454 Pyrosequencing to Describe Microbial Eukaryotic Community Composition, Diversity and Relative Abundance: A Test for Marine Haptophytes
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{"title"=>"454 Pyrosequencing to Describe Microbial Eukaryotic Community Composition, Diversity and Relative Abundance: A Test for Marine Haptophytes", "type"=>"journal", "authors"=>[{"first_name"=>"Elianne", "last_name"=>"Egge", "scopus_author_id"=>"55312632300"}, {"first_name"=>"Lucie", "last_name"=>"Bittner", "scopus_author_id"=>"24480550400"}, {"first_name"=>"Tom", "last_name"=>"Andersen", "scopus_author_id"=>"56326390200"}, {"first_name"=>"Stéphane", "last_name"=>"Audic", "scopus_author_id"=>"6602862007"}, {"first_name"=>"Colomban", "last_name"=>"de Vargas", "scopus_author_id"=>"6603028438"}, {"first_name"=>"Bente", "last_name"=>"Edvardsen", "scopus_author_id"=>"6602419000"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84884191022", "sgr"=>"84884191022", "pui"=>"369822278", "isbn"=>"1932-6203", "pmid"=>"24069303", "doi"=>"10.1371/journal.pone.0074371"}, "id"=>"a1349f7b-32ca-316b-9188-5f8297ca3233", "abstract"=>"Next generation sequencing of ribosomal DNA is increasingly used to assess the diversity and structure of microbial communities. Here we test the ability of 454 pyrosequencing to detect the number of species present, and assess the relative abundance in terms of cell numbers and biomass of protists in the phylum Haptophyta. We used a mock community consisting of equal number of cells of 11 haptophyte species and compared targeting DNA and RNA/cDNA, and two different V4 SSU rDNA haptophyte-biased primer pairs. Further, we tested four different bioinformatic filtering methods to reduce errors in the resulting sequence dataset. With sequencing depth of 11000–20000 reads and targeting cDNA with Haptophyta specific primers Hap454 we detected all 11 species. A rarefaction analysis of expected number of species recovered as a function of sampling depth suggested that minimum 1400 reads were required here to recover all species in the mock community. Relative read abundance did not correlate to relative cell numbers. Although the species represented with the largest biomass was also proportionally most abundant among the reads, there was generally a weak correlation between proportional read abundance and proportional biomass of the different species, both with DNA and cDNA as template. The 454 sequencing generated considerable spurious diversity, and more with cDNA than DNA as template. With initial filtering based only on match with barcode and primer we observed 100-fold more operational taxonomic units (OTUs) at 99% similarity than the number of species present in the mock community. Filtering based on quality scores, or denoising with PyroNoise resulted in ten times more OTU99% than the number of species. Denoising with AmpliconNoise reduced the number of OTU99% to match the number of species present in the mock community. Based on our analyses, we propose a strategy to more accurately depict haptophyte diversity using 454 pyrosequencing.", "link"=>"http://www.mendeley.com/research/454-pyrosequencing-describe-microbial-eukaryotic-community-composition-diversity-relative-abundance", "reader_count"=>133, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>8, "Researcher"=>30, "Student > Ph. D. Student"=>39, "Student > Postgraduate"=>2, "Student > Master"=>24, "Other"=>6, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>8, "Researcher"=>30, "Student > Ph. D. Student"=>39, "Student > Postgraduate"=>2, "Student > Master"=>24, "Other"=>6, "Student > Bachelor"=>6, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Engineering"=>2, "Environmental Science"=>24, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>80, "Chemistry"=>1, "Earth and Planetary Sciences"=>9}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>9}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>80}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>9}, "Environmental Science"=>{"Environmental Science"=>24}}, "reader_count_by_country"=>{"Colombia"=>1, "Canada"=>1, "Argentina"=>1, "Belgium"=>1, "Norway"=>1, "Denmark"=>1, "United Kingdom"=>2, "Israel"=>1, "France"=>2, "Chile"=>2, "Germany"=>3, "Spain"=>4}, "group_count"=>8}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1203485"], "description"=>"<p>Compared to the initial distribution of species in terms of cell number (first row) and biomass (second row) in the mock community. The different combinations of template (DNA or RNA/cDNA), primer pair, (Hap454 or Prym454), and read filtering strategy are indicated on the figure. Initial Filtering (IF): Initial filtering based on match with barcode and primer, and removal of reads with Ns and/or homopolymers >8 bp, and reads that are shorter than 365 bp. Quality Score (QS): requiring minimum average quality score 30 over a 50 bp moving window along the read, in addition to IF. PyroNoise (PN): the PyroNoise algorithm as implemented in mothur, with default settings. AmpliconNoise (AN): AmpliconNoise as implemented in Qiime v.1.4.0, with default settings. Chimera identification by Perseus was applied to all datasets. The filtering strategies are described in the methods section.</p>", "links"=>[], "tags"=>["abundance", "454", "pyrosequencing", "reads", "mock"], "article_id"=>798710, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proportional_species_abundance_in_454_pyrosequencing_reads_from_a_mock_community_of_haptophytes_/798710", "title"=>"Proportional species abundance in 454 pyrosequencing reads from a mock community of haptophytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203487"], "description"=>"<p>Stress value: 0.04. The green point represents the proportional distribution of species by biomass in the original mixture of cells. The blue point represents the distribution in terms of cell number. Points that cluster together represent similar proportional species distributions. Red: DNA, yellow: RNA/cDNA, Upward triangle: Primer pair Hap454, Square: Primer pair Prym454. Black diamonds represent the pool of equal amounts of DNA from each species, amplified with primer pair Prym454.</p>", "links"=>[], "tags"=>["multidimensional", "scaling", "bray-curtis", "dissimilarities", "filtering"], "article_id"=>798712, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Non_metric_multidimensional_scaling_NMDS_of_Bray_Curtis_dissimilarities_between_the_samples_after_treatment_with_four_filtering_strategies_/798712", "title"=>"Non-metric multidimensional scaling (NMDS) of Bray-Curtis dissimilarities between the samples, after treatment with four filtering strategies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203488"], "description"=>"<p>(A) Based on DNA as a template in the PCR, (B) based on RNA/cDNA. The coordinates for each species correspond to the proportional abundance in the biomass (x-axis) and the proportional abundance among the reads (y-axis), after ‘Initial Filtering’-treatment of the reads. The straight line <i>x</i> = <i>y</i> shows the expected proportion of reads based on proportion of biomass. Species that lie below the line are proportionally less abundant in the reads than in the biomass, and vice versa. Note that the axes are scaled by squaring the values to better distinguish between the data points. The correlation between proportional biomass and read abundance with DNA as template was r = 0.94, p<0.001. With cDNA as template the correlation was r = 0.48, p = 0.16. When <i>P. pseudoroscoffensis</i> was omitted from the DNA-values the correlation was not significant (r = 0.24, p = 0.53). The data shown here are obtained with primer pair Hap454. We obtained a similar result with primer pair Prym454 (not shown.). Correlation between the primer pairs was r = 0.99 for DNA, r = 0.93 for cDNA.</p>", "links"=>[], "tags"=>["proportional", "abundance", "reads", "biomass", "mock"], "article_id"=>798713, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_between_proportional_species_abundance_among_the_reads_and_the_proportional_species_abundance_by_biomass_in_the_mock_community_/798713", "title"=>"Correlation between proportional species abundance among the reads and the proportional species abundance by biomass in the mock community.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203490"], "description"=>"<p>The 454 pyrosequencing reads were processed with four different sequence filtering strategies, and the number of OTUs were calculated with and without singletons. (A) DNA-Hap454, (B) DNA-Prym454, (C) cDNA-Hap454, (D) cDNA-Prym454, (E) DNApool. Initial Filtering (IF): Initial filtering based on match with barcode and primer, and removal of reads with Ns and/or homopolymers >8 bp, and reads that are shorter than 365 bp. Quality Score (QS): requiring minimum average quality score 30 over a 50 bp moving window along the read, in addition to IF. PyroNoise (PN): the PyroNoise algorithm as implemented in mothur, with default settings. AmpliconNoise (AN): AmpliconNoise as implemented in Qiime v. 1.4.0, with default settings. The filtering strategies are described in the methods section.</p>", "links"=>[], "tags"=>["otus", "clustering", "filtering"], "article_id"=>798715, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Number_of_OTUs_as_a_function_of_clustering_level_and_filtering_procedure_/798715", "title"=>"Number of OTUs as a function of clustering level and filtering procedure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203492"], "description"=>"<p>Constructed from unique OTUs at a clustering level of 99% similarity, obtained after the filtering procedures (A) Initial Filtering, (B) Quality Score, (C) PyroNoise and (D) AmpliconNoise. The numbers next to the branches indicate the placement of the reference sequences from the strains used in this study. (1) <i>Chrysochromulina throndsenii</i> (AJ246279), (2) <i>Diacronema ennorea</i> (JF714242), (3) <i>Emiliania huxleyi</i> (AF184167), (4) <i>Haptolina fragaria</i> (AM491013), (5) <i>Imantonia rotunda</i> (AJ246267), (6) <i>Isochrysis galbana</i> (AJ246266), (7) <i>Phaeocystis globosa</i> (AF182111), (8) <i>Pleurochrysis pseudoroscoffensis</i> (AM490973), (9) <i>Prymnesium kappa</i> (AJ246271), (10) <i>Prymnesium parvum</i> (AJ246269), (11) <i>Prymnesium polylepis</i> (AJ004866).</p>", "links"=>[], "tags"=>["trees", "filtering"], "article_id"=>798717, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neighbour_Joining_trees_of_OTU_99_obtained_after_the_different_filtering_procedures_in_sample_DNA_Hap454_/798717", "title"=>"Neighbour-Joining trees of OTU<sub>99%</sub> obtained after the different filtering procedures, in sample DNA-Hap454.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203493"], "description"=>"<p>χ<sup>2</sup>-values and corresponding p-values from comparisons of the species distributions in the samples, treated with ‘Initial Filtering’. Significant (p<0.05) differences in bold type. The Bray-Curtis dissimilarities between the samples are given in parentheses.</p>", "links"=>[], "tags"=>["proportional", "samples", "mock"], "article_id"=>798718, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.t004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_proportional_species_distribution_between_the_samples_and_the_species_distribution_in_the_mock_community_in_terms_of_cell_number_and_biomass_/798718", "title"=>"Comparison of proportional species distribution between the samples and the species distribution in the mock community in terms of cell number and biomass.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203494"], "description"=>"<p>(A) Number of reads, number of singletons, number of unique reads before any filtering, and proportion of chimeras detected by Perseus in the different samples. (B) Effect of filtering procedures on proportion of reads remaining after filtering, number of OTU<sub>99%</sub>, proportion of unclassified sequences, and error rate. ‘Unclassified’ reads are reads that could not be assigned to species level.</p>", "links"=>[], "tags"=>["454", "pyrosequencing", "reads", "bioinformatic", "filtering"], "article_id"=>798719, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.t005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_statistics_of_the_454_pyrosequencing_reads_and_effect_of_bioinformatic_filtering_strategies_/798719", "title"=>"Summary statistics of the 454 pyrosequencing reads and effect of bioinformatic filtering strategies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203495"], "description"=>"<p>The strains are maintained at the University of Oslo Culture Collection of Algae. Algal medium were IMR ½ at salinity 30 or 34, or ES at salinity 30 as indicated. Cell volumes were determined by CASY measurements, and cell diameter estimated assuming a spherical cell shape. Accession numbers are of the strains used (bold) or of a different strain of the same species. nd = no data.</p>", "links"=>[], "tags"=>["haptophyta", "strains", "included", "mock"], "article_id"=>798720, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_Haptophyta_strains_included_in_the_mock_community_/798720", "title"=>"Summary of Haptophyta strains included in the mock community.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203496"], "description"=>"<p>PCR primers for 454 pyrosequencing, targeting the V4 region of SSU rDNA.</p>", "links"=>[], "tags"=>["primers", "454", "targeting", "v4", "ssu"], "article_id"=>798721, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCR_primers_for_454_pyrosequencing_targeting_the_V4_region_of_SSU_rDNA_/798721", "title"=>"PCR primers for 454 pyrosequencing, targeting the V4 region of SSU rDNA.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203497"], "description"=>"<p>Overview over the 454 pyrosequencing samples.</p>", "links"=>[], "tags"=>["454", "pyrosequencing"], "article_id"=>798722, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_over_the_454_pyrosequencing_samples_/798722", "title"=>"Overview over the 454 pyrosequencing samples.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-09-12 03:33:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1203498", "https://ndownloader.figshare.com/files/1203499", "https://ndownloader.figshare.com/files/1203500", "https://ndownloader.figshare.com/files/1203501", "https://ndownloader.figshare.com/files/1203502", "https://ndownloader.figshare.com/files/1203503", "https://ndownloader.figshare.com/files/1203504", "https://ndownloader.figshare.com/files/1203505"], "description"=>"<div><p>Next generation sequencing of ribosomal DNA is increasingly used to assess the diversity and structure of microbial communities. Here we test the ability of 454 pyrosequencing to detect the number of species present, and assess the relative abundance in terms of cell numbers and biomass of protists in the phylum Haptophyta. We used a mock community consisting of equal number of cells of 11 haptophyte species and compared targeting DNA and RNA/cDNA, and two different V4 SSU rDNA haptophyte-biased primer pairs. Further, we tested four different bioinformatic filtering methods to reduce errors in the resulting sequence dataset. With sequencing depth of 11000–20000 reads and targeting cDNA with Haptophyta specific primers Hap454 we detected all 11 species. A rarefaction analysis of expected number of species recovered as a function of sampling depth suggested that minimum 1400 reads were required here to recover all species in the mock community. Relative read abundance did not correlate to relative cell numbers. Although the species represented with the largest biomass was also proportionally most abundant among the reads, there was generally a weak correlation between proportional read abundance and proportional biomass of the different species, both with DNA and cDNA as template. The 454 sequencing generated considerable spurious diversity, and more with cDNA than DNA as template. With initial filtering based only on match with barcode and primer we observed 100-fold more operational taxonomic units (OTUs) at 99% similarity than the number of species present in the mock community. Filtering based on quality scores, or denoising with PyroNoise resulted in ten times more OTU<sub>99%</sub> than the number of species. Denoising with AmpliconNoise reduced the number of OTU<sub>99%</sub> to match the number of species present in the mock community. Based on our analyses, we propose a strategy to more accurately depict haptophyte diversity using 454 pyrosequencing.</p></div>", "links"=>[], "tags"=>["pyrosequencing", "microbial", "eukaryotic"], "article_id"=>798723, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Elianne Egge", "Lucie Bittner", "Tom Andersen", "Stéphane Audic", "Colomban de Vargas", "Bente Edvardsen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074371.s001", "https://dx.doi.org/10.1371/journal.pone.0074371.s002", "https://dx.doi.org/10.1371/journal.pone.0074371.s003", "https://dx.doi.org/10.1371/journal.pone.0074371.s004", "https://dx.doi.org/10.1371/journal.pone.0074371.s005", "https://dx.doi.org/10.1371/journal.pone.0074371.s006", "https://dx.doi.org/10.1371/journal.pone.0074371.s007", "https://dx.doi.org/10.1371/journal.pone.0074371.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_454_Pyrosequencing_to_Describe_Microbial_Eukaryotic_Community_Composition_Diversity_and_Relative_Abundance_A_Test_for_Marine_Haptophytes_/798723", "title"=>"454 Pyrosequencing to Describe Microbial Eukaryotic Community Composition, Diversity and Relative Abundance: A Test for Marine Haptophytes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-12 03:33:20"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"34", "full-text"=>"28", "pdf"=>"18", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"19", "full-text"=>"14", "pdf"=>"6", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"7", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"1", "abstract"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
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  • {"unique-ip"=>"20", "full-text"=>"17", "pdf"=>"25", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"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"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"21", "full-text"=>"24", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"4", "year"=>"2015", "month"=>"4"}
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  • {"unique-ip"=>"16", "full-text"=>"19", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"6"}
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  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
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  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
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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]}]}
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