Systematic Identification of Cyclic-di-GMP Binding Proteins in Vibrio cholerae Reveals a Novel Class of Cyclic-di-GMP-Binding ATPases Associated with Type II Secretion Systems
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{"title"=>"Systematic Identification of Cyclic-di-GMP Binding Proteins in Vibrio cholerae Reveals a Novel Class of Cyclic-di-GMP-Binding ATPases Associated with Type II Secretion Systems", "type"=>"journal", "authors"=>[{"first_name"=>"Kevin G.", "last_name"=>"Roelofs", "scopus_author_id"=>"45961362500"}, {"first_name"=>"Christopher J.", "last_name"=>"Jones", "scopus_author_id"=>"55474278600"}, {"first_name"=>"Sarah R.", "last_name"=>"Helman", "scopus_author_id"=>"56940339000"}, {"first_name"=>"Xiaoran", "last_name"=>"Shang", "scopus_author_id"=>"56939932200"}, {"first_name"=>"Mona W.", "last_name"=>"Orr", "scopus_author_id"=>"56120504700"}, {"first_name"=>"Jonathan R.", "last_name"=>"Goodson", "scopus_author_id"=>"55317669100"}, {"first_name"=>"Michael Y.", "last_name"=>"Galperin", "scopus_author_id"=>"7007084819"}, {"first_name"=>"Fitnat H.", "last_name"=>"Yildiz", "scopus_author_id"=>"7006760654"}, {"first_name"=>"Vincent T.", "last_name"=>"Lee", "scopus_author_id"=>"7402507283"}], "year"=>2015, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"26506097", "doi"=>"10.1371/journal.ppat.1005232", "sgr"=>"84946016384", "isbn"=>"10.1371/journal.ppat.1005232", "scopus"=>"2-s2.0-84946016384", "issn"=>"15537374", "pui"=>"606740900"}, "id"=>"c1aeb7c7-6c01-33a2-bb19-3ae681943f71", "abstract"=>"Cyclic-di-GMP (c-di-GMP) is a ubiquitous bacterial signaling molecule that regulates a variety of complex processes through a diverse set of c-di-GMP receptor proteins. We have utilized a systematic approach to identify c-di-GMP receptors from the pathogen Vibrio cholerae using the Differential Radial Capillary Action of Ligand Assay (DRaCALA). The DRaCALA screen identified a majority of known c-di-GMP binding proteins in V. cholerae and revealed a novel c-di-GMP binding protein, MshE (VC0405), an ATPase associated with the mannose sensitive hemagglutinin (MSHA) type IV pilus. The known c-di-GMP binding proteins identified by DRaCALA include diguanylate cyclases, phosphodiesterases, PilZ domain proteins and transcription factors VpsT and VpsR, indicating that the DRaCALA-based screen of open reading frame libraries is a feasible approach to uncover novel receptors of small molecule ligands. Since MshE lacks the canonical c-di-GMP-binding motifs, a truncation analysis was utilized to locate the c-di-GMP binding activity to the N-terminal T2SSE_N domain. Alignment of MshE homologs revealed candidate conserved residues responsible for c-di-GMP binding. Site-directed mutagenesis of these candidate residues revealed that the Arg9 residue is required for c-di-GMP binding. The ability of c-di-GMP binding to MshE to regulate MSHA dependent processes was evaluated. The R9A allele, in contrast to the wild type MshE, was unable to complement the ΔmshE mutant for the production of extracellular MshA to the cell surface, reduction in flagella swimming motility, attachment to surfaces and formation of biofilms. Testing homologs of MshE for binding to c-di-GMP identified the type II secretion ATPase of Pseudomonas aeruginosa (PA14_29490) as a c-di-GMP receptor, indicating that type II secretion and type IV pili are both regulated by c-di-GMP.", "link"=>"http://www.mendeley.com/research/systematic-identification-cyclicdigmp-binding-proteins-vibrio-cholerae-reveals-novel-class-cyclicdig-3", "reader_count"=>30, "reader_count_by_academic_status"=>{"Researcher"=>3, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Professor"=>1, "Professor > Associate Professor"=>2}, "reader_count_by_user_role"=>{"Researcher"=>3, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>4, "Professor"=>1, "Professor > Associate Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>14, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>2, "Sports and Recreations"=>1, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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Figshare

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  • {"files"=>["https://ndownloader.figshare.com/files/2382215"], "description"=>"<p>(A) Fraction bound <sup>32</sup>P-c-di-GMP to decreasing concentrations of purified His-MBP-MshE. The dissociation constant (K<sub>d</sub>) is indicated. Fraction bound of His-MBP-MshE to (B) <sup>32</sup>P-c-di-GMP and (C) <sup>32</sup>P-ATP in the presence of 100 μM nucleotide competitors. P-value was determined by two-tailed t-test (*** p≤0.001). All data are average of three independent assays and standard deviation is indicated by error bars.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586824, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g002", "stats"=>{"downloads"=>4, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_C_di_GMP_bind_to_MshE_ATPase_with_high_affinity_specificity_and_independently_of_ATP_/1586824", "title"=>"C-di-GMP bind to MshE ATPase with high affinity, specificity and independently of ATP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382226"], "description"=>"<p>(A) Schematic of the charged and polar conserved residues in the first 200 amino acids of MshE targeted for site-directed alanine substitution. (B) Fraction bound of <sup>32</sup>P-c-di-GMP to purified MshE (WT) and indicated pairs of alanine substitutions. (C) Fraction bound of <sup>32</sup>P-c-di-GMP to purified MshE (WT) and indicated individual alanine substitution. All data are average of three independent assays and standard deviation is indicated by error bars.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586832, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g005", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R9_is_required_for_MshE_to_bind_c_di_GMP_/1586832", "title"=>"R9 is required for MshE to bind c-di-GMP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382221"], "description"=>"<p>Schematic of the truncations generated in (A) PA14_29490 and (E) MshE. C-di-GMP binding to <i>E</i>. <i>coli</i> whole cell lysates expressing each fragment of (B) PA14_29490 and (F) MshE. (C) Fraction bound <sup>32</sup>P-c-di-GMP to decreasing concentrations of purified PA14_29490 fragment 1. (D) Fraction bound of purified PA14_29490 fragment 1 to <sup>32</sup>P-c-di-GMP in the presence of 100 μM nucleotide competitors. (G) Fraction bound of <sup>32</sup>P-c-di-GMP to purified MshE and fragments 1–6. Indicated p-value was determined by two-tailed t-test (*** p≤0.001) by comparing the indicated samples. All data are average of three independent assays and standard deviation is indicated by error bars.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586830, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_C_di_GMP_binds_MshE_and_PA14_29490_in_the_N_terminal_T2SSE_N_domain_/1586830", "title"=>"C-di-GMP binds MshE and PA14_29490 in the N-terminal T2SSE_N domain.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382236"], "description"=>"<p><sup>1</sup> Only genes represented in the <i>V</i>. <i>cholerae</i> ORF library are shown.</p><p><sup>2</sup> GGDEF containing the RxxD I-site was determined by sequence alignment (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#ppat.1005232.s001\" target=\"_blank\">S1 Fig</a>) [<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#ppat.1005232.ref027\" target=\"_blank\">27</a>].</p><p><sup>3</sup> PilZ domains containing the RxxxR…DxSxxG were determined by sequence alignment [<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#ppat.1005232.ref016\" target=\"_blank\">16</a>][<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#ppat.1005232.ref038\" target=\"_blank\">38</a>]. PlzB is omitted since it lacks the RxxxR…DxSxxG motifs.</p><p><sup>4</sup> EAL include all proteins containing the EAL domain (PF00563).</p><p><sup>5</sup> HD-GYP is defined as described in [<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#ppat.1005232.ref060\" target=\"_blank\">60</a>].</p><p>Hit rate of <i>V</i>. <i>cholerae</i> ORFs encoding predicted and previously demonstrated cdiGMP-binding proteins.<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1005232#t002fn001\" target=\"_blank\"><sup>1</sup></a></p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586841, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.t002", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hit_rate_of_V_cholerae_ORFs_encoding_predicted_and_previously_demonstrated_cdiGMP_binding_proteins_1_/1586841", "title"=>"Hit rate of <i>V</i>. <i>cholerae</i> ORFs encoding predicted and previously demonstrated cdiGMP-binding proteins.<sup>1</sup>", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382217"], "description"=>"<p>(A) Average fraction bound <sup>32</sup>P-c-di-GMP of <i>E</i>. <i>coli</i> whole cell lysate expressing <i>Vibrio cholerae</i> and <i>Pseudomonas aeruginosa</i> homologs of MshE. The dashed red line indicates background binding for a vector control strain. All data are average of three independent assays and standard deviation is indicated by error bars. (B) Unrooted phylogenetic tree of the T2SSE_N domain. Protein sequences present in the tree corresponding to proteins analyzed for c-di-GMP binding are highlighted in green (binds c-di-GMP), red (does not bind), or blue (candidate binding protein). The dark grey background corresponds to primarily type IV pili PilB sequences, and the light grey background corresponds to type II secretion protein E ATPase sequences. (C, D) Sub-trees containing VC0405 or PA14_29490 and closely related proteins.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586826, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g003", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_C_di_GMP_binds_to_V_cholerae_and_P_aeruginosa_homologs_of_MshE_/1586826", "title"=>"C-di-GMP binds to <i>V</i>. <i>cholerae</i> and <i>P</i>. <i>aeruginosa</i> homologs of MshE.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382234"], "description"=>"<p>(A) Surface MshA pilin production under varying IPTG induction determined via ELISA with MshA-specific antibody. Two biological replicates were assayed in duplicate and normalized to the average of the WT strain with vector. (B) Expression of <i>mshE</i> reduces motility in soft agar. The diameters of migration zones were measured after 16 hours of growth at 30°C with or without IPTG induction and normalized to the motility of the WT strain harboring the empty vector. Three biological replicates were performed in duplicate. Induced strains were compared to uninduced strains with ANOVA followed by Bonferroni Multiple Comparison test. (** p≤0.01, *** p≤0.001). (C) Attachment phenotypes observed with confocal microscopy 4 h post inoculation in a flow cell system. Scale bar represents 40μm. (D) Three-dimensional biofilm structures observed with confocal microscopy 24 h post inoculation in a flow cell system. Scale bar represents 40μm. (E,F) COMSTAT quantitative analysis of biomass and surface coverage of biofilms from (D). Three images from each of two independent experiments were analyzed.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586839, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MshE_interaction_with_c_di_GMP_is_essential_for_MSHA_function_/1586839", "title"=>"MshE interaction with c-di-GMP is essential for MSHA function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382235"], "description"=>"<p><sup>1</sup> Binding and enzymatic activity is deemed positive if activity has been demonstrated for the purified protein or if mutation of residues required for c-di-GMP binding or enyzmatic activity regulate a c-di-GMP dependent phenotype.</p><p>(+) = c-di-GMP binding observed,</p><p>DGC = diguanylate cyclase activity observed,</p><p>PDE = phosphodiesterase activity observed.</p><p>Two-way ANOVA was used to determine if the fraction bound to <sup>32</sup>P-c-di-GMP in the presence unlabeled c-di-GMP competitor differed significantly from no competitor (NC).</p><p>* = p < 0.001.</p><p>Specific binding of validated ORFs to c-di-GMP.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586840, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Specific_binding_of_validated_ORFs_to_c_di_GMP_/1586840", "title"=>"Specific binding of validated ORFs to c-di-GMP.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-10-27 04:10:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/2382212"], "description"=>"<p>Average fraction bound <sup>32</sup>P-c-di-GMP vs. individual <i>V</i>. <i>cholerae</i> (A) His-ORFs and (B) His-MBP-ORFs overexpressed in <i>E</i>. <i>coli</i> whole cell lysates. ORFs are arranged by VC gene number along the X-axis. ORFs validated as positive in the secondary screen are indicated by color and classified by type of c-di-GMP-binding protein. “Other” refers to proteins that have not been predicted or demonstrated to bind c-di-GMP.</p>", "links"=>[], "tags"=>["MshE homologs", "Vibrio cholerae", "molecule ligands", "Ligand Assay", "2SSE", "Arg 9 residue", "novel receptors", "Differential Radial Capillary Action", "extracellular MshA", "pathogen Vibrio cholerae", "Systematic Identification", "pa", "diguanylate cyclases", "R 9A allele", "PilZ domain proteins", "reading frame libraries", "Testing homologs", "DRaCALA screen", "novel class", "candidate residues", "Pseudomonas aeruginosa", "Δ mshE", "transcription factors VpsT", "type MshE", "binding", "cell surface", "vc", "type II secretion", "msha", "type II secretion ATPase", "type IV Pilus", "type iv pili", "truncation analysis"], "article_id"=>1586821, "categories"=>["Biological Sciences"], "users"=>["Kevin G. Roelofs", "Christopher J. Jones", "Sarah R. Helman", "Xiaoran Shang", "Mona W. Orr", "Jonathan R. Goodson", "Michael Y. Galperin", "Fitnat H. Yildiz", "Vincent T. Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1005232.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primary_DRaCALA_screen_of_Vibrio_cholerae_ORF_libraries_/1586821", "title"=>"Primary DRaCALA screen of <i>Vibrio cholerae</i> ORF libraries.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-10-27 04:10:12"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"33", "full-text"=>"43", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
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Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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