In Silico Analysis of Putative Paralytic Shellfish Poisoning Toxins Export Proteins in Cyanobacteria
Publication Date
February 15, 2013
Journal
PLOS ONE
Authors
Katia Soto Liebe, Xaviera A. López Cortés, Juan José Fuentes Valdes, Karina Stucken, et al
Volume
8
Issue
2
Pages
e55664
DOI
https://dx.plos.org/10.1371/journal.pone.0055664
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0055664
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23457475
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3574068
Europe PMC
http://europepmc.org/abstract/MED/23457475
Web of Science
000315603700016
Scopus
84874080405
Mendeley
http://www.mendeley.com/research/silico-analysis-putative-paralytic-shellfish-poisoning-toxins-export-proteins-cyanobacteria
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Mendeley | Further Information

{"title"=>"In Silico Analysis of Putative Paralytic Shellfish Poisoning Toxins Export Proteins in Cyanobacteria", "type"=>"journal", "authors"=>[{"first_name"=>"Katia", "last_name"=>"Soto-Liebe", "scopus_author_id"=>"24399935900"}, {"first_name"=>"Xaviera A.", "last_name"=>"López-Cortés", "scopus_author_id"=>"27467451500"}, {"first_name"=>"Juan José", "last_name"=>"Fuentes-Valdes", "scopus_author_id"=>"25928484500"}, {"first_name"=>"Karina", "last_name"=>"Stucken", "scopus_author_id"=>"25928833400"}, {"first_name"=>"Fernando", "last_name"=>"Gonzalez-Nilo", "scopus_author_id"=>"6603635113"}, {"first_name"=>"Mónica", "last_name"=>"Vásquez", "scopus_author_id"=>"55310853800"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84874080405", "sgr"=>"84874080405", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0055664", "pmid"=>"23457475", "pui"=>"368367895"}, "id"=>"0e97fe48-9ce1-3ea0-a558-4ffaa1326e10", "abstract"=>"Paralytic shellfish poisoning toxins (PSTs) are a family of more than 30 natural alkaloids synthesized by dinoflagellates and cyanobacteria whose toxicity in animals is mediated by voltage-gated Na(+) channel blocking. The export of PST analogues may be through SxtF and SxtM, two putative MATE (multidrug and toxic compound extrusion) family transporters encoded in PSTs biosynthetic gene cluster (sxt). sxtM is present in every sxt cluster analyzed; however, sxtF is only present in the Cylindrospermopsis-Raphidiopsis clade. These transporters are energetically coupled with an electrochemical gradient of proton (H(+)) or sodium (Na(+)) ions across membranes. Because the functional role of PSTs remains unknown and methods for genetic manipulation in PST-producing organisms have not yet been developed, protein structure analyses will allow us to understand their function. By analyzing the sxt cluster of eight PST-producing cyanobacteria, we found no correlation between the presence of sxtF or sxtM and a specific PSTs profile. Phylogenetic analyses of SxtF/M showed a high conservation of SxtF in the Cylindrospermopsis-Raphidiopsis clade, suggesting conserved substrate affinity. Two domains involved in Na(+) and drug recognition from NorM proteins (MATE family) of Vibrio parahaemolyticus and V. cholerae are present in SxtF/M. The Na(+) recognition domain was conserved in both SxtF/M, indicating that Na(+) can maintain the role as a cation anti-transporter. Consensus motifs for toxin binding differed between SxtF and SxtM implying differential substrate binding. Through protein modeling and docking analysis, we found that there is no marked affinity between the recognition domain and a specific PST analogue. This agrees with our previous results of PST export in R. brookii D9, where we observed that the response to Na(+) incubation was similar to different analogues. These results reassert the hypothesis regarding the involvement of Na(+) in toxin export, as well as the motifs L(398)XGLQD(403) (SxtM) and L(390)VGLRD(395) (SxtF) in toxin recognition.", "link"=>"http://www.mendeley.com/research/silico-analysis-putative-paralytic-shellfish-poisoning-toxins-export-proteins-cyanobacteria", "reader_count"=>28, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>7, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>2, "Student > Master"=>5, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>7, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>2, "Student > Master"=>5, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>7, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Mexico"=>1, "France"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/486188", "https://ndownloader.figshare.com/files/486189", "https://ndownloader.figshare.com/files/486191", "https://ndownloader.figshare.com/files/486192", "https://ndownloader.figshare.com/files/486194"], "description"=>"<div><p>Paralytic shellfish poisoning toxins (PSTs) are a family of more than 30 natural alkaloids synthesized by dinoflagellates and cyanobacteria whose toxicity in animals is mediated by voltage-gated Na<sup>+</sup> channel blocking. The export of PST analogues may be through SxtF and SxtM, two putative MATE (multidrug and toxic compound extrusion) family transporters encoded in PSTs biosynthetic gene cluster (<em>sxt</em>). <em>sxtM</em> is present in every <em>sxt</em> cluster analyzed; however, <em>sxtF</em> is only present in the <em>Cylindrospermopsis-Raphidiopsis</em> clade. These transporters are energetically coupled with an electrochemical gradient of proton (H<sup>+</sup>) or sodium (Na<sup>+</sup>) ions across membranes. Because the functional role of PSTs remains unknown and methods for genetic manipulation in PST-producing organisms have not yet been developed, protein structure analyses will allow us to understand their function. By analyzing the <em>sxt</em> cluster of eight PST-producing cyanobacteria, we found no correlation between the presence of <em>sxtF</em> or <em>sxtM</em> and a specific PSTs profile. Phylogenetic analyses of SxtF/M showed a high conservation of SxtF in the <em>Cylindrospermopsis-Raphidiopsis</em> clade, suggesting conserved substrate affinity. Two domains involved in Na<sup>+</sup> and drug recognition from NorM proteins (MATE family) of <em>Vibrio parahaemolyticus</em> and <em>V. cholerae</em> are present in SxtF/M. The Na<sup>+</sup> recognition domain was conserved in both SxtF/M, indicating that Na<sup>+</sup> can maintain the role as a cation anti-transporter. Consensus motifs for toxin binding differed between SxtF and SxtM implying differential substrate binding. Through protein modeling and docking analysis, we found that there is no marked affinity between the recognition domain and a specific PST analogue. This agrees with our previous results of PST export in <em>R. brookii</em> D9, where we observed that the response to Na<sup>+</sup> incubation was similar to different analogues. These results reassert the hypothesis regarding the involvement of Na<sup>+</sup> in toxin export, as well as the motifs L<sup>398</sup>XGLQD<sup>403</sup> (SxtM) and L<sup>390</sup>VGLRD<sup>395</sup> (SxtF) in toxin recognition.</p> </div>", "links"=>[], "tags"=>["putative", "paralytic", "shellfish", "poisoning", "toxins", "proteins", "cyanobacteria"], "article_id"=>157123, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.s001", "https://dx.doi.org/10.1371/journal.pone.0055664.s002", "https://dx.doi.org/10.1371/journal.pone.0055664.s003", "https://dx.doi.org/10.1371/journal.pone.0055664.s004", "https://dx.doi.org/10.1371/journal.pone.0055664.s005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_Silico_Analysis_of_Putative_Paralytic_Shellfish_Poisoning_Toxins_Export_Proteins_in_Cyanobacteria__/157123", "title"=>"<em>In Silico</em> Analysis of Putative Paralytic Shellfish Poisoning Toxins Export Proteins in Cyanobacteria", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-02-15 01:58:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/487596"], "description"=>"<p>Variations of the structure of saxitoxin are circled: carbamoyl group (black), sulfate group (red), sulfonate group (green) and hydroxyl group (blue).</p>", "links"=>[], "tags"=>["saxitoxin", "analogues", "synthesized", "cyanobacteria"], "article_id"=>158109, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Final_saxitoxin_STX_analogues_synthesized_by_cyanobacteria_as_described_in_21_/158109", "title"=>"Final saxitoxin (STX) analogues synthesized by cyanobacteria (as described in [21]).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-15 02:15:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/487745"], "description"=>"<p>. ORFs <i>sxtF</i> and <i>sxtM</i> are shown in yellow and pink, respectively. Homologous segments are indicated in black (<i>sxtG/H/M/I</i>) and green (<i>sxtSUL/DIOX/M</i>). Putative scare sequence present in intergenic region <i>sxtH-sxtI</i> and also identified in the end of <i>sxtF</i>, <i>sxtM</i> sequences, is shown in red. ORFs with unknown functions are shown in black, ORFs flanking the clusters in white and the transposases element in grey.</p>", "links"=>[], "tags"=>["clusters"], "article_id"=>158261, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparative_analysis_of_five_sxt_clusters_in_cyanobacteria_/158261", "title"=>"Comparative analysis of five <i>sxt</i> clusters in cyanobacteria", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-15 02:17:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/487855"], "description"=>"<p>The dendrogram was inferred with a JTT amino acid substitution model, uniform rate and a bootstrap of 1000 replications (only values over 60% are shown) (MEGA version 5). The subdivisions of the tree correspond to the two different types of transporters, whose amino acid sequence in the two specific recognition motifs (Cation and Toxin), are given in the right part of the figure. The cyanobacterial branch is marked in green. SxtM recognition motifs are shown in a pink rectangle and SxtF motifs in a yellow rectangle. The toxin recognition motif of SxtM2 from <i>L. wollei</i> contains a non- expected amino acid sequence (orange rectangle), corresponding to an amino acid mixture: in position 399 there is a V (Valine) similar to SxtF toxin motif, and in position 402 there is a Q (Glutamine), similar to SxtM. CR: <i>C. raciborskii</i>; Raph: <i>Raphidiopsis</i>; Apha: <i>Aphanizomenon</i>; AC: <i>A. circinalis</i>; LW: <i>L. wollei</i> ¸ PmC: <i>Peltigera membranacea</i> cyanobiont; VC: <i>Vibrio cholerae</i>.</p>", "links"=>[], "tags"=>["phylogenetic", "homologues"], "article_id"=>158374, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maximum_Likelihood_phylogenetic_tree_for_SxtF_SxtM_and_its_homologues_in_Nostoc_sp_and_Vibrio_cholerae_/158374", "title"=>"Maximum Likelihood phylogenetic tree for SxtF/SxtM and its homologues in <i>Nostoc</i> sp. and <i>Vibrio cholerae</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-15 02:19:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/487982"], "description"=>"<p>The model was built based on the X-ray structure of the MATE transporter NorM of <i>Vibrio cholerae</i> (ID code: 3MKT; Resolution: 3,65 Å; R-Value: 0,312). The location in which we obtained the most favorable binding energies (domain <sup>390</sup>VGLRD<sup>395</sup> in licorice representation) is shown circled in blue. STX corresponds to the yellow colored molecule.</p>", "links"=>[], "tags"=>["sxtf", "lateral"], "article_id"=>158496, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_protein_structure_of_SxtF_of_R_brookii_D9_lateral_view_/158496", "title"=>"Predicted protein structure of SxtF of <i>R. brookii</i> D9, lateral view.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-15 02:21:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/488089"], "description"=>"<p>The PST recognition region in licorice representation corresponds to: SxtF <i>R. brookii</i> D9 (A, B and C) for the conserved region LVGLRD; SxtM <i>R. brookii</i> D9 (D, E and F) for the conserved region LIGLQD; SxtF <i>C. raciborskii</i> T3 (G and H), for the conserved region LVGLRD; SxtM <i>C. raciborskii</i> T3 (I and J) for the conserved region LIGLQD; SxtM <i>A. circinalis</i> AWQC131C (K, L, M and N) for the conserved region LIGLQD. PSTs are depicted in the surfaces representations. The name of the each PST is indicated in the bottom section of the model. The licorice representation shows: carbon atoms in cyan, oxygen in red, nitrogen in blue and sulfur in yellow. Hydrogen atoms were omitted.</p>", "links"=>[], "tags"=>["pst-recognition", "sites"], "article_id"=>158608, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Representation_view_of_PST_recognition_sites_in_SxtF_M_/158608", "title"=>"Representation view of PST-recognition sites in SxtF/M.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-15 02:23:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/488322"], "description"=>"*<p>Interactions obtained from docking calculations to Grid 2.</p><p>Raph: <i>Raphidiopsis brookii</i>; CR: <i>C. raciborskii</i>; AC: <i>A. circinalis</i>.</p><p>NP: Analogue is not present.</p><p>(−): System was not analyzed.</p>", "links"=>[], "tags"=>["energies", "pst", "analogues", "putative", "binding", "sites", "sxtf"], "article_id"=>158836, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Binding_energies_of_the_PST_analogues_and_putative_binding_sites_in_SxtF_and_SxtM_/158836", "title"=>"Binding energies of the PST analogues and putative binding sites in SxtF and SxtM.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-15 02:27:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/488361"], "description"=>"a<p>Toxin profile.</p>b<p>Gene sequences.</p>?<p>Classification is not clear.</p>+<p>Gene or toxin is present.</p>++<p>PST analogue is synthesized in higher proportion (final analogue).</p>\n <p>This work.</p><p>CR: <i>C. raciborskii</i>; Raph: <i>Raphidiopsis</i>; Apha: <i>Aphanizomenon</i>; AC: <i>A. circinalis</i>; LW: <i>L. wollei.</i></p><p>Sources: <sup>(1)</sup>Brazil,</p>(2)<p>Uruguay,</p>(3)<p>USA,</p>(4)<p>Australia.</p>", "links"=>[], "tags"=>["transporter", "genes", "cyanobacterial"], "article_id"=>158885, "categories"=>["Inorganic Chemistry", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Katia Soto-Liebe", "Xaviera A. López-Cortés", "Juan José Fuentes-Valdes", "Karina Stucken", "Fernando Gonzalez-Nilo", "Mónica Vásquez"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0055664.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PSTs_profiles_presence_of_sxtM_F_transporter_genes_and_source_of_cyanobacterial_strains_/158885", "title"=>"PSTs profiles, presence of <i>sxtM/F</i> transporter genes and source of cyanobacterial strains.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-15 02:28:05"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"20", "cited-by"=>"0", "year"=>"2013", "month"=>"3"}
  • {"unique-ip"=>"17", "full-text"=>"18", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"4"}
  • {"unique-ip"=>"17", "full-text"=>"19", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2013", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2013", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2013", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"12", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"15", "full-text"=>"18", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"3", "abstract"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"25", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"18", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"20", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"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"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"2", "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"=>"10", "full-text"=>"11", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
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  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"11", "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"=>"12", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[266, 468, 593, 703, 804, 903, 993, 1084, 1171, 1256, 1339, 1422, 1492]}, {"subject_area"=>"/Biology and life sciences/Microbiology", "average_usage"=>[293, 503, 638, 755, 861, 960, 1056, 1146, 1239, 1323, 1403, 1491, 1568]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Biology and life sciences/Taxonomy", "average_usage"=>[315, 535, 673, 799, 934, 1049, 1169, 1261, 1387, 1467, 1612, 1696, 1781]}, {"subject_area"=>"/Biology and life sciences/Toxicology", "average_usage"=>[247, 444, 560, 669, 769, 863, 947, 1036, 1129, 1204, 1296, 1374, 1437]}, {"subject_area"=>"/Medicine and health sciences/Pathology and laboratory medicine", "average_usage"=>[267, 466, 592, 709, 806, 901, 989, 1075, 1162, 1254, 1342, 1424, 1486]}]}
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Net::HTTPTooManyRequests

Source
Scopus
Time
2019-08-27 20:08:02 UTC
Target URL
https://api.elsevier.com/content/search/index:SCOPUS?query=DOI(10.1371%2Fjournal.pone.0055664)
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'