_type_of_enzyme_on_product_profile_/380189", "title"=>"Effect of substrate and type of enzyme on product profile.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:25:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/709769"], "description"=>"<p>The figure shows overlayed HPAEC chromatograms showing that release of oligosaccharides from cellulose by <i>Pc</i>GH61D increases with increasing ascorbic acid concentration. <i>Pc</i>GH61D (4 µg/mL) was incubated with 10 mg/mL Avicel in 50 mM MES buffer pH 6.6 containing different concentrations of ascorbic acid. The reactions were incubated for 24 hours at 50°C with vertical agitation at 900 rpm after which products were analysed. The ascorbic acid concentrations were 0 mM (red), 0.8 mM (magenta), 1.6 mM (orange), 2.0 mM (green), 2.4 mM (blue) and 4.8 mM (black).</p>", "links"=>[], "tags"=>["reductant"], "article_id"=>380124, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g004", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_reductant_concentration_on_Pc_GH61D_activity_/380124", "title"=>"Effect of reductant concentration on <i>Pc</i>GH61D activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:25:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/710241"], "description"=>"<p>Panel <b>A</b> shows glucose release from 10 mg/mL Avicel by Celluclast (CC) after 1 day (1d) and 3 days (3d) for reactions with (red bars) or without <i>Pc</i>GH61D (green bars). Reactions incubated with <i>Pc</i>GH61D alone did not release detectable amounts of glucose or cellobiose. Panel <b>B</b> shows typical chromatograms of the soluble sugars obtained in these reactions (1 day) with accumulation of Glc and Glc<sub>2</sub> and some Glc<sub>3</sub> (green, reaction without <i>Pc</i>GH61D; red, reaction with <i>Pc</i>GH61D). In the case of reactions with <i>Pc</i>GH61D, the oxidized oligosaccharides GlcGlcA (DP2<sub>ox</sub>) and Glc<sub>2</sub>GlcA (DP3<sub>ox</sub>) were also observed. In the reactions without <i>Pc</i>GH61D, BSA was added to keep the protein concentration constant in all reactions. See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027807#s2\" target=\"_blank\">Materials & Methods</a> section for conditions.</p>", "links"=>[], "tags"=>["chemistry", "microbiology", "plant biology", "biotechnology", "biophysics", "Biochemistry"], "article_id"=>380586, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g008", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synergy_between_Pc_GH61D_and_Celluclast_/380586", "title"=>"Synergy between <i>Pc</i>GH61D and Celluclast.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:27:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/709955"], "description"=>"<p>0.8 mg/mL <i>Pc</i>GH61D was incubated with 400 µM EDTA for 3 hours at 20°C. This EDTA treated <i>Pc</i>GH61D (final concentration 40 µg/mL) was incubated with 10 mg/mL Avicel in 50 mM MES buffer pH 6.6 containing 1.7 mM reduced glutathione and one of 7 different metal ions (10 µM; Mg<sup>2+</sup>, Fe<sup>3+</sup>, Zn<sup>2+</sup>, Co<sup>2+</sup>, Ca<sup>2+</sup>, Cu<sup>2+</sup>, Mn<sup>2+</sup>). The final concentration of EDTA in the reaction mixtures was 20 µM. The superimposed HPAEC chromatograms show products released after 20 hours of incubation at 50°C. Incubation of Avicel without addition of <i>Pc</i>GH61D under these same conditions led to release of small amounts of native oligomeric products from the substrate and yielded a chromatogram similar to that labelled “no metal”.</p>", "links"=>[], "tags"=>["dependency"], "article_id"=>380312, "categories"=>["Microbiology", "Biochemistry", "Plant Biology", "Biotechnology", "Chemistry", "Biophysics"], "users"=>["Bjørge Westereng", "Takuya Ishida", "Gustav Vaaje-Kolstad", "Miao Wu", "Vincent G. H. Eijsink", "Kiyohiko Igarashi", "Masahiro Samejima", "Jerry Ståhlberg", "Svein J. Horn", "Mats Sandgren"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027807.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Metal_dependency_of_Pc_GH61D_/380312", "title"=>"Metal dependency of <i>Pc</i>GH61D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:26:10"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"13", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2014", "month"=>"11"}
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  • {"unique-ip"=>"4", "full-text"=>"7", "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"=>"7", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"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"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"4", "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"=>"4", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"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"=>"12"}
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  • {"unique-ip"=>"19", "full-text"=>"18", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"15", "full-text"=>"19", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
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  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
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  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"17", "full-text"=>"18", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"22", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
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Relative Metric

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