The Condition-Dependent Transcriptional Landscape of Burkholderia pseudomallei
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{"title"=>"The Condition-Dependent Transcriptional Landscape of Burkholderia pseudomallei", "type"=>"journal", "authors"=>[{"first_name"=>"Wen Fong", "last_name"=>"Ooi", "scopus_author_id"=>"36442824900"}, {"first_name"=>"Catherine", "last_name"=>"Ong", "scopus_author_id"=>"7401968184"}, {"first_name"=>"Tannistha", "last_name"=>"Nandi", "scopus_author_id"=>"6603709858"}, {"first_name"=>"Jason F.", "last_name"=>"Kreisberg", "scopus_author_id"=>"8398634600"}, {"first_name"=>"Hui Hoon", "last_name"=>"Chua", "scopus_author_id"=>"7102800955"}, {"first_name"=>"Guangwen", "last_name"=>"Sun", "scopus_author_id"=>"8937476800"}, {"first_name"=>"Yahua", "last_name"=>"Chen", "scopus_author_id"=>"55870417100"}, {"first_name"=>"Claudia", "last_name"=>"Mueller", "scopus_author_id"=>"55866088000"}, {"first_name"=>"Laura", "last_name"=>"Conejero", "scopus_author_id"=>"6507831894"}, {"first_name"=>"Majid", "last_name"=>"Eshaghi", "scopus_author_id"=>"6602434183"}, {"first_name"=>"Roy Moh Lik", "last_name"=>"Ang", "scopus_author_id"=>"55882176600"}, {"first_name"=>"Jianhua", "last_name"=>"Liu", "scopus_author_id"=>"55706006500"}, {"first_name"=>"Bruno W.", "last_name"=>"Sobral", "scopus_author_id"=>"6603924027"}, {"first_name"=>"Sunee", "last_name"=>"Korbsrisate", "scopus_author_id"=>"6603206426"}, {"first_name"=>"Yunn Hwen", "last_name"=>"Gan", "scopus_author_id"=>"7102646497"}, {"first_name"=>"Richard W.", "last_name"=>"Titball", "scopus_author_id"=>"7005676571"}, {"first_name"=>"Gregory J.", "last_name"=>"Bancroft", "scopus_author_id"=>"7101830716"}, {"first_name"=>"Eric", "last_name"=>"Valade", "scopus_author_id"=>"6508079827"}, {"first_name"=>"Patrick", "last_name"=>"Tan", "scopus_author_id"=>"34769387900"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537390", "scopus"=>"2-s2.0-84884686614", "sgr"=>"84884686614", "pui"=>"369904001", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"24068961", "doi"=>"10.1371/journal.pgen.1003795"}, "id"=>"71506cd5-dc46-3a39-aee0-c4d5d4afbb77", "abstract"=>"Burkholderia pseudomallei (Bp), the causative agent of the often-deadly infectious disease melioidosis, contains one of the largest prokaryotic genomes sequenced to date, at 7.2 Mb with two large circular chromosomes (1 and 2). To comprehensively delineate the Bp transcriptome, we integrated whole-genome tiling array expression data of Bp exposed to >80 diverse physical, chemical, and biological conditions. Our results provide direct experimental support for the strand-specific expression of 5,467 Sanger protein-coding genes, 1,041 operons, and 766 non-coding RNAs. A large proportion of these transcripts displayed condition-dependent expression, consistent with them playing functional roles. The two Bp chromosomes exhibited dramatically different transcriptional landscapes--Chr 1 genes were highly and constitutively expressed, while Chr 2 genes exhibited mosaic expression where distinct subsets were expressed in a strongly condition-dependent manner. We identified dozens of cis-regulatory motifs associated with specific condition-dependent expression programs, and used the condition compendium to elucidate key biological processes associated with two complex pathogen phenotypes--quorum sensing and in vivo infection. Our results demonstrate the utility of a Bp condition-compendium as a community resource for biological discovery. Moreover, the observation that significant portions of the Bp virulence machinery can be activated by specific in vitro cues provides insights into Bp's capacity as an \"accidental pathogen\", where genetic pathways used by the bacterium to survive in environmental niches may have also facilitated its ability to colonize human hosts.", "link"=>"http://www.mendeley.com/research/conditiondependent-transcriptional-landscape-burkholderia-pseudomallei", "reader_count"=>51, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>12, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>3, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>12, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>3, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>6, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>30, "Medicine and Dentistry"=>5, "Computer Science"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>30}, "Computer Science"=>{"Computer Science"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Italy"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1202095"], "description"=>"<p>High-resolution views of different genomic features are depicted. All transcripts depicted were expressed above the median cut-off threshold. (A) Transcriptional annotation of the <i>Burkholderia pseudomallei</i> K96243 reference genome. The transcriptome map is presented along the chromosomal coordinates in a strand-specific manner, with the outermost track composed of Sanger annotated genes (orange), followed by novel genes (green), the Bp operons (purple) and finally the non-coding RNAs (ncRNAs; red). In all tracks, predicted genomic features that do not have an associated transcript in this study are colored in grey. The genes, operons and ncRNAs are arranged in a strand-specific manner by visualizing them in either the forward (+) or the reverse (−) tracks. The black vertical lines indicate the start/stop sites of the circular chromosomes. (B) Sanger genes and novel genes. Expressed strand-specific transcripts are presented as blue bars along the forward and reverse strands. Transcript boundaries correspond to predicted start and stop coordinates of Sanger annotated genes and FGENESB novel genes. (C) Differential expression of a Bp operon. Expression of a predicted flagella operon (<i>BPSL0026 – BPSL0032</i>) in a specific condition (taurine exposure). (D) Antisense transcription. <i>BPSL0095</i>, a gene coding for hypothetical protein exhibits antisense transcription upon exposure to human serum.</p>", "links"=>[], "tags"=>["transcripts", "bp"], "article_id"=>797723, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expressed_transcripts_in_the_Bp_condition_compendium_/797723", "title"=>"Expressed transcripts in the Bp condition compendium.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202097"], "description"=>"<p>(A) Condition-dependence of ncRNA expression. The heat-map depicts 766 identified ncRNAs and their patterns of expression across the condition compendium. Red depicts high expression, and green depicts low expression. (B) <i>BPNC10061R</i> expression is triggered by sorbitol. <i>BPNC10061R</i> is highly expressed under condition of osmotic stress (2M Sorbitol) compared to desiccation. (C) Secondary structure and species conservation of <i>BPNC10061R</i>. Consensus sequences homologous to <i>BPNC10061R</i> are found in <i>B. mallei</i>, <i>B. cenocepacia</i> and <i>B. thailandensis</i> strains. The sequences were aligned, and corresponding secondary structures were predicted.</p>", "links"=>[], "tags"=>["bp"], "article_id"=>797725, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_Bp_ncRNAs_/797725", "title"=>"Identification of Bp ncRNAs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202098"], "description"=>"<p>(A) Cumulative curves for expression of genes across the condition compendium. The graph represents the percentage of new genes expressed on Chr 1 (red) and Chr 2 (green) (y-axis) upon the successive addition of conditions (x-axis). This analysis was confined to Sanger genes to minimize annotation errors. (B) Chr 1 and Chr 2 exhibit constitutive and mosaic expression respectively. The graph relates the proportion of genes expressed on each chromosome (y-axis) under any particular number of conditions (x-axis). Chr 1 genes are expressed in most conditions (rightward upslope, red), while Chr 2 genes are expressed in specific conditions (leftward upslope, green). (C) Chr 1 genes exhibit higher expression levels than Chr 2 genes. Each dot represents the median expression of all detectably expressed genes on the respective chromosome, joined by the same condition. Chromosomal expression levels were compared using one-tailed paired t-test ().</p>", "links"=>[], "tags"=>["chromosomes", "transcriptional"], "article_id"=>797726, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bp_chromosomes_display_distinct_transcriptional_landscapes_/797726", "title"=>"Bp chromosomes display distinct transcriptional landscapes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202099"], "description"=>"<p>(A) Co-expression network. Nodes are individual genes, connected to one another by significant co-expression relationships (mutual information score ). The colours represent clusters over-represented in different Riley annotations, and their respective annotations are provided at the bottom. (B) Condition dependent cluster expression. The heat-map depicts representative clusters and patterns of expression across conditions. Gene expression levels were mean-normalized. (C) Inter-cluster relationships. The MRCN unit M036 consists of two clusters: C131 and C265, which include genes encoding proteins for degrading misfolded proteins and other genes with hypothetical functions. Thickness of edges represents the strength of the co-expression relationship between two genes. (D) Condition groups. The different condition-specific transcriptional profiles were clustered to one another based on similarities in expression of genes from the Bp core genome. Condition groups deemed to be stable by bootstrap assessment are marked in colors.</p>", "links"=>[], "tags"=>["bp", "condition-dependent"], "article_id"=>797727, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_expression_network_of_Bp_condition_dependent_transcription_/797727", "title"=>"Co-expression network of Bp condition-dependent transcription.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202101"], "description"=>"<p>Motifs were identified by analysing upstream sequences of constituent genes or operons in each cluster. The asterisk (*) indicates that the motif was detected using MEME and BioProspector. Tick symbols indicate that all cluster genes have a cognate homolog in the specified species (i.e. 100%), otherwise the proportion of homologs in that species is reported. Filled circles indicate that the discovered <i>cis</i>-motifs in Bp are significantly similar () to Bt or Bm. Motifs that match to known binding sites and corresponding binding proteins in other species are reported in the last column. Bt, <i>B. thailandensis</i>; Bm, <i>B. mallei</i>.</p>", "links"=>[], "tags"=>[], "article_id"=>797729, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Discovery_of_cis_regulatory_motifs_/797729", "title"=>"Discovery of <i>cis</i>-regulatory motifs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202102"], "description"=>"<p>(A) <i>pmlI</i> transcriptional network. The diagram shows genes differentially expressed in <i>pmlI</i>-disrupted mutants (>2-fold change), overlaid onto the condition-dependent network. Red and green spots represent up- and down-regulated genes. Yellow star - location of the <i>pmlI</i> gene. Genes coding for chemotaxis/mobility (violet-dotted line) and surface polysaccharide antigens (blue-dotted line) are shown. (B) Motility assays. The wild type parental strain Bp008 is motile, as shown by the more turbid medium. The QS mutant is non-motile and only grows along the line of inoculation. (C) Electron microscope photographs of the Bp capsule. The exopolysaccharide material typical of Bp capsule I (CPSI) is apparent in the parental strain Bp008 as shown by the black streaks surrounding the rod-shaped bacterium. In contrast, neither exopolysaccharide material nor capsule architecture is observable in the mutant. (D) Disruption of QS system results in altered bacterial phenotype. The wild type parental strain Bp008 exhibits a smooth colony phenotype when grown on agar plate whereas the QS mutant has a wrinkled phenotype.</p>", "links"=>[], "tags"=>["deconvolution", "qs"], "article_id"=>797730, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Condition_specific_deconvolution_of_QS_mutants_/797730", "title"=>"Condition-specific deconvolution of QS mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-12 01:47:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/1202129", "https://ndownloader.figshare.com/files/1202130", "https://ndownloader.figshare.com/files/1202131", "https://ndownloader.figshare.com/files/1202132", "https://ndownloader.figshare.com/files/1202133", "https://ndownloader.figshare.com/files/1202134", "https://ndownloader.figshare.com/files/1202135", "https://ndownloader.figshare.com/files/1202136", "https://ndownloader.figshare.com/files/1202137", "https://ndownloader.figshare.com/files/1202138", "https://ndownloader.figshare.com/files/1202139", "https://ndownloader.figshare.com/files/1202141", "https://ndownloader.figshare.com/files/1202142", "https://ndownloader.figshare.com/files/1202143", "https://ndownloader.figshare.com/files/1202144", "https://ndownloader.figshare.com/files/1202145", "https://ndownloader.figshare.com/files/1202146", "https://ndownloader.figshare.com/files/1202147", "https://ndownloader.figshare.com/files/1202148", "https://ndownloader.figshare.com/files/1202149", "https://ndownloader.figshare.com/files/1202150", "https://ndownloader.figshare.com/files/1202151", "https://ndownloader.figshare.com/files/1202152", "https://ndownloader.figshare.com/files/1202153"], "description"=>"<div><p><i>Burkholderia pseudomallei</i> (Bp), the causative agent of the often-deadly infectious disease melioidosis, contains one of the largest prokaryotic genomes sequenced to date, at 7.2 Mb with two large circular chromosomes (1 and 2). To comprehensively delineate the Bp transcriptome, we integrated whole-genome tiling array expression data of Bp exposed to >80 diverse physical, chemical, and biological conditions. Our results provide direct experimental support for the strand-specific expression of 5,467 Sanger protein-coding genes, 1,041 operons, and 766 non-coding RNAs. A large proportion of these transcripts displayed condition-dependent expression, consistent with them playing functional roles. The two Bp chromosomes exhibited dramatically different transcriptional landscapes — Chr 1 genes were highly and constitutively expressed, while Chr 2 genes exhibited mosaic expression where distinct subsets were expressed in a strongly condition-dependent manner. We identified dozens of <i>cis</i>-regulatory motifs associated with specific condition-dependent expression programs, and used the condition compendium to elucidate key biological processes associated with two complex pathogen phenotypes — quorum sensing and <i>in vivo</i> infection. Our results demonstrate the utility of a Bp condition-compendium as a community resource for biological discovery. Moreover, the observation that significant portions of the Bp virulence machinery can be activated by specific <i>in vitro</i> cues provides insights into Bp's capacity as an “accidental pathogen”, where genetic pathways used by the bacterium to survive in environmental niches may have also facilitated its ability to colonize human hosts.</p></div>", "links"=>[], "tags"=>["condition-dependent", "transcriptional"], "article_id"=>797753, "categories"=>["Biological Sciences", "Information And Computing Sciences"], "users"=>["Wen Fong Ooi", "Catherine Ong", "Tannistha Nandi", "Jason F. Kreisberg", "Hui Hoon Chua", "Guangwen Sun", "Yahua Chen", "Claudia Mueller", "Laura Conejero", "Majid Eshaghi", "Roy Moh Lik Ang", "Jianhua Liu", "Bruno W. Sobral", "Sunee Korbsrisate", "Yunn Hwen Gan", "Richard W. Titball", "Gregory J. Bancroft", "Eric Valade", "Patrick Tan"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003795.s001", "https://dx.doi.org/10.1371/journal.pgen.1003795.s002", "https://dx.doi.org/10.1371/journal.pgen.1003795.s003", "https://dx.doi.org/10.1371/journal.pgen.1003795.s004", "https://dx.doi.org/10.1371/journal.pgen.1003795.s005", "https://dx.doi.org/10.1371/journal.pgen.1003795.s006", "https://dx.doi.org/10.1371/journal.pgen.1003795.s007", "https://dx.doi.org/10.1371/journal.pgen.1003795.s008", "https://dx.doi.org/10.1371/journal.pgen.1003795.s009", "https://dx.doi.org/10.1371/journal.pgen.1003795.s010", "https://dx.doi.org/10.1371/journal.pgen.1003795.s011", "https://dx.doi.org/10.1371/journal.pgen.1003795.s012", "https://dx.doi.org/10.1371/journal.pgen.1003795.s013", "https://dx.doi.org/10.1371/journal.pgen.1003795.s014", "https://dx.doi.org/10.1371/journal.pgen.1003795.s015", "https://dx.doi.org/10.1371/journal.pgen.1003795.s016", "https://dx.doi.org/10.1371/journal.pgen.1003795.s017", "https://dx.doi.org/10.1371/journal.pgen.1003795.s018", "https://dx.doi.org/10.1371/journal.pgen.1003795.s019", "https://dx.doi.org/10.1371/journal.pgen.1003795.s020", "https://dx.doi.org/10.1371/journal.pgen.1003795.s021", "https://dx.doi.org/10.1371/journal.pgen.1003795.s022", "https://dx.doi.org/10.1371/journal.pgen.1003795.s023", "https://dx.doi.org/10.1371/journal.pgen.1003795.s024"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Condition_Dependent_Transcriptional_Landscape_of_Burkholderia_pseudomallei_/797753", "title"=>"The Condition-Dependent Transcriptional Landscape of <i>Burkholderia pseudomallei</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-12 01:47:42"}

PMC Usage Stats | Further Information

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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/Computational biology", "average_usage"=>[295, 511, 651, 775, 882, 992, 1100, 1201, 1304, 1400, 1486, 1570, 1650]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[302, 488, 607, 717, 832, 931, 1024, 1117, 1212, 1302, 1389, 1469, 1535]}, {"subject_area"=>"/Biology and life sciences/Genetics", "average_usage"=>[284, 491, 620, 738, 843, 945, 1043, 1137, 1225, 1315, 1400, 1479, 1555]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[272, 466, 589, 702, 806, 903, 995, 1086, 1176, 1258, 1347, 1422, 1493]}, {"subject_area"=>"/Computer and information sciences", "average_usage"=>[297, 488, 616, 724, 828, 939, 1038, 1127, 1223, 1311, 1393, 1479, 1556]}, {"subject_area"=>"/Computer and information sciences/Network analysis", "average_usage"=>[340, 548, 701, 844, 945, 1073, 1189, 1282, 1391, 1488, 1562, 1660, 1731]}]}
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