ATPase-Independent Type-III Protein Secretion in Salmonella enterica
Publication Date
November 13, 2014
Journal
PLOS Genetics
Authors
Marc Erhardt, Max E. Mertens, Florian D. Fabiani & Kelly T. Hughes
Volume
10
Issue
11
Pages
e1004800
DOI
https://dx.plos.org/10.1371/journal.pgen.1004800
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1004800
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25393010
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4230889
Europe PMC
http://europepmc.org/abstract/MED/25393010
Web of Science
000345455200042
Scopus
84912081031
Mendeley
http://www.mendeley.com/research/atpaseindependent-typeiii-protein-secretion-salmonella-enterica
Events
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Mendeley | Further Information

{"title"=>"ATPase-Independent Type-III Protein Secretion in Salmonella enterica", "type"=>"journal", "authors"=>[{"first_name"=>"Marc", "last_name"=>"Erhardt", "scopus_author_id"=>"23667111900"}, {"first_name"=>"Max E.", "last_name"=>"Mertens", "scopus_author_id"=>"56428703800"}, {"first_name"=>"Florian D.", "last_name"=>"Fabiani", "scopus_author_id"=>"56428775500"}, {"first_name"=>"Kelly T.", "last_name"=>"Hughes", "scopus_author_id"=>"7202448707"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537404", "scopus"=>"2-s2.0-84912081031", "sgr"=>"84912081031", "pui"=>"600618145", "isbn"=>"1553-7404 (Electronic)\r1553-7390 (Linking)", "pmid"=>"25393010", "doi"=>"10.1371/journal.pgen.1004800"}, "id"=>"56e96919-edde-3708-b989-2d7579464b95", "abstract"=>"Type-III protein secretion systems are utilized by gram-negative pathogens to secrete building blocks of the bacterial flagellum, virulence effectors from the cytoplasm into host cells, and structural subunits of the needle complex. The flagellar type-III secretion apparatus utilizes both the energy of the proton motive force and ATP hydrolysis to energize substrate unfolding and translocation. We report formation of functional flagella in the absence of type-III ATPase activity by mutations that increased the proton motive force and flagellar substrate levels. We additionally show that increased proton motive force bypassed the requirement of the Salmonella pathogenicity island 1 virulence-associated type-III ATPase for secretion. Our data support a role for type-III ATPases in enhancing secretion efficiency under limited secretion substrate concentrations and reveal the dispensability of ATPase activity in the type-III protein export process.", "link"=>"http://www.mendeley.com/research/atpaseindependent-typeiii-protein-secretion-salmonella-enterica", "reader_count"=>18, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>2, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Student > Doctoral Student"=>2, "Researcher"=>2, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>9, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1792369"], "description"=>"<p>Secreted FliC flagellin protein was analyzed by anti-FliC immunostaining in the FliC-phase locked wildtype and <i>fliHIJ</i> mutant strains. (<b>A</b>) Wildtype and <i>fliHIJ</i> mutants in combination with Δ<i>atpA</i>. (<b>B</b>) Wildtype and <i>fliHIJ</i> mutants in combination with Δ<i>flgM</i> and Δ<i>atpA</i>. (<b>C</b>) Wildtype and <i>fliHI</i> deletion mutant in combination with Δ<i>clpX</i> and Δ<i>atpA</i>. (<b>D</b>) Wildtype and <i>fliHI</i> deletion mutant in combination with <i>fliA<sup>H14D</sup></i> and Δ<i>atpA</i>.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239853, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g005", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Flagellin_protein_secretion_is_restored_in_the_absence_of_FliHIJ_ATPase_components_by_atpA_916_flgM_916_clpX_and_fliA_H14D_mutations_/1239853", "title"=>"Flagellin protein secretion is restored in the absence of FliHIJ ATPase components by Δ<i>atpA</i>, <i>ΔflgM</i>, <i>ΔclpX</i>, and <i>fliA<sup>H14D</sup></i> mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792336"], "description"=>"<p>Null mutations in <i>atpA</i>, <i>flgM</i>, <i>clpX</i>, and the more stable FliA<sup>H14D</sup> variant increased motility of <i>fliHIJ</i> mutant strains in a swimming motility assay using 0.3% soft agar plates. (<b>A</b>) Representative soft agar motility plates after 4.5 hours incubation at 37°C of the FliC-phase locked wildtype and <i>fliHIJ</i> mutant strains. n.d., not determined. (<b>B</b>) Quantified relative motility of <i>fliHIJ</i> mutant strains. The diameter of the motility swarm relative to the wildtype was measured after 4.5 hours incubation. Biological replicates are shown as individual data points. Data were analyzed by the Student's <i>t</i> test. Stars indicate significantly different motility (*, P<0.05; **, P<0.01; ***, P<0.001).</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239820, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g002", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Motility_of_fliHIJ_mutants_is_increased_by_mutations_in_atpA_916_flgM_916_clpX_and_fliA_H14D_/1239820", "title"=>"Motility of <i>fliHIJ</i> mutants is increased by mutations in Δ<i>atpA</i>, <i>ΔflgM</i>, <i>ΔclpX</i> and <i>fliA</i><sup>H14D</sup>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792365"], "description"=>"<p>A deletion in <i>clpX</i> (<b>A</b>) and the more stable <i>fliA<sup>H14D</sup></i> variant (<b>B</b>) increase the frequency of flagellar filament formation in a <i>fliHI</i> mutant strain. Flagellar formation is further enhanced by combination with an <i>atpA</i> mutation. Top: A montage of representative fluorescent microscopy images is shown. Flagellar filaments were stained using anti-FliC immunostaining and detected by FITC-coupled secondary antibodies (green), DNA was stained using Hoechst (blue) and cell membranes using FM-64 (red). Scale bar 2 µm. The percentage of cells with at least one filament is presented in the upper left corner. Bottom: Histogram of counted flagellar filaments per cell body. Number of counted cells and average number of filaments per cell +/− standard deviation based on Gaussian non-linear regression analysis is given in the upper right hand corner.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239849, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g004", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Frequency_of_flagellar_filament_formation_of_a_fliHI_mutant_strain_is_increased_in_clpX_null_and_fliA_H14D_backgrounds_/1239849", "title"=>"Frequency of flagellar filament formation of a <i>fliHI</i> mutant strain is increased in <i>clpX</i> null and <i>fliA<sup>H14D</sup></i> backgrounds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792377"], "description"=>"<p>List of <i>Salmonella enterica</i> servovar Typhimurium LT2 strains used in this study.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239861, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.t001", "stats"=>{"downloads"=>2, "page_views"=>39, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_Salmonella_enterica_servovar_Typhimurium_LT2_strains_used_in_this_study_/1239861", "title"=>"List of <i>Salmonella enterica</i> servovar Typhimurium LT2 strains used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792326"], "description"=>"<p>The flagellar transcriptional hierarchy of <i>Salmonella enterica</i> is composed of three classes of promoters. The Class I promoter transcribes a single operon encoding for the master regulator of the flagellar transcriptional hierarchy, the FlhD<sub>4</sub>C<sub>2</sub> complex, which is negatively regulated by ClpXP protease. FlhD<sub>4</sub>C<sub>2</sub>, together with σ<sup>70</sup>, directs RNA polymerase to transcribe from Class II promoters. Genes transcribed from Class II promoters encode structural components of the hook-basal-body complex (shaded in blue), the flagellar type-III secretion apparatus (composed of the membrane proteins FlhA, FlhB, FliO, FliP, FliQ and FliR; and the soluble proteins FliH, FliI and FliJ), as well as regulatory proteins, in particular the flagellar-specific σ-factor, σ<sup>28</sup> (encoded by <i>fliA</i>), and its cognate anti-σ factor, FlgM. The hook-basal-body is completed as soon as the hook reaches an approximate length of 55 nm, upon which the type-III secretion apparatus switches secretion specificity to its late-substrate secretion mode (indicated by the orange star). Subsequently, the late substrate FlgM is exported out of the cell, thereby freeing σ<sup>28</sup> to turn on transcription from Class III promoters. Class III gene products include the filament subunits, motor-force generators and the chemotactic system (shaded in red).</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239814, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g001", "stats"=>{"downloads"=>9, "page_views"=>96, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_overview_of_the_flagellar_transcriptional_hierarchy_and_biogenesis_/1239814", "title"=>"Schematic overview of the flagellar transcriptional hierarchy and biogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792376"], "description"=>"<p>Secretion of the Spi1 vT3SS substrate InvJ or a 3×HA tagged InvJ variant. (<b>A</b>) Secreted InvJ protein in the wildtype, Δ<i>invJ</i>, Δ<i>atpA</i>, the catalytically-inactive Spi1 ATPase <i>invC<sup>K165E</sup></i>, <i>invC<sup>K165E</sup></i> Δ<i>atpA</i>, <i>invC<sup>K165E</sup></i> Δ<i>flgM</i>, and <i>invC<sup>K165E</sup></i> Δ<i>flgM ΔfliHIJ ΔssaN ΔatpA</i> mutant strains. Detection of DnaK protein was included as a cell lysis control. (<b>B</b>) Levels of secreted InvJ::3×HA protein in the wildtype, Δ<i>invJ::3×HA</i>, Δ<i>invJ::3×HA</i> Δ<i>atpA</i>, Δ<i>invJ::3×HA invC<sup>K165E</sup></i>, and Δ<i>invJ::3×HA invC<sup>K165E</sup></i> Δ<i>atpA</i> mutant strains. 288 ng BSA was added to each supernatant fractions (except for lane 2) and served as a precipitation control. DnaK protein served as a cell lysis control.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239860, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g008", "stats"=>{"downloads"=>4, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protein_secretion_via_the_vT3SS_in_a_catalytically_inactive_ATPase_mutant_strain_is_rescued_by_deletion_of_atpA_/1239860", "title"=>"Protein secretion via the vT3SS in a catalytically-inactive ATPase mutant strain is rescued by deletion of <i>atpA</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792375"], "description"=>"<p>Export of FlgE-Bla fusion protein into the periplasm was analyzed in various <i>fliHIJ</i> deletion strains. All strains additionally harbored a deletion of the proximal rod genes (<i>ΔflgBC6557</i>) and the FlgE-Bla fusion protein under its native promoter (<i>flgE6569</i>::<i>bla</i>). (A) Minimal inhibitory concentration (MIC) values with flagellar genes expressed at normal levels. (B) Summary of MIC values with flagellar genes expressed at elevated levels due to a P<i><sub>flhD</sub></i> promoter-up mutation (P<i><sub>flhD*</sub></i> = (P1+P4 -10 TATAAT)). The error bars represent the standard error of the mean (SEM) and biological replicates are shown as individual data points.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239859, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g007", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_FliH_functions_as_a_negative_regulator_of_type_III_protein_translocation_/1239859", "title"=>"FliH functions as a negative regulator of type-III protein translocation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792357"], "description"=>"<p>The absence of the flagellar ATPase subunits FliH, FliI and FliJ results in a non-flagellated phenotype (<b>A</b>). Additional deletions in <i>atpA</i> (<b>B</b>) and <i>flgM</i> (<b>C</b>) substantially increase the frequency of flagellar filament formation of <i>fliI</i>, <i>fliHI</i> and <i>fliHIJ</i> mutant strains. Flagellar formation in the <i>flgM</i> null background is further enhanced by combination with the <i>atpA</i> mutation (<b>D</b>). Top: A montage of representative fluorescent microscopy images is shown. Flagellar filaments were stained using anti-FliC immunostaining and detected by FITC-coupled secondary antibodies (green), DNA was stained using Hoechst (blue) and cell membranes using FM-64 (red). Scale bar 2 µm. The percentage of cells with at least one filament is presented in the upper left corner. Bottom: Histogram of counted flagellar filaments per cell body. Number of counted cells and average number of filaments per cell +/− standard deviation based on Gaussian non-linear regression analysis is given in the upper right hand corner.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239841, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Frequency_of_flagellar_filament_formation_of_fliHIJ_mutants_is_increased_in_atpA_and_flgM_null_backgrounds_/1239841", "title"=>"Frequency of flagellar filament formation of <i>fliHIJ</i> mutants is increased in <i>atpA</i> and <i>flgM</i> null backgrounds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792374"], "description"=>"<p>Plot showing the lengths of individual flagellar filaments of the <i>fliHIJ</i> mutants visualized by anti-FliC immunostaining in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004800#pgen-1004800-g003\" target=\"_blank\">Figure 3</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004800#pgen-1004800-g004\" target=\"_blank\">Figure 4</a>. The average lengths of flagellar filaments +/− standard deviation and the number of measured filaments are presented in the upper part of the graph.</p>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239858, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004800.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lengths_of_flagellar_filaments_in_fliHIJ_mutants_/1239858", "title"=>"Lengths of flagellar filaments in <i>fliHIJ</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:18:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/1792450", "https://ndownloader.figshare.com/files/1792451", "https://ndownloader.figshare.com/files/1792452", "https://ndownloader.figshare.com/files/1792453", "https://ndownloader.figshare.com/files/1792454", "https://ndownloader.figshare.com/files/1792455", "https://ndownloader.figshare.com/files/1792456"], "description"=>"<div><p>Type-III protein secretion systems are utilized by gram-negative pathogens to secrete building blocks of the bacterial flagellum, virulence effectors from the cytoplasm into host cells, and structural subunits of the needle complex. The flagellar type-III secretion apparatus utilizes both the energy of the proton motive force and ATP hydrolysis to energize substrate unfolding and translocation. We report formation of functional flagella in the absence of type-III ATPase activity by mutations that increased the proton motive force and flagellar substrate levels. We additionally show that increased proton motive force bypassed the requirement of the <i>Salmonella</i> pathogenicity island 1 virulence-associated type-III ATPase for secretion. Our data support a role for type-III ATPases in enhancing secretion efficiency under limited secretion substrate concentrations and reveal the dispensability of ATPase activity in the type-III protein export process.</p></div>", "links"=>[], "tags"=>["flagellar substrate levels", "ATPase activity", "protein", "proton motive force", "report formation", "secretion efficiency", "Salmonella", "secrete building blocks", "data support", "virulence effectors", "ATP hydrolysis", "secretion substrate concentrations", "Host cells"], "article_id"=>1239913, "categories"=>["Uncategorised"], "users"=>["Marc Erhardt", "Max E. Mertens", "Florian D. Fabiani", "Kelly T. Hughes"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004800.s001", "https://dx.doi.org/10.1371/journal.pgen.1004800.s002", "https://dx.doi.org/10.1371/journal.pgen.1004800.s003", "https://dx.doi.org/10.1371/journal.pgen.1004800.s004", "https://dx.doi.org/10.1371/journal.pgen.1004800.s005", "https://dx.doi.org/10.1371/journal.pgen.1004800.s006", "https://dx.doi.org/10.1371/journal.pgen.1004800.s007"], "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/ATPase_Independent_Type_III_Protein_Secretion_in_Salmonella_enterica_/1239913", "title"=>"ATPase-Independent Type-III Protein Secretion in <i>Salmonella enterica</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-11-13 03:18:27"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"21", "full-text"=>"20", "pdf"=>"19", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"1", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[306, 482]}, {"subject_area"=>"/Biology and life sciences/Microbiology", "average_usage"=>[317]}, {"subject_area"=>"/Biology and life sciences/Physiology", "average_usage"=>[280]}, {"subject_area"=>"/Medicine and health sciences/Pathology and laboratory medicine", "average_usage"=>[287]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[271]}, {"subject_area"=>"/Physical sciences/Physics", "average_usage"=>[266]}]}
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Net::HTTPInternalServerError

Source
Counter
Time
2019-04-06 02:41:56 UTC
Target URL
http://counter-101.soma.plos.org/api/v1.0/stats/doi/10.1371%2Fjournal.pgen.1004800
Trace

/app/models/concerns/networkable.rb:21:in `get_result'
/app/models/source.rb:165:in `get_data'
/app/models/retrieval_status.rb:47:in `perform_get_data'
/app/jobs/source_job.rb:52:in `block (2 levels) in perform'
/app/jobs/source_job.rb:51:in `block in perform'
/app/jobs/source_job.rb:35:in `each'
/app/jobs/source_job.rb:35:in `perform'