Genome-scale Analysis of Escherichia coli FNR Reveals Complex Features of Transcription Factor Binding
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{"title"=>"Genome-scale Analysis of Escherichia coli FNR Reveals Complex Features of Transcription Factor Binding", "type"=>"journal", "authors"=>[{"first_name"=>"Kevin S.", "last_name"=>"Myers", "scopus_author_id"=>"55779787100"}, {"first_name"=>"Huihuang", "last_name"=>"Yan", "scopus_author_id"=>"7403395508"}, {"first_name"=>"Irene M.", "last_name"=>"Ong", "scopus_author_id"=>"57196185583"}, {"first_name"=>"Dongjun", "last_name"=>"Chung", "scopus_author_id"=>"23992248900"}, {"first_name"=>"Kun", "last_name"=>"Liang", "scopus_author_id"=>"48761592700"}, {"first_name"=>"Frances", "last_name"=>"Tran", "scopus_author_id"=>"56442245500"}, {"first_name"=>"Sündüz", "last_name"=>"Keleş", "scopus_author_id"=>"6701338031"}, {"first_name"=>"Robert", "last_name"=>"Landick", "scopus_author_id"=>"7005639387"}, {"first_name"=>"Patricia J.", "last_name"=>"Kiley", "scopus_author_id"=>"7003423944"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84879620270", "doi"=>"10.1371/journal.pgen.1003565", "pui"=>"369235358", "pmid"=>"23818864", "scopus"=>"2-s2.0-84879620270", "issn"=>"15537390", "isbn"=>"1553-7404 (Electronic)\\n1553-7390 (Linking)"}, "id"=>"2d3e0512-90f9-3d7d-aaf0-367775961f66", "abstract"=>"FNR is a well-studied global regulator of anaerobiosis, which is widely conserved across bacteria. Despite the importance of FNR and anaerobiosis in microbial lifestyles, the factors that influence its function on a genome-wide scale are poorly understood. Here, we report a functional genomic analysis of FNR action. We find that FNR occupancy at many target sites is strongly influenced by nucleoid-associated proteins (NAPs) that restrict access to many FNR binding sites. At a genome-wide level, only a subset of predicted FNR binding sites were bound under anaerobic fermentative conditions and many appeared to be masked by the NAPs H-NS, IHF and Fis. Similar assays in cells lacking H-NS and its paralog StpA showed increased FNR occupancy at sites bound by H-NS in WT strains, indicating that large regions of the genome are not readily accessible for FNR binding. Genome accessibility may also explain our finding that genome-wide FNR occupancy did not correlate with the match to consensus at binding sites, suggesting that significant variation in ChIP signal was attributable to cross-linking or immunoprecipitation efficiency rather than differences in binding affinities for FNR sites. Correlation of FNR ChIP-seq peaks with transcriptomic data showed that less than half of the FNR-regulated operons could be attributed to direct FNR binding. Conversely, FNR bound some promoters without regulating expression presumably requiring changes in activity of condition-specific transcription factors. Such combinatorial regulation may allow Escherichia coli to respond rapidly to environmental changes and confer an ecological advantage in the anaerobic but nutrient-fluctuating environment of the mammalian gut.", "link"=>"http://www.mendeley.com/research/genomescale-analysis-escherichia-coli-fnr-reveals-complex-features-transcription-factor-binding", "reader_count"=>114, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>25, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>8, "Student > Master"=>11, "Other"=>7, "Student > Bachelor"=>6, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>25, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>8, "Student > Master"=>11, "Other"=>7, "Student > Bachelor"=>6, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>4, "Unspecified"=>4, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>20, "Mathematics"=>2, "Agricultural and Biological Sciences"=>71, "Medicine and Dentistry"=>2, "Veterinary Science and Veterinary Medicine"=>1, "Chemical Engineering"=>1, "Chemistry"=>1, "Computer Science"=>4, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>71}, "Computer Science"=>{"Computer Science"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>20}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>3}, "Chemical Engineering"=>{"Chemical Engineering"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>3, "Brazil"=>1, "Denmark"=>1, "United Kingdom"=>1, "Mexico"=>1, "Russia"=>1, "India"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1096068"], "description"=>"<p>The precision-recall curve used to determine the optimal threshold for predicting high quality FNR binding sites throughout the genome. The precision and recall values were determined for many ln(p-value) thresholds using the PatSer algorithm and the optimal value is identified by the arrow. The inset shows the FNR position weight matrix (PWM) constructed from the FNR ChIP-seq peak sequences. The height (y-axis) of the letters represents the degree of conservation at that position within the aligned sequence set (in bits), with perfect conservation being 2 bits. The x-axis shows the position of each base (1–14) starting at the 5′ end of the motif.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "binding", "sites", "updated"], "article_id"=>727469, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Precision_recall_curve_used_to_determine_the_prediction_threshold_of_FNR_binding_sites_and_updated_FNR_PWM_/727469", "title"=>"Precision-recall curve used to determine the prediction threshold of FNR binding sites and updated FNR PWM.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096082"], "description"=>"a<p>Genomic location within each FNR ChIP-seq peak with the highest read count (the summit of the peak).</p>b<p>First gene of the operon downstream of the FNR ChIP-seq peak, and operon designation was obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with both operons repressed by Fur, both genes are identified, separated by “/”.</p>c<p>Identification number (B-number) for the first gene in each operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with both operons repressed by Fur, both B-numbers are identified, separated by “/”.</p>d<p>Functional description of the products of the operons, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with operons repressed by Fur, the functions of both operons are listed, separated by “/”.</p>e<p>Reference for Fur repression of each operon.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "ChIP-seq", "lacking", "fnr-dependent", "gmm", "repressed"], "article_id"=>727483, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.t004", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Operons_associated_with_a_FNR_ChIP_seq_peak_and_lacking_a_FNR_dependent_change_in_expression_in_GMM_but_are_repressed_by_Fur_Category_4_/727483", "title"=>"Operons associated with a FNR ChIP-seq peak and lacking a FNR-dependent change in expression in GMM but are repressed by Fur (Category 4).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-20 02:04:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096067"], "description"=>"<p>The tracks are (from top): FNR ChIP-seq −O<sub>2</sub> (blue) with peaks upstream of a subset of genes labeled, FNR ChIP-chip in Δ<i>hns/ΔstpA</i> −O<sub>2</sub> (black), σ<sup>70</sup> subunit of RNAP ChIP-seq −O<sub>2</sub> (green), σ<sup>70</sup> subunit of RNAP ChIP-seq +O<sub>2</sub> (red), H-NS CHIP-chip +O<sub>2</sub> (light purple), H-NS ChIP-chip −O<sub>2</sub> (orange), IHF ChIP-chip −O<sub>2</sub> (purple), Fis ChIP-seq +O<sub>2 </sub><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Kahramanoglou1\" target=\"_blank\">[30]</a> (aqua), β subunit of RNAP −O<sub>2</sub> (yellow), β subunit of RNAP +O<sub>2</sub> (dark purple), and genomic coordinates. Locations of FNR binding sites are also shown: predicted FNR binding sites (red lines), FNR ChIP-seq peaks (black lines), FNR peaks upstream of operons showing a FNR-dependent change in expression (blue lines), FNR peaks co-activated by NarL/NarP (green lines), FNR peaks co-activated by CRP (purple lines), and FNR peaks repressed by Fur (yellow lines).</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "chip-chip"], "article_id"=>727468, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g001", "stats"=>{"downloads"=>1, "page_views"=>39, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ChIP_seq_and_ChIP_chip_data_used_in_this_study_/727468", "title"=>"ChIP-seq and ChIP-chip data used in this study.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096090", "https://ndownloader.figshare.com/files/1096092", "https://ndownloader.figshare.com/files/1096093", "https://ndownloader.figshare.com/files/1096094", "https://ndownloader.figshare.com/files/1096096", "https://ndownloader.figshare.com/files/1096098", "https://ndownloader.figshare.com/files/1096099", "https://ndownloader.figshare.com/files/1096100", "https://ndownloader.figshare.com/files/1096101", "https://ndownloader.figshare.com/files/1096102", "https://ndownloader.figshare.com/files/1096103", "https://ndownloader.figshare.com/files/1096104", "https://ndownloader.figshare.com/files/1096105", "https://ndownloader.figshare.com/files/1096106", "https://ndownloader.figshare.com/files/1096107", "https://ndownloader.figshare.com/files/1096108", "https://ndownloader.figshare.com/files/1096109", "https://ndownloader.figshare.com/files/1096110", "https://ndownloader.figshare.com/files/1096111", "https://ndownloader.figshare.com/files/1096112", "https://ndownloader.figshare.com/files/1096113"], "description"=>"<div><p>FNR is a well-studied global regulator of anaerobiosis, which is widely conserved across bacteria. Despite the importance of FNR and anaerobiosis in microbial lifestyles, the factors that influence its function on a genome-wide scale are poorly understood. Here, we report a functional genomic analysis of FNR action. We find that FNR occupancy at many target sites is strongly influenced by nucleoid-associated proteins (NAPs) that restrict access to many FNR binding sites. At a genome-wide level, only a subset of predicted FNR binding sites were bound under anaerobic fermentative conditions and many appeared to be masked by the NAPs H-NS, IHF and Fis. Similar assays in cells lacking H-NS and its paralog StpA showed increased FNR occupancy at sites bound by H-NS in WT strains, indicating that large regions of the genome are not readily accessible for FNR binding. Genome accessibility may also explain our finding that genome-wide FNR occupancy did not correlate with the match to consensus at binding sites, suggesting that significant variation in ChIP signal was attributable to cross-linking or immunoprecipitation efficiency rather than differences in binding affinities for FNR sites. Correlation of FNR ChIP-seq peaks with transcriptomic data showed that less than half of the FNR-regulated operons could be attributed to direct FNR binding. Conversely, FNR bound some promoters without regulating expression presumably requiring changes in activity of condition-specific transcription factors. Such combinatorial regulation may allow <i>Escherichia coli</i> to respond rapidly to environmental changes and confer an ecological advantage in the anaerobic but nutrient-fluctuating environment of the mammalian gut.</p></div>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "genome-scale", "fnr", "reveals", "transcription", "binding"], "article_id"=>727491, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003565.s001", "https://dx.doi.org/10.1371/journal.pgen.1003565.s002", "https://dx.doi.org/10.1371/journal.pgen.1003565.s003", "https://dx.doi.org/10.1371/journal.pgen.1003565.s004", "https://dx.doi.org/10.1371/journal.pgen.1003565.s005", "https://dx.doi.org/10.1371/journal.pgen.1003565.s006", "https://dx.doi.org/10.1371/journal.pgen.1003565.s007", "https://dx.doi.org/10.1371/journal.pgen.1003565.s008", "https://dx.doi.org/10.1371/journal.pgen.1003565.s009", "https://dx.doi.org/10.1371/journal.pgen.1003565.s010", "https://dx.doi.org/10.1371/journal.pgen.1003565.s011", "https://dx.doi.org/10.1371/journal.pgen.1003565.s012", "https://dx.doi.org/10.1371/journal.pgen.1003565.s013", "https://dx.doi.org/10.1371/journal.pgen.1003565.s014", "https://dx.doi.org/10.1371/journal.pgen.1003565.s015", "https://dx.doi.org/10.1371/journal.pgen.1003565.s016", "https://dx.doi.org/10.1371/journal.pgen.1003565.s017", "https://dx.doi.org/10.1371/journal.pgen.1003565.s018", "https://dx.doi.org/10.1371/journal.pgen.1003565.s019", "https://dx.doi.org/10.1371/journal.pgen.1003565.s020", "https://dx.doi.org/10.1371/journal.pgen.1003565.s021"], "stats"=>{"downloads"=>35, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genome_scale_Analysis_of_Escherichia_coli_FNR_Reveals_Complex_Features_of_Transcription_Factor_Binding/727491", "title"=>"Genome-scale Analysis of <i>Escherichia coli</i> FNR Reveals Complex Features of Transcription Factor Binding", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-06-20 02:04:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096075"], "description"=>"<p>Pathway map showing the glycolysis and mixed acid fermentation pathway overlaid with FNR ChIP-seq peak occupancy and expression changes <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Neuweger1\" target=\"_blank\">[124]</a>. Reactions are represented by arrows connecting metabolites and each operon is represented by a box with three ovals. The first oval of each box indicates the presence (blue) or absence (white) of a FNR ChIP-seq peak upstream of that operon. The color of the second oval indicates the impact of FNR on the expression of the operon (red is FNR repression, while green is FNR activation). The color of the third oval indicates the expression under WT aerobic and anaerobic growth conditions (red is WT aerobic expression, while green is WT anaerobic expression). The blue stars indicate newly identified direct targets of FNR regulation within this pathway.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fermentation", "pathway", "overlaid", "fnr"], "article_id"=>727476, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glycolysis_and_mixed_acid_fermentation_pathway_overlaid_with_FNR_and_O_2_regulation_/727476", "title"=>"Glycolysis and mixed acid fermentation pathway overlaid with FNR and O<sub>2</sub> regulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096071"], "description"=>"<p><b>A</b>) Venn diagram showing the overlap of FNR peaks identified only in the WT strain (purple), in both the WT and the Δ<i>hns</i>/Δ<i>stpA</i> strains (blue) or only in the Δ<i>hns</i>/Δ<i>stpA</i> strain (green). <b>B</b>) Example of a high-quality predicted FNR binding site (blue line) within <i>fimE</i> that showed no FNR binding in the WT strain (blue trace), but did show enrichment of H-NS in the WT strain (purple trace). A FNR ChIP-chip peak was identified in the Δ<i>hns</i>/Δ<i>stpA</i> strain (green trace) at the location of the predicted FNR binding site. <b>C</b>) The 193 FNR peaks found only in the Δ<i>hns</i>/Δ<i>stpA</i> strain with a statistical increase in FNR occupancy in the Δ<i>hns</i>/Δ<i>stpA</i> strain compared to the WT strain (p-value<0.05). Correlation of ChIP-chip peak average (log<sub>2</sub>(IP/INPUT) average) and the corresponding FNR PWM score (determined by PatSer <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Hertz1\" target=\"_blank\">[36]</a>). <b>D</b>) Correlation of ChIP-chip peak averages (log<sub>2</sub>(IP/INPUT) average) for FNR ChIP-chip peaks found in both WT and Δ<i>hns</i>/Δ<i>stpA</i> strains. Shown are peaks with no statistical difference in occupancy (red points) and those peaks that showed a statistical increase in FNR occupancy (blue points) in the Δ<i>hns</i>/Δ<i>stpA</i> strain compared to the WT strain (p-value<0.05).</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "occupancy", "compared"], "article_id"=>727472, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_FNR_occupancy_in_a_hns_stpA_strain_compared_to_WT_/727472", "title"=>"Identification of FNR occupancy in a Δ<i>hns</i>/Δ<i>stpA</i> strain compared to WT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096069"], "description"=>"<p><b>A</b>)Correlation between FNR ChIP-seq peak height (read count at the summit of the peak) and the degree of agreement to the FNR PWM at each peak (as scored by PatSer <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Hertz1\" target=\"_blank\">[36]</a>, with higher values indicating a better match to the FNR PWM). The line is the best-fit between peak height and PWM score. <b>B</b>) Comparison of the average ChIP-chip peak height for FNR in WT cultures (open symbols) (∼2.5 µM FNR) and PK8263 (P<i>tac</i>::<i>fnr</i>) cultures (closed symbols) at three [IPTG] concentrations: 4 µM IPTG (∼450 nM FNR), 8 µM IPTG (∼700 nM FNR), 16 µM IPTG (∼1.9 µM FNR). [FNR] determined by quantitative Western blot. Shown are four representative examples from the 39 regions examined (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565.s001\" target=\"_blank\">Figure S1</a>). A <i>t</i>-test shows a statistically significant difference in peak average at all genes between 4 µM IPTG and 8 µM IPTG.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "correlated", "pwm", "fnr"], "article_id"=>727470, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ChIP_peak_height_correlated_with_PWM_score_and_over_a_range_of_FNR_levels_/727470", "title"=>"ChIP peak height correlated with PWM score and over a range of FNR levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096083"], "description"=>"a<p>Operon showing a statistically significant FNR-dependent change in expression compared to WT but lacking a FNR ChIP-seq peak upstream. Operon definitions obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>b<p>Identification number (B-number) for the first gene in each operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>c<p>Cellular function of the product of the operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>d<p>FNR regulation of each operon as identified in the transcriptomic experiments performed in this study.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "lacking", "fnr", "ChIP-seq", "fnr-dependent", "gmm", "regulated", "rna", "fnrs"], "article_id"=>727484, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.t005", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Operons_lacking_a_FNR_ChIP_seq_peak_but_with_a_FNR_dependent_change_in_expression_in_GMM_that_are_known_to_be_regulated_through_the_action_of_the_small_regulatory_RNA_FnrS_Category_6_/727484", "title"=>"Operons lacking a FNR ChIP-seq peak but with a FNR-dependent change in expression in GMM that are known to be regulated through the action of the small regulatory RNA FnrS (Category 6).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-20 02:04:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096080"], "description"=>"a<p>Genomic location within each FNR ChIP-seq peak with the highest read count (the summit of the peak).</p>b<p>First gene of the operon downstream of the FNR ChIP-seq peak, and operon designation was obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with both operons activated by CRP, both genes are identified, separated by “/”.</p>c<p>Identification number (B-number) for the first gene in each operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with both operons activated by CRP, both B-numbers are identified, separated by “/”.</p>d<p>Functional description of the products of the operons, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>. For peaks located within divergent promoters with both operons activated by CRP, the functions of both operons are listed, separated by “/”.</p>e<p>Increase of expression (+) or no change in expression (−) of gene as determined using microarray analyses when WT <i>E. coli</i> was grown with carbon sources other than glucose (<i>e.g.</i> glycerol, xylose, mannose, arabinose). For peaks located within divergent promoters the expression changes of both operons are listed, separated by “/”.</p>f<p>Indication if the FNR site different than the CRP site (+) or overlapping the CRP site (−). For peaks located within divergent promoters the FNR and CRP site positions of both operons are listed, separated by “/”.</p>g<p>Reference for CRP activation of each operon or regulation in alternative carbon sources of each operon.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "ChIP-seq", "lacking", "fnr-dependent", "gmm", "co-activated", "crp"], "article_id"=>727481, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.t003", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Operons_associated_with_a_FNR_ChIP_seq_peak_and_lacking_a_FNR_dependent_change_in_expression_in_GMM_but_are_potentially_co_activated_by_CRP_and_FNR_Category_3_/727481", "title"=>"Operons associated with a FNR ChIP-seq peak and lacking a FNR-dependent change in expression in GMM but are potentially co-activated by CRP and FNR (Category 3).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-20 02:04:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096078"], "description"=>"a<p>Genomic location within each FNR ChIP-seq peak with the highest read count (the summit of the peak).</p>b<p>Operon downstream of the FNR ChIP-seq peak, and operon designation was obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>c<p>Identification number (B-number) for the first gene in each operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>d<p>Functional description of the products of the operons, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>e<p>Number of predicted FNR motifs identified within the FNR ChIP-seq peak region.</p>f<p>Location of FNR PWM (motif with best PatSer score used if more than one motif identified) relative to the transcription start site (if known). Start site locations obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a> and Kim <i>et al</i><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Kim1\" target=\"_blank\">[142]</a>.</p>g<p>Analysis of σ<sup>70</sup> occupancy (as determined using ChIP-seq data) under aerobic compared to anaerobic growth conditions. Increases (+) and decreases (−) in σ<sup>70</sup> occupancy were statistically determined using a one-sided, paired <i>t</i>-test and p-values were corrected using the Bonferroni method. Also listed are those sites with no σ<sup>70</sup> ChIP-seq peaks (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565.s008\" target=\"_blank\">Table S2</a>).</p>h<p>The expression of each operon in WT −O<sub>2</sub> cultures was compared to expression in WT +O<sub>2</sub> cultures. Each operon was determined to have a significant (>2 fold) increase (+), decrease (−) and no change (o) in WT −O<sub>2</sub> relative to WT +O<sub>2</sub> (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565.s018\" target=\"_blank\">Table S12</a>).</p>i<p>Reference for experimentally determined FNR binding at the location of the FNR ChIP-seq peak, if previously identified. Those operons without experimentally determined FNR binding data are marked “None”.</p>j<p>Reference for FNR-dependent change in expression of each operon, if previously identified. Those without previous FNR expression data are marked “None”.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "upstream", "fnr", "ChIP-seq", "fnr-dependent"], "article_id"=>727479, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.t001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Operons_with_an_upstream_FNR_ChIP_seq_peak_and_a_FNR_dependent_change_in_expression_under_GMM_/727479", "title"=>"Operons with an upstream FNR ChIP-seq peak and a FNR-dependent change in expression under GMM.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-20 02:04:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096079"], "description"=>"a<p>Genomic location within each FNR ChIP-seq peak with the highest read count (the summit of the peak).</p>b<p>First gene of the operon downstream of the FNR ChIP-seq peak, and operon designation was obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>c<p>Identification number (B-number) for the first gene in each operon, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>d<p>Functional description of the products of the operons, obtained from EcoCyc <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Keseler1\" target=\"_blank\">[70]</a>.</p>e<p>Growth conditions (presence of NO<sub>3</sub><sup>−</sup>, NO<sub>2</sub><sup>−</sup>, NarL or NarP) in which FNR activated the operon, according to <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Constantinidou1\" target=\"_blank\">[19]</a>.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "ChIP-seq", "lacking", "fnr-dependent", "gmm", "activated", "narl", "narp", "constantinidou"], "article_id"=>727480, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.t002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Operons_associated_with_a_FNR_ChIP_seq_peak_and_lacking_a_FNR_dependent_change_in_expression_in_GMM_but_are_activated_by_FNR_in_the_presence_of_NO_3_8722_NO_2_8722_NarL_or_NarP_Category_3_according_to_Constantinidou_et_al_19_/727480", "title"=>"Operons associated with a FNR ChIP-seq peak and lacking a FNR-dependent change in expression in GMM but are activated by FNR in the presence of NO<sub>3</sub><sup>−</sup>, NO<sub>2</sub><sup>−</sup>, NarL or NarP (Category 3) according to Constantinidou <i>et al.</i>[19].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-20 02:04:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096077"], "description"=>"<p>Representative examples of FNR directly activated (<i>dmsA</i>, panel A) and repressed (<i>ndh</i>, panel B) promoters confirmed in our study. Shown are the ChIP-seq data traces of anaerobic FNR (blue), anaerobic σ<sup>70</sup> (green) and aerobic σ<sup>70</sup> (red). ChIP-seq peak heights are represented on the y-axis (log<sub>2</sub> kernel density <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Valouev1\" target=\"_blank\">[115]</a>). The chromosomal location is shown on the x-axis with genes represented by arrows pointing in the direction of transcription. Known promoters are represented as red arrows and previously identified FNR binding sites are shown by blue brackets. The inset shows the linear expression levels for each gene from the RNA-seq experiments comparing FNR<sup>+</sup> and <i>Δfnr</i> -O<sub>2</sub> expression. Linear tag density <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003565#pgen.1003565-Li2\" target=\"_blank\">[125]</a> for each gene is shown on the y-axis.</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "examples", "fnr", "activated", "repressed"], "article_id"=>727478, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Representative_examples_of_FNR_directly_activated_and_repressed_promoters_/727478", "title"=>"Representative examples of FNR directly activated and repressed promoters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1096073"], "description"=>"<p><b>A</b>) Graphical representation of the FNR transcriptional network. FNR is shown in the blue octagon, while other TFs (CRP, Fur, NarL) are shown as purple diamonds. Circles represent operons with an upstream FNR ChIP-seq peak, while squares represent operons indirectly regulated by FNR. Dark blue circles are operons directly dependent on FNR for expression, with the lighter blue circles representing FnrS other TFs (CaiF, BssR, PdhR, GadE) that potentially control the indirect regulon, shown by yellow squares. Red circles are operons known or predicted to be co-regulated by FNR and other TFs, while green circles have other potential regulatory mechanisms with FNR. <b>B</b>) Each box represents different categories of FNR regulation identified in this study. Categories 1 and 2 (upper left and middle boxes) show direct activation and repression of operons by FNR (blue ovals). Category 3 (upper right box) show co-activation by other TFs (red star; <i>e.g.</i> CRP, NarL, NarP) and Category 4 (lower left box) shows TF repression that prevents FNR regulation (green rectangle; <i>e.g.</i> Fur). Category 5 (lower middle box) represents operons with other possible regulatory mechanisms with FNR and Category 6 (lower right box) shows the subset of the indirect regulon affected by other TFs and, for example, by the small, regulatory RNA FnrS (red line).</p>", "links"=>[], "tags"=>["Computational biology", "microarrays", "Regulatory networks", "genomics", "Functional genomics", "Genome expression analysis", "microbiology", "Microbial physiology", "Model organisms", "Prokaryotic models", "Escherichia coli", "fnr", "transcriptional", "categories"], "article_id"=>727474, "categories"=>["Biological Sciences"], "users"=>["Kevin S. Myers", "Huihuang Yan", "Irene M. Ong", "Dongjun Chung", "Kun Liang", "Frances Tran", "Sunduz Keles", "Robert Landick", "Patricia J. Kiley"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003565.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_FNR_transcriptional_network_and_categories_of_FNR_regulation_/727474", "title"=>"The FNR transcriptional network and categories of FNR regulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-20 02:04:34"}

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Relative Metric

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