RecFOR Is Not Required for Pneumococcal Transformation but Together with XerS for Resolution of Chromosome Dimers Frequently Formed in the Process
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{"title"=>"RecFOR Is Not Required for Pneumococcal Transformation but Together with XerS for Resolution of Chromosome Dimers Frequently Formed in the Process", "type"=>"journal", "authors"=>[{"first_name"=>"Calum", "last_name"=>"Johnston", "scopus_author_id"=>"55618267600"}, {"first_name"=>"Isabelle", "last_name"=>"Mortier-Barrière", "scopus_author_id"=>"6507238697"}, {"first_name"=>"Chantal", "last_name"=>"Granadel", "scopus_author_id"=>"6506346837"}, {"first_name"=>"Patrice", "last_name"=>"Polard", "scopus_author_id"=>"6603832546"}, {"first_name"=>"Bernard", "last_name"=>"Martin", "scopus_author_id"=>"7402931602"}, {"first_name"=>"Jean Pierre", "last_name"=>"Claverys", "scopus_author_id"=>"7005212332"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"25569614", "sgr"=>"84924405885", "pui"=>"602890686", "scopus"=>"2-s2.0-84924405885", "issn"=>"15537404", "doi"=>"10.1371/journal.pgen.1004934"}, "id"=>"211d39fd-b09e-34e2-a2bc-2e5c73f86bbe", "abstract"=>"Homologous recombination (HR) is a widespread process which maintains genome integrity and promotes diversity. In bacteria, HR mends damaged DNA to ensure genome integrity and is also involved in transformation, a mechanism of horizontal gene transfer allowing acquisition of new genetic traits. HR is driven by recombinases, which are loaded onto single-stranded DNA by the recombinase loaders RecBCD and RecFOR for genome maintenance. DprA was recently proposed as another loader dedicated to transformation. During transformation, foreign DNA is taken up as single strands and integrated into the chromosome by HR. In this study, we show that RecFOR is not involved in transformation in Streptococcus pneumoniae. These results provide further support to the existence of different HR machineries dedicated to genetic transformation and genome maintenance in this pathogen. In addition, we show that transformation with chromosomal DNA generates chromosome dimers with unexpectedly high frequency, and that their resolution requires RecFOR and the site-specific recombinase XerS. In cells lacking these proteins, dimers persist and have a detrimental effect on the efficiency of transformation. Since the HR mechanisms leading to dimer formation are most likely conserved, this effect is presumably general to naturally transformable species.", "link"=>"http://www.mendeley.com/research/recfor-not-required-pneumococcal-transformation-together-xers-resolution-chromosome-dimers-frequentl", "reader_count"=>8, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Ph. D. Student"=>5, "Student > Master"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Ph. D. Student"=>5, "Student > Master"=>2}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>7, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Computer Science"=>{"Computer Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Norway"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1862316"], "description"=>"<p>(A) Chromosomal transformation frequencies in wildtype, <i>dprA</i>, <i>recO</i> and <i>dprA recO</i> mutant cells. Saturating concentration of R304 chromosomal DNA as donor (1 µg mL<sup>−1</sup>). Recipient strains: wild type, R1521; <i>recO</i> mutant, R3424; <i>dprA</i> mutant, R3426; <i>dprA</i>-<i>recO</i> double mutant, R3428. Error bars calculated from duplicate repeats. (B) Chromosomal transformation frequencies in wild type, <i>recF</i>, <i>recO</i> and <i>recR</i> mutant cells. Recipient strains: wild type, R1502; <i>recF</i> mutant, R2371; <i>recO</i> mutant, R2372, <i>recR</i> mutant, R2373. Donor DNA and selection for Str<sup>R</sup> transformants as in panel A, as well as selection for Rif<sup>R</sup> transformants. (C) Impact of <i>recO</i> inactivation on transformation with a unique PCR fragment as donor. Transformation with a 4.2-kb <i>rpsL41</i> (Str<sup>R</sup>) PCR fragment as donor (0.3 µg mL<sup>−1</sup>). Same recipient strains as in panel A. Error bars calculated from duplicate repeats.</p>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286011, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_recFOR_inactivation_on_transformation_/1286011", "title"=>"Impact of <i>recFOR</i> inactivation on transformation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862317"], "description"=>"<p>(A) Diagrammatic representation of the formation of merodiploids by transformation. This model involves ‘alternative pairing’ of a repeat sequence (R<sub>1</sub>) within the transforming ssDNA, i.e. pairing not with its chromosomal counterpart but with a similar repeat (R<sub>2</sub>) on one arm of a partially replicated recipient chromosome, coupled with ‘normal pairing’ of the non-repeat flanking ssDNA (A) on the other chromosome arm (next to the true chromosomal counterpart of R<sub>1</sub>). This bridges the two chromosome arms, creating a chromosome dimer. It is of note that this dimer differs from 'simple' chromosome dimers made of two directly repeated monomers. Resolution of this 'rearranged' chromosome dimer generates one merodiploid chromosome with the region between repeats duplicated and another chromosome lacking this region <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004934#pgen.1004934-Johnston2\" target=\"_blank\">[27]</a> (panel B). (B) Chromosome dimer resolution can be mediated by XerS or by homologous recombination, where RecA could be loaded by RecO. The duplicated region is shown in green. Δ, deletion; †, abortive chromosome. (C) Stimulation of merodiploid formation by transformation in wildtype cells (R246). (D) Stimulation of merodiploid formation by transformation in <i>recO</i> mutant cells (R3170).</p>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286012, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RecO_and_the_generation_of_merodiploids_by_transformation_/1286012", "title"=>"RecO and the generation of merodiploids by transformation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862318"], "description"=>"<p>(A) Fold reduction in merodiploids formed in <i>recO</i> mutant compared to wildtype cells. Merodiploid formation was triggered using the R<sub>1</sub>-A PCR fragment as donor and the <i>codY</i>::<i>trim</i> donor cassette was used to score merodiploid transformants. Recipient strains used: wildtype, R246; <i>recO<sup>-</sup></i>, R3170. (B) Fold reduction in merodiploids formed in <i>xerS</i> and <i>recO xerS</i> mutant compared to wildtype cells. Same experimental set up as in panel A. Recipient strains used: <i>xerS<sup>-</sup></i>, R3214; <i>xerS<sup>-</sup> recO<sup>-</sup></i>; R3873. Since merodiploid frequency was low in the double mutant, representing few clones, we confirmed on a few randomly chosen clones that they were indeed merodiploid by detection of the tandem-duplication junction by PCR (panel D), as well as confirming that they had retained the antibiotic sensitivities associated with the parent. (C) Schematic of chromosome dimer and novel tandem duplication and deletion junctions detected by PCR. α and β represent primers used to detect the novel junction created by tandem duplication. δ and γ represent primers used to detect the deletion junction created as a consequence of tandem duplication. Both junctions are present on the chromosome dimer, while the merodiploid chromosome possesses only the tandem-duplication junction, and the abortive chromosome possesses only the deletion junction. (D) Detection of tandem-duplication junction on cultures of wildtype or <i>recO<sup>-</sup> xerS<sup>-</sup></i> cells transformed with either R<sub>1</sub>-A and R<sub>2</sub>-Z PCR fragments or no DNA. PCRs carried out at different time-points after DNA addition with primers CJ242 and merod-b to amplify a 4,438 bp DNA fragment diagnostic of the tandem duplication. (E) Detection of deletion junction on same cells as in panel A (DNA added only). PCRs carried out with primers CJ244 and CJ245 to amplify a 2,980 bp DNA fragment diagnositic of the deletion junction. Strains used in both panels: wildtype; R246, <i>recO<sup>-</sup> xerS<sup>-</sup></i>; R3873.</p>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286013, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RecO_and_XerS_are_involved_in_pneumococcal_chromosome_dimer_resolution_/1286013", "title"=>"RecO and XerS are involved in pneumococcal chromosome dimer resolution.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862324"], "description"=>"<p>(A) Experiment in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004934#pgen-1004934-g003\" target=\"_blank\">Fig. 3D</a> repeated with different time-points after DNA addition. (B) Growth curves representing growth of wildtype and <i>recO<sup>-</sup> xerS<sup>-</sup></i> cells during experiment in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004934#pgen-1004934-g003\" target=\"_blank\">Fig. 3D</a> and panel A. (C) Repeat of experiment in panel A but with cells diluted 10-fold 20 min after DNA addition, and later time points taken. <i>xerS</i> and <i>recO</i> mutants were included to determine the kinetics of deletion junction disappearance in these two backgrounds. (D) Growth curves representing growth of wildtype and <i>recO<sup>-</sup> xerS<sup>-</sup></i> cells during experiment in panel C. Strains used in all four panels: wildtype; R246, <i>recO<sup>-</sup> xerS<sup>-</sup></i>; R3873.</p>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286017, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Growth_phase_impacts_the_kinetics_of_deletion_junction_loss_in_transformed_cultures_/1286017", "title"=>"Growth phase impacts the kinetics of deletion-junction loss in transformed cultures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862332"], "description"=>"<p>(A) <i>S. mitis</i> DNA impacts transformation frequency of <i>recO</i>, <i>xerS</i> and <i>recO xerS</i> mutant cells. Comparison of transformation efficiency using as donor a mixture of PCR fragment carrying the <i>rpsL41</i> mutation (Sm<sup>R</sup>) and <i>S. mitis</i> chromosomal DNA. As a slight competition for uptake is observed between the PCR fragment and <i>S. mitis</i> chromosomal DNA in wildtype cells (reducing efficiency compared to PCR fragment alone by 1.6-fold), we adjusted fold reduction in wildtype to 1 and normalized to this same factor in all mutant cells. PCR concentration: 1.5 ng mL<sup>−1</sup>; chromosomal DNA concentration: 1 µg mL<sup>−1</sup>. Strains used: wildtype; R246, <i>recO<sup>-</sup></i>; R3170, <i>xerS<sup>-</sup></i>; R3214, <i>recO<sup>-</sup> xerS<sup>-</sup></i>; R3873. (B) Monitoring ploidy through DAPI staining in cells transformed with <i>S. mitis</i> chromosomal DNA and grown to stationary phase (blue bars), compared to non-transformed competent cells (grey bars). Samples were taken at 160 min (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004934#pgen-1004934-g004\" target=\"_blank\">Fig. 4B</a>). No difference in DAPI fluorescence intensity profile was observed in wildtype cells. Relative fluorescence intensity calculated by dividing total cell intensity by cell area. Results shown are representative of three individual experiments. Strain used: wildtype, R246. (C) Monitoring ploidy through DAPI staining in <i>recO<sup>-</sup> xerS<sup>-</sup></i> cells transformed with <i>S. mitis</i> chromosomal DNA and grown to stationary phase. Two individual sets of data showing with non-transformed cells (light and dark grey) and transformed cells (two shades of blue). A shift in intensity profile towards greater fluorescence was observed with cells transformed with <i>S. mitis</i> DNA (compare blue and grey bars). Sampling and analysis as in panel B. Strain used: <i>recO<sup>-</sup> xerS<sup>-</sup></i>, R3873. (D) Monitoring ploidy through DAPI staining in <i>recO<sup>-</sup> xerS<sup>-</sup></i> cells transformed with <i>S. mitis</i> chromosomal DNA and maintained in exponential growth (blue bars), compared to non-transformed competent cells (grey bars). Samples were taken at 80 min (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004934#pgen-1004934-g004\" target=\"_blank\">Fig. 4D</a>). A shift in intensity profile towards greater fluorescence was observed with cells transformed with <i>S. mitis</i> DNA (compare blue and grey bars). Same calculations and strain as in panel C.</p>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286018, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_High_frequency_formation_of_chromosome_dimers_upon_transformation_with_S_mitis_chromosomal_DNA_/1286018", "title"=>"High frequency formation of chromosome dimers upon transformation with <i>S. mitis</i> chromosomal DNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-01-08 03:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1862404", "https://ndownloader.figshare.com/files/1862406", "https://ndownloader.figshare.com/files/1862407", "https://ndownloader.figshare.com/files/1862408", "https://ndownloader.figshare.com/files/1862410", "https://ndownloader.figshare.com/files/1862411", "https://ndownloader.figshare.com/files/1862412", "https://ndownloader.figshare.com/files/1862413", "https://ndownloader.figshare.com/files/1862414", "https://ndownloader.figshare.com/files/1862415"], "description"=>"<div><p>Homologous recombination (HR) is required for both genome maintenance and generation of diversity in eukaryotes and prokaryotes. This process initiates from single-stranded (ss) DNA and is driven by a universal recombinase, which promotes strand exchange between homologous sequences. The bacterial recombinase, RecA, is loaded onto ssDNA by recombinase loaders, RecBCD and RecFOR for genome maintenance. DprA was recently proposed as a third loader dedicated to genetic transformation. Here we assessed the role of RecFOR in transformation of the human pathogen <i>Streptococcus pneumoniae</i>. We firstly established that RecFOR proteins are not required for plasmid transformation, strongly suggesting that DprA ensures annealing of plasmid single-strands internalized in the process. We then observed no reduction in chromosomal transformation using a PCR fragment as donor, contrasting with the 10,000-fold drop in <i>dprA</i><sup>-</sup> cells and demonstrating that RecFOR play no role in transformation. However, a ∼1.45-fold drop in transformation was observed with total chromosomal DNA in <i>recFOR</i> mutants. To account for this limited deficit, we hypothesized that transformation with chromosomal DNA stimulated unexpectedly high frequency (>30% of cells) formation of chromosome dimers as an intermediate in the generation of tandem duplications, and that RecFOR were crucial for dimer resolution. We validated this hypothesis, showing that the site-specific recombinase XerS was also crucial for dimer resolution. An even higher frequency of dimer formation (>80% of cells) was promoted by interspecies transformation with <i>Streptococcus mitis</i> chromosomal DNA, which contains numerous inversions compared to pneumococcal chromosome, each potentially promoting dimerization. In the absence of RecFOR and XerS, dimers persist, as confirmed by DAPI staining, and can limit the efficiency of transformation, since resulting in loss of transformant chromosome. These findings strengthen the view that different HR machineries exist for genome maintenance and transformation in pneumococci. These observations presumably apply to most naturally transformable species.</p></div>", "links"=>[], "tags"=>["genome maintenance", "transformation", "hr", "pathogen Streptococcus pneumoniae", "recfor", "dapi", "chromosomal DNA", "recombinase", "Process Homologous recombination", "pcr", "dimer resolution", "Streptococcus mitis chromosomal DNA"], "article_id"=>1286064, "categories"=>["Biological Sciences"], "users"=>["Calum Johnston", "Isabelle Mortier-Barrière", "Chantal Granadel", "Patrice Polard", "Bernard Martin", "Jean-Pierre Claverys"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004934.s001", "https://dx.doi.org/10.1371/journal.pgen.1004934.s002", "https://dx.doi.org/10.1371/journal.pgen.1004934.s003", "https://dx.doi.org/10.1371/journal.pgen.1004934.s004", "https://dx.doi.org/10.1371/journal.pgen.1004934.s005", "https://dx.doi.org/10.1371/journal.pgen.1004934.s006", "https://dx.doi.org/10.1371/journal.pgen.1004934.s007", "https://dx.doi.org/10.1371/journal.pgen.1004934.s008", "https://dx.doi.org/10.1371/journal.pgen.1004934.s009", "https://dx.doi.org/10.1371/journal.pgen.1004934.s010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RecFOR_Is_Not_Required_for_Pneumococcal_Transformation_but_Together_with_XerS_for_Resolution_of_Chromosome_Dimers_Frequently_Formed_in_the_Process_/1286064", "title"=>"RecFOR Is Not Required for Pneumococcal Transformation but Together with XerS for Resolution of Chromosome Dimers Frequently Formed in the Process", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-01-08 03:02:07"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"1", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"30", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"10", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

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

Source
Scopus
Time
2019-09-27 15:05:35 UTC
Target URL
https://api.elsevier.com/content/search/index:SCOPUS?query=DOI(10.1371%2Fjournal.pgen.1004934)
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'