A LysR-Type Transcriptional Regulator, RovM, Senses Nutritional Cues Suggesting that It Is Involved in Metabolic Adaptation of Yersinia pestis to the Flea Gut
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{"title"=>"A LysR-Type transcriptional regulator, rovm, senses nutritional cues suggesting that it is involved in metabolic adaptation of yersinia pestis to the flea gut", "type"=>"journal", "authors"=>[{"first_name"=>"Viveka", "last_name"=>"Vadyvaloo", "scopus_author_id"=>"22136890600"}, {"first_name"=>"Angela K.", "last_name"=>"Hinz", "scopus_author_id"=>"14028234100"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0137508", "issn"=>"19326203", "sgr"=>"84945218772", "pui"=>"606476825", "scopus"=>"2-s2.0-84945218772"}, "id"=>"4a0cba85-2f7e-3fbc-9cab-d97644a8fe70", "abstract"=>"Yersinia pestis has evolved as a clonal variant of Yersinia pseudotuberculosis to cause flea-borne biofilm–mediated transmission of the bubonic plague. The LysR-type transcriptional regulator, RovM, is highly induced only during Y. pestis infection of the flea host. RovM homologs in other pathogens regulate biofilm formation, nutrient sensing, and virulence; including in Y. pseudotuberculosis, where RovM represses the major virulence factor, RovA. Here the role that RovM plays during flea infection was investigated using a Y. pestis KIM6+ strain deleted of rovM, ΔrovM. The ΔrovM mutant strain was not affected in characteristic biofilm gut blockage, growth, or survival during single infection of fleas. Nonetheless, during a co-infection of fleas, the ΔrovM mutant exhibited a significant competitive fitness defect relative to the wild type strain. This competitive fitness defect was restored as a fitness advantage relative to the wild type in a ΔrovM mutant complemented in trans to over-express rovM. Consistent with this, Y. pestis strains, producing elevated transcriptional levels of rovM, displayed higher growth rates, and differential ability to form biofilm in response to specific nutrients in comparison to the wild type. In addition, we demonstrated that rovA was not repressed by RovM in fleas, but that elevated transcriptional levels of rovM in vitro correlated with repression of rovA under specific nutritional conditions. Collectively, these findings suggest that RovM likely senses specific nutrient cues in the flea gut environment, and accordingly directs metabolic adaptation to enhance flea gut colonization by Y. pestis.", "link"=>"http://www.mendeley.com/research/lysrtype-transcriptional-regulator-rovm-senses-nutritional-cues-suggesting-it-involved-metabolic-ada", "reader_count"=>7, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Other"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Other"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Medicine and Dentistry"=>1, "Agricultural and Biological Sciences"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2255119"], "description"=>"<p>Growth of WT (pACYC177) (●), Δ<i>rovM</i> (pACYC177) mutant (■) and Δ<i>rovM</i> (pACrovM) complemented mutant (♦) strains in Sebbane minimal medium (SMM) supplemented with 0.2% (A) glucose (dark grey), galactose (light grey), or diacteylchitobiose (black) as additional carbon sources or, (B) amino acids, glutamine (light grey), arginine (dark grey) and histidine (black). Error bars indicate the mean±SD of three independent experiments. To calculate the growth rate linear regression analysis was performed on the exponential phase time points of growth between 18–32 hours for (A) and 16–32 hours for (B). The <i>ΔrovM</i> (pACrovM) complemented strain grew at a significantly higher growth rate (*, P<0.001) in SMM supplemented with diacetylchitobiose, glutamine and arginine compared to the Δ<i>rovM</i> mutant and wild type strains. WT = wild type.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537196, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g005", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RovM_senses_nutritional_cues_/1537196", "title"=>"RovM senses nutritional cues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255115"], "description"=>"<p>Percentage infection per flea at 0 and 28 day post-infection, with (A) a <i>rovM</i> mutant and wild type strain or, (B) <i>rovM</i> (pACrovM) and the wild type strain. The mean of the percentage infection for 16–20 fleas is indicated by the horizontal bar. A student’s t-test was used to determine the significant differences between the percentage infections of each strain in fleas. The P values are given. Black symbols represent the first infection and grey symbols the second infection.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537193, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g004", "stats"=>{"downloads"=>3, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_rovM_in_Y_pestis_confers_a_competitive_fitness_defect_while_the_complemented_mutant_rovM_pACrovM_has_a_competitive_fitness_advantage_during_flea_infection_/1537193", "title"=>"Deletion of <i>rovM</i> in <i>Y</i>. <i>pestis</i> confers a competitive fitness defect while the complemented mutant, <i>rovM</i> (pACrovM) has a competitive fitness advantage, during flea infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255113"], "description"=>"<p>Flea infection of the <i>Y</i>. <i>pestis</i> KIM6+ WT (grey), <i>Y</i>. <i>pestis</i> KIM6+ Δ<i>rovM</i> (pACYC177) mutant (black) and corresponding <i>Y</i>. <i>pestis</i> KIM6+ Δ<i>rovM</i> (pACrovM) complemented mutant strain (unfilled). The percentage of fleas that develop blockage after infection (A), percentage of infected fleas (B) and average bacterial load (cfu/flea) (C) are not different between the Δ<i>rovM</i> (pACYC177) mutant, wild type or complemented Δ<i>rovM</i> (pACrovM) strains for the 2–3 independent flea infection studies presented. An average of 20 fleas per strain at each time point represents data for cfu/flea and percentage of infected fleas for the studies. Error bars are the mean±SD of 2–3 independent biological replicates.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537191, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RovM_does_not_contribute_to_biofilm_blockage_growth_and_survival_of_Y_pestis_in_the_flea_gut_/1537191", "title"=>"RovM does not contribute to biofilm blockage, growth and survival of <i>Y</i>. <i>pestis</i> in the flea gut.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255110"], "description"=>"<p>Biofilm formation of <i>Y</i>. <i>pestis</i> KIM6<i>+</i> strains in LB medium supplemented with 4mM MgCl<sub>2</sub> and 4mM CaCl<sub>2</sub> (A) and TMH-gal<sup>+</sup> medium (B). Error bars are the mean±SD of four independent biological replicates. A One Way ANOVA combined with a Tukey’s test was used to test significant differences in the biofilm formation between strains. The overall P-value for the ANOVA was P<0.0001. *** represents P<0.001 and indicates a significant difference in biofilm formed between the strains. Horizontal lines mark a groups of bars that are being compared.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537187, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g001", "stats"=>{"downloads"=>2, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Y_pestis_strains_with_multiple_plasmid_encoded_copies_of_rovM_show_differential_ability_to_form_biofilm_in_varying_nutritional_conditions_/1537187", "title"=>"<i>Y</i>. <i>pestis</i> strains with multiple plasmid-encoded copies of <i>rovM</i> show differential ability to form biofilm in varying nutritional conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255125"], "description"=>"<p>Quantitative transcript levels of (A) <i>rovM</i> and (B) <i>rovA</i> genes from exponential phase planktonic cultures of wild type (pACYC177), Δ<i>rovM</i> (pACYC177) mutant, wild type (pCRrovM) and Δ<i>rovM</i> (pACrovM) complemented mutant in Sebbane minimal medium supplemented with arginine. Error bars represent the mean±SD of at least 3 independent replicates. A One Way ANOVA combined with a Tukey’s post-test was used to test significant differences in transcript level. The overall P-value for the ANOVAs was 0.0003 for (A) and 0.0173 for (B). Significant differences in gene transcript levels between strains is indicated by *for P<0.05 and *** for P<0.001 Average fold increase in expression±SD of <i>rovM</i> and <i>rovA</i> is indicated in parentheses. WT = wild type, ns = not significant.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537201, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g008", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RT_qPCR_of_rovM_and_rovA_in_minimal_medium_containing_arginine_/1537201", "title"=>"RT-qPCR of <i>rovM</i> and <i>rovA</i> in minimal medium containing arginine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255122"], "description"=>"<p>(A) Biofilm formation of <i>Y</i>. <i>pestis</i> KIM6+ strains in TMH-gal<sup>+</sup>arg<sup>-</sup>. Error bars are the mean±SD of four independent biological replicates. A One Way ANOVA combined with a Tukey’s test was used to test significant differences in biofilm formation between strains. The overall P-value for the ANOVA was P<0.0001. Significant differences in biofilm formation are indicated by * for P<0.05 and *** for P<0.001. (B) Growth of <i>Y</i>. <i>pestis</i> strains in TMH-gal<sup>+</sup>arg<sup>-</sup>. Error bars are the mean±SD of four independent biological replicates. The mean mean±SD of the growth rate (μ) is given in parentheses. All closed symbol growth curves represent strains containing multiple copies of <i>rovM</i>. A One Way ANOVA combined with a Tukey’s test was used to test significant differences in the growth rate between strains. The overall P-value was P<0.0001. Significant difference in growth rates is indicated by *** for a P-value of 0.0001. Horizontal lines group a set of bars together. Capped lines mark the two bars (or groups of bars) that are being compared.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537199, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g007", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Arginine_is_sensed_by_RovM_to_control_biofilm_production_/1537199", "title"=>"Arginine is sensed by RovM to control biofilm production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255121"], "description"=>"<p>Quantitative transcript levels of (A) <i>rovM</i> and (B) <i>rovA</i> genes from exponential phase planktonic cultures of WT (pACYC177), Δ<i>rovM</i> (pACYC177) mutant and Δ<i>rovM</i> (pACrovM) complemented mutant strains in fleas (light grey bars), LB, and Sebbane minimal medium supplemented with 0.2% glucose. Error bars indicate the mean± SD of three independent experiments. A One Way ANOVA combined with a Tukey’s test was used to test significant differences in transcript levels between strains. The overall P-value for (A) and (B) is P<0.0001. Significant differences in gene transcript levels between stains is indicated by *for P<0.05 and *** for P<0.001. Average fold increased expression±SD of <i>rovM</i> and <i>rovA</i> is indicated in parentheses. WT = wild type, ns = not significant.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537198, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcription_of_rovA_and_rovM_in_distinct_nutritive_media_/1537198", "title"=>"Transcription of <i>rovA</i> and <i>rovM</i> in distinct nutritive media.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255112"], "description"=>"<p>Growth of <i>Y</i>. <i>pestis</i> strains in LB medium (A) and TMH supplemented with 0.2% galactose (B). Growth curves are the mean±SD of four independent biological replicates. The mean mean±SD of the growth rate (μ) is given in parentheses. All closed symbol growth curves represent strains containing multiple copies of <i>rovM</i>. A One Way ANOVA combined with a Tukey’s test was used to test significant differences in the growth rate between strains. The overall P-value for the ANOVA was P<0.0001. Significant differences in μ between strains are indicated by *** for P<0.001, ** for P<0.01 and * for P<0.05. Curly brackets group together strains that do not have significant differences. Capped bars indicate strains that are being compared.</p>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537189, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508.g002", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Y_pestis_strains_with_multiple_plasmid_encoded_copies_of_rovM_grow_at_a_faster_rate_/1537189", "title"=>"<i>Y</i>. <i>pestis</i> strains with multiple plasmid-encoded copies of <i>rovM</i> grow at a faster rate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-09-08 03:16:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/2255126"], "description"=>"<div><p><i>Yersinia pestis</i> has evolved as a clonal variant of <i>Yersinia pseudotuberculosis</i> to cause flea-borne biofilm–mediated transmission of the bubonic plague. The LysR-type transcriptional regulator, RovM, is highly induced only during <i>Y</i>. <i>pestis</i> infection of the flea host. RovM homologs in other pathogens regulate biofilm formation, nutrient sensing, and virulence; including in <i>Y</i>. <i>pseudotuberculosis</i>, where RovM represses the major virulence factor, RovA. Here the role that RovM plays during flea infection was investigated using a <i>Y</i>. <i>pestis</i> KIM6+ strain deleted of <i>rovM</i>, Δ<i>rovM</i>. The Δ<i>rovM</i> mutant strain was not affected in characteristic biofilm gut blockage, growth, or survival during single infection of fleas. Nonetheless, during a co-infection of fleas, the Δ<i>rovM</i> mutant exhibited a significant competitive fitness defect relative to the wild type strain. This competitive fitness defect was restored as a fitness advantage relative to the wild type in a Δ<i>rovM</i> mutant complemented <i>in trans</i> to over-express <i>rovM</i>. Consistent with this, <i>Y</i>. <i>pestis</i> strains, producing elevated transcriptional levels of <i>rovM</i>, displayed higher growth rates, and differential ability to form biofilm in response to specific nutrients in comparison to the wild type. In addition, we demonstrated that <i>rovA</i> was not repressed by RovM in fleas, but that elevated transcriptional levels of <i>rovM in vitro</i> correlated with repression of <i>rovA</i> under specific nutritional conditions. Collectively, these findings suggest that RovM likely senses specific nutrient cues in the flea gut environment, and accordingly directs metabolic adaptation to enhance flea gut colonization by <i>Y</i>. <i>pestis</i>.</p></div>", "links"=>[], "tags"=>["biofilm gut blockage", "kim", "rovm", "transcriptional levels", "flea gut environment", "fitness defect", "type", "Senses Nutritional Cues Suggesting", "infection", "strain", "Flea Gut Yersinia pestis", "flea gut colonization", "Δ rovM"], "article_id"=>1537202, "categories"=>["Uncategorised"], "users"=>["Viveka Vadyvaloo", "Angela K. Hinz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0137508", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_LysR_Type_Transcriptional_Regulator_RovM_Senses_Nutritional_Cues_Suggesting_that_It_Is_Involved_in_Metabolic_Adaptation_of_Yersinia_pestis_to_the_Flea_Gut/1537202", "title"=>"A LysR-Type Transcriptional Regulator, RovM, Senses Nutritional Cues Suggesting that It Is Involved in Metabolic Adaptation of <i>Yersinia pestis</i> to the Flea Gut", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-09-08 03:16:18"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"20", "full-text"=>"19", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"17", "full-text"=>"14", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"12", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"4", "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"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
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  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"4", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"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"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}

Relative Metric

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