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Research Article

cAMP Receptor Protein Controls Vibrio cholerae Gene Expression in Response to Host Colonization

Jainaba Manneh-Roussel, James R. J. Haycocks, Andrés Magán, Nicolas Perez-Soto, Kerstin Voelz, Andrew Camilli, Anne-Marie Krachler, David C. Grainger
Susan Gottesman, Editor
Jainaba Manneh-Roussel
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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James R. J. Haycocks
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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Andrés Magán
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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Nicolas Perez-Soto
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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Kerstin Voelz
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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Andrew Camilli
bDepartment of Molecular Biology and Microbiology, Tufts University, Boston, Massachusetts, USA
cHoward Hughes Medical Institute, Tufts University, Boston, Massachusetts, USA
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Anne-Marie Krachler
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
dDepartment of Microbiology and Molecular Genetics, University of Texas McGovern Medical School at Houston, Houston, Texas, USA
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David C. Grainger
aInstitute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom
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Susan Gottesman
National Cancer Institute
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DOI: 10.1128/mBio.00966-18
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  • FIG 1 
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    FIG 1 

    Global analysis of CRP and σ70 binding in Vibrio cholerae. (a) Genome-wide distribution of CRP and the RNA polymerase σ70 subunit in Vibrio cholerae strain N16961. Plots are shown for the two N16961 chromosomes. In each plot, the tick mark at the 12 o’clock position represents the first base pair (bp) of the chromosome and subsequent tick marks are spaced by 0.5 Mbp. In each plot, the first and second tracks (mauve lines) show the positions of genes, the third track (blue) is the σ70 binding profile, and the fourth track (orange) is the CRP binding profile. (b) DNA sequence motifs recovered from CRP and σ70 binding peaks. Top, DNA sequence motif identified by MEME present in DNA sequences associated with σ70 binding; bottom, DNA sequence motif generated from CRP binding peaks. (c) Locations of CRP and RNA polymerase binding peaks with respect to genes. Histogram depicts the distances between ChIP-seq binding peaks and the nearest 5′ end of a gene; data for CRP binding are in orange, and data for σ70 binding are in blue. Each binding peak was allocated to a series of 100-bp bins. Inset, Venn diagram that illustrates the number of overlapping CRP and σ70 binding peaks. (d) Overlap between σ70 DNA binding and transcription start sites. The Venn diagram illustrates numbers of overlapping σ70 binding sites (blue) and transcription start sites (green) (40). A σ70 binding peak centered within 50 bp of a transcription start was considered to overlap. To generate the P value, we used the chi-square test. To generate values for the expected overlap between the data sets, assuming no correlation, we randomized the positions of the σ70 peaks. (e) Overlap between CRP binding and CRP-regulated genes. The Venn diagram illustrates overlap between genes adjacent to CRP binding peaks (orange) and genes that were differently expressed in the absence of CRP (mauve) (41). To generate the P value, we used the chi-square test. To generate values for the expected overlap between the data sets, assuming no correlation, we randomly selected 831 genes from the V. cholerae genome and determined the number that were adjacent to CRP binding peaks.

  • FIG 2 
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    FIG 2 

    Repression of the rtxBDE operon by CRP. (a) The intergenic region between rtxBDE and rtxHCA is associated with CRP but not σ70. The graphs illustrate ChIP-seq data for CRP (orange) and σ70 (blue) binding to the rtx locus. Data have been smoothed in a 100-bp window. Genes are depicted by mauve arrows and labeled. (b) Sequence of the rtxBDE-rtxHCA gene regulatory region. The DNA sequence between rtxBDE and rtxHCA is shown. The center of the CRP binding peak identified in our ChIP-seq analysis is indicated by an asterisk. Putative CRP sites (orange) are underlined and labeled. The rtxH transcription start site (+1) is underlined and further highlighted by a bent arrow. The associated promoter −10 element is similarly colored and underlined. Two transcription start sites for rtxB are also labeled in the same way. The 5′ end of the rtxB.1 DNA fragment (see the legend to panel e) is indicated by an inverted black triangle. Point mutations used to inactivate CRP binding sites or promoter −10 elements are shown in red. (c) DNase I footprint of CRP binding to the rtxBDE-rtxHCA gene regulatory region. Results of a DNase I footprinting experiment using the rtxBDE intergenic region and purified V. cholerae CRP. The experiment is calibrated with a Maxam-Gilbert GA sequencing ladder, and positions relative to the P1rtxB transcription start site (+1) are labeled. The triangle indicates the addition of CRP at concentrations of 175, 350, 700, 1,400, 2,100, or 2,800 nM. The positions of the predicted CRP binding sites are shown by orange boxes. (d) Primer extension analysis of rtxH and rtxB promoter-derived transcripts. The gel shows arbitrary Sanger sequencing reactions for calibration (lanes 1 to 4) and primer extension products for rtxB (lanes 5 and 6) or rtxH (lanes 7 and 8) promoter-derived transcripts. (e) Transcripts derived from the rtxBDE intergenic region in vitro. The gel shows transcripts generated by V. cholerae RNA polymerase σ70 holoenzyme using the rtxBDE intergenic region, cloned in plasmid pSR, as a DNA template. The RNAI transcript is derived from the plasmid replication origin and serves as an internal control. The rtxB.1 derivative contains a truncated version of the rtxBDE intergenic region. The site of the truncation is marked in panel b. Mutations introduced to disrupt potential −10 hexamers are noted above the gel and are also shown in panel b. (f) Activity of PrtxH is not affected by CRP. Results of a β-galactosidase assay done using lysates of N16961 cells transformed with derivatives of the lacZ reporter plasmid, pRW50T, where lacZ expression is controlled by PrtxH. (g) Expression of rtxB is repressed by CRP. Results of a β-galactosidase assay done using lysates of N16961 cells transformed with derivatives of the lacZ reporter plasmid, pRW50T, where lacZ expression is controlled by P1rtxB and P2rtxB.

  • FIG 3 
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    FIG 3 

    Nutrient availability controls rtxBDE expression in a CRP-dependent manner. Results of β-galactosidase assays done using lysates of N16961 cells transformed with derivatives of the lacZ reporter plasmid, pRW50T, carrying different rtxB::lacZ fusions. Cells were grown in M9 minimal medium, LB, or LB supplemented with 0.4% (vol/vol) glucose.

  • FIG 4 
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    FIG 4 

    CRP is required for efficient host colonization and dependent induction of rtxBDE. (a) Colonization of the zebrafish larva intestinal tract by V. cholerae strain E7946 and derivatives. The three panels show representative fluorescence microscopy images overlaid on light microscopy images of zebrafish larvae colonized with the indicated V. cholerae strains. All bacterial strains were transformed with plasmid pMW-GFP and express green fluorescent protein (GFP) to facilitate detection. Further images are shown in Fig. S1c in the supplemental material. (b) Survival of zebrafish larvae following infection with V. cholerae strain E7946 and derivatives. (c) Expression of rtxBDE is induced by zebrafish larva colonization. Results of a β-galactosidase assay done using lysates of bacterial cells growing planktonically in E3 medium or obtained from the zebrafish intestinal tract. Strains are indicated and were transformed with derivatives of pRW50T encoding different rtxB::lacZ fusions.

  • FIG 5 
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    FIG 5 

    CRP couples the expression of many V. cholerae genes to host colonization. Results of β-galactosidase assays done using lysates of bacterial cells grown planktonically in E3 medium or obtained from the zebrafish intestinal tract. Strains are indicated and were transformed with derivatives of pRW50T encoding different LacZ fusions. Significant differences between levels of β-galactosidase activity in planktonic and intestinal populations were observed in all cases for wild-type cells (P values determined using a two-tailed Student’s t test were 0.0014, 0.0011, 0.0003, 0.0005, and 0.0037 for the tolC, acfA, acfD, nudF, and hlyA promoters, respectively). For cells lacking CRP, a significant, albeit much smaller difference was only apparent for the acfD promoter (P = 0.0036).

Tables

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  • Supplemental Material
  • TABLE 1 

    CRP binding peaks identified by ChIP-seq in the V. cholerae strain N16961 genome

    Genome
    component
    Peak centeraSite centerbSite P valuecSequencedGene(s) close to
    CRP binding sitese
    CRP
    regulatedf
    Chromosome I5577155796.53.5E−03AGTGACTAAGCGTACA23Sa1ND
    9987199790.58.3E−03TGTTACGAATATTACAglpE<(VC0103)Yes
    134815134755.55.6E−03TTTGTTTTGGATCGATVC0142a<>VC0143Yes
    150732150753.53.2E−07TGAGATTCAAATCACAVC0159<>16SbYes
    177320177327.53.2E−03CATAATCTGTATCAAAVC0175Yes
    242521242505.57.1E−03TAAGGTTTAAGCCATT(VC0237)No
    249227249187.59.8E−03TTTGAAGGATGGCGTT(VC0242)No
    264229264210.55.1E−03TTAAATATGTATCATAVC0258><VC0259No
    274582NAgNANA(VC0269)No
    294153294127.57.6E−03TGTAGGTGATATCTCAVC0284No
    454607454517.53.4E−03TGTGTTGTTGCTCAATVC0423<>VC0424Yes
    516492516436.51.7E−03TGACAGTAATATCACTVC0485<>VC0486No
    522621522571.55.3E−03AGTCCATTTGCTCACAVC0489No
    527963527988.51.1E−03AGTTATTTTTTTCACTVC0493<>VC0494No
    569841569895.54.9E−04AACGATTTTCCTCATAVC0537<>VC0538Yes
    657711657766.55.2E−05TGTGACTCCCTTCGCAVC0621No
    676093676049.52.4E−03AATGATATAAATCCAAompU<>greAYes
    707829707908.57.3E−03GCCGCTTGGCATCACAVC0661<>VC0662No
    712256712206.51.6E−03TGCAATCTAAGTCATTVC0665No
    713923714007.51.1E−03TTAGAATTTAATCGTAVC0666No
    748263748338.54.1E−03GGCGAGATTACGCGTAVC0699<>VC0700No
    756779756854.58.4E−07TGTGATAAAAGTCACTVC0706No
    762509762522.51.8E−03TCTGACAATTATCTCGVC0713Yes
    788515788501.56.9E−03TGTGAAATTTCACAAGVC0734No
    815345815346.53.6E−07TGTGATATGATTCACAengAYes
    818079818158.52.6E−03GGTTAATTAAGTCGCAVC0765Yes
    819917819936.51.0E−02CGTCCGCAATATCAAAVC0766<>VC0767No
    880295880357.55.3E−03TATGAGAAAGATAAAA(VC0821)No
    888697888746.52.1E−03TGCAATTAAGTTCTCAtcpI<>tcpPYes
    894874894817.57.9E−03TATTATTGGATTCATT(VC0833)No
    904634NANANA(VC0842)Yes
    906219NANANAacfA<>acfDNo
    911066911128.53.1E−03TATGATGAAAAACATTVC0845><VC0846No
    936058936026.51.5E−03AAAGAGCTAAATCGTT(VC0870)No
    999018999093.59.6E−03CTTGGTTGTTTTCAATVC0932<>VC0934Yes
    10118351011745.52.4E−03AGTGAGCTTGCCCAAG(VC0947)No
    10375601037566.51.2E−03TTCGACGCATTTCAAAVC0972Yes
    10540131054031.51.4E−05CGTGATTTTTGTCGCGtppB<>rfaHNo
    10611591061198.51.5E−06GGTGATTAGGATCACAnagA<>VC0995No
    10901451090112.55.6E−04TGTGATGTTTGGCATCVC1021No
    11002041100264.54.0E−05TGTGATGCAAATCGATVC1034Yes
    11394711139535.54.0E−03TCTGATTATTTTCAAGVC1073No
    11749541174946.56.7E−06TGTGGTTTATGTCACAVC1104No
    11987581198847.56.0E−05TGTGAGCTGTGGCACTVC1130<>VC1131No
    12125391212568.54.7E−03AGAGGCGAAATTCATTVC1142<>clpSYes
    12247861224787.54.2E−06TGTGATACTGGTCTCAVC1152<>tfoXNo
    13829251382894.55.9E−03TGTGAGAATTGTTAATVC1301Yes
    13967721396717.51.2E−03ATTGATGTCACTCAAAVC1313<>VC1314Yes
    14089361408937.53.8E−03TTTTAACTGGTTCACAVC1323<>VC1325Yes
    15490421549038.56.9E−03TGTGCAATTTGTCTGArtxB<>rtxHYes
    15681641568072.55.5E−03TATGAAAATGATGATActxANo
    16836521683636.52.0E−03AGTGATGGGGTTAACAVC1571<>VC1572No
    17035841703620.56.4E−03TAATAAAAATGTCACAVC1592No
    17416001741668.54.7E−05TGTGATACGCTTCTCGVC1620<>VC1621Yes
    17766781776642.54.8E−03AGTGATTTATCACTAAVC1649<>VC1650No
    17895101789532.51.9E−05TATGACCAGTATCGCAVC1656<>VC1658No
    19034701903498.58.0E−04TTTGAGTTAATTCAAT(VC1736)Yes
    19196511919579.56.2E−03TGTGCTAAATACAACG(VC1771)Yes
    1922932NANANA(VC1773)No
    19672951967278.52.1E−06CGAGATCTAAATCACAVC1825<>VC1826No
    19847761984846.53.3E−04TGAGAACTTTGTCAAAVC1844Yes
    19900741990055.54.4E−03GTCGAGACCACTCATAVC1851No
    19940541994088.55.4E−03ATTAATAAAAATCAAAompT<>dinGYes
    20048392004771.52.9E−03TTTTAACAAAGTCACAVC1864<>VC1865Yes
    20553952055442.56.2E−03CATCAAATTTTTCACAVC1904<>VC1905Yes
    20590772059085.59.7E−03TGCCACGCAACGCTCAcysB<>VC1909Yes
    21683872168407.54.2E−03TTTGAGGAATTCCGCTVC2013Yes
    21906662190734.55.0E−03TGTGCGAATGTTAACAVC2035No
    21931102193078.51.1E−05AACGATATAAATCACAVC2036<>VC2037Yes
    23744762374498.53.0E−05TGTGAGCTTTATCATGVC2219<>VC2220No
    24337432433742.51.1E−06GGTGATTAAAATCACAVC2278<>VC2279No
    24576082457631.51.3E−06AGCGATTAAGATCACAVC2303<>VC2305No
    25373892537396.54.6E−03TGTGAATTCGGTGAAAgltBNo
    25503522550386.58.7E−03TGTTACTGGTATAACA(VC2385)No
    25513562551299.53.5E−03AGTGATAAAAGTGAAG(VC2386)No
    25586082558615.53.7E−03GATGAATTTATTCATCVC2390Yes
    26103822610307.59.8E−03GCTGATTCGCGTCTTGVC2435<>tolCNo
    26538382653780.57.5E−04CGCGAGTCTCTTCAAAVC2473Yes
    26673262667406.58.8E−03TAATATTCACGTCAAAVC2486No
    26993902699329.51.5E−03GGTGATGGTCGCCACTpyrBNo
    27433492743361.58.1E−04ATCGCGTCACATCACAVC2561<>cpdBNo
    27879392787903.53.0E−04TGAGATAAACCCCACAVC2618Yes
    28452462845280.55.7E−07TGTGATTTTCATCACGVC2677No
    28647572864763.59.2E−04ATAGATAAAACTCTCAVC2698<>aspAYes
    29334682933432.57.5E−04TTTGATTATCATCAAC16sgND
    29368692936904.53.1E−04TTCGATACCAAGCACA23ShND
     
    Chromosome II1206712085.55.4E−08TGTGATCCGAATCACTVCA0012<>VCA0013Yes
    8636486274.55.8E−03GTCGAAATTCGCCACAVCA0076No
    9901698927.52.0E−07TGTGATCTTTATCACTVCA0089No
    114856114864.58.6E−03TTTAATAGATTTCTCAVCA0104<>VCA0105No
    152867152849.57.4E−04TGTGATTGATGTGGCAVCA0138No
    181749181688.52.5E−03TGAGAAAGCATTCAAAVCA0164<>VCA0165No
    217815217798.56.0E−03TGTTATAAAAACCAAT(VCA0200)No
    237015237049.56.6E−03TAAGAATTATTTTACAhlyB<>hlyANo
    247246247185.57.5E−03TTGGCATAGCATCACAVCA0224<>VCA0225Yes
    267292267253.53.7E−03TGATAGGTAGATCACCVCA0246<>VCA0247No
    300413300391.58.4E−03TGCCCTATCTATCAAAVCA0281Yes
    334916334914.54.3E−03ATTGACAGCTATCTAA(VCA0334)No
    458259458254.53.8E−03CGTGATTAAAAACGTCVCA0523Yes
    481906481918.52.0E−03TTTCATAAAAGTCACGVCA0544<>VCA0545Yes
    492167492243.56.9E−07TGTGATTGGAATCACTVCA0554<>VCA0556No
    564616NANANA(VCA0628)Yes
    598381598370.54.9E−04GTTGACAACAGTCACA(VCA0662)<>VCA0663No
    630430630499.51.5E−03AATGATAGATAACACAVCA0691Yes
    687485687472.53.3E−03CGTGATCGACATTAAA(VCA0742)>VCA0743No
    741821741822.57.8E−06TGTGCTTTACATCACTVCA0801Yes
    784413784364.52.1E−05TGTGATGCCGCTCGCAVCA0840Yes
    785337785352.55.1E−04TTTGAACTTAGTCATTVCA0843Yes
    801056801043.51.7E−05TGTGAAATGGCTCGCAVCA0849Yes
    832501832514.56.2E−03TGCGACCTTGATTAACVCA0880Yes
    849892849906.53.0E−03GTTGACGCCTTTCTCAVCA0896Yes
    870862870876.51.1E−03AATGATCAGGGGCAAAVCA0917<>VCA0919Yes
    874452874411.54.1E−03TATAAATCAAATCATTVCA0923Yes
    897315897352.54.8E−06AGCGAGCCAAATCACAVCA0945<>VCA0946Yes
    902411902377.56.6E−03TGAAACACTTACCACTVCA0952Yes
    930851NANANA(VCA0982)<>VCA0983No
    963517963536.58.2E−04TGTTAAGCAAATCGCAVCA1013<>VCA1015No
    994614994588.52.5E−05CATGACACAGGTCACAVCA1043<>(VCA1044)Yes
    10159571015902.52.0E−05TTTGACCATTATCACAVCA1063No
    • ↵a Center of peak for CRP binding in ChIP-seq assays.

    • ↵b Center of binding site identified by FIMO (Find Individual Motif Occurrences) using DNA motif recovered from the ChIP-seq data by MEME (Multiple Em for Motif Elicitation).

    • ↵c P value assigned to each site by FIMO describing the significance of the match to the motif generated by MEME.

    • ↵d DNA sequence of site identified by FIMO.

    • ↵e Parentheses indicate that the CRP site is located within that gene. Pairs of arrows represent divergent (<>) or convergent (><) genes. Single arrows indicate that gene pairs are in the same orientation on either the forward (>) or reverse (<) strand. Gene identification numbers are shown unless an alternative name for the gene is provided in the genome annotation or the wider literature. Genes regulated by ToxR or ToxT are underlined.

    • ↵f CRP-regulated genes described by Fong and Yildiz (41). ND, not detected: genes encoding stable rRNA species were not included in the transcriptome analysis and so no change in transcription could be detected.

    • ↵g NA, not applicable.

Supplemental Material

  • Figures
  • Tables
  • FIG S1 

    (a) Transcription from PrtxH requires identified promoter elements. (i) The results of primer extension assays that detect the rtxH transcript derived from plasmid pRW50T carrying the rtxH (panel ii, top) or truncated rtxH.1 (panel ii, bottom) DNA fragment. (ii) PrtxH is highlighted blue and CRP binding sites are shown in orange. (b) P1rtxB and P2rtxB make similar contributions to rtxB transcription. The figure shows β-galactosidase activity measurements for lysates of V. cholerae cells transformed with pRW50T derivatives carrying the full-length rtxB regulatory region (rtxB), a truncated derivative lacking CRP binding sites (rtxB.1), or versions of the truncated fragment with indicated promoter mutations. (c) Effects of crp and tcpA on zebrafish larva colonization. (i) Images from multiple zebrafish larvae colonized with the indicated V. cholerae strains. All strains were transformed with plasmid pMW-GFP to facilitate visualization of bacteria. (ii) Quantified fluorescence from multiple microscopy images. (d) Raw gel images. Download FIG S1, PDF file, 0.4 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1 

    Strains, plasmids, and oligonucleotides. Download TABLE S1, DOCX file, 0.03 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S1 

    N16961 chromosome I GenBank file. Download DATA SET S1, TXT file, 6 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S2 

    N16961 chromosome II GenBank file. Download DATA SET S2, TXT file, 2.2 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S3 

    CRP ChIP-seq Artemis graph file for N16961 chromosome I. Download DATA SET S3, TXT file, 17.5 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S4 

    CRP ChIP-seq Artemis graph file for N16961 chromosome II. Download DATA SET S4, TXT file, 6.4 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S5 

    RNA polymerase σ70 ChIP-seq Artemis graph file for N16961 chromosome I. Download DATA SET S5, TXT file, 10.7 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S6 

    RNA polymerase σ70 ChIP-seq Artemis graph file for N16961 chromosome II. Download DATA SET S6, TXT file, 4.2 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TEXT S1 

    Instructions for viewing ChIP-seq data in the Artemis genome browser. Download TEXT S1, PDF file, 0.6 MB.

    Copyright © 2018 Manneh-Roussel et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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cAMP Receptor Protein Controls Vibrio cholerae Gene Expression in Response to Host Colonization
Jainaba Manneh-Roussel, James R. J. Haycocks, Andrés Magán, Nicolas Perez-Soto, Kerstin Voelz, Andrew Camilli, Anne-Marie Krachler, David C. Grainger
mBio Jul 2018, 9 (4) e00966-18; DOI: 10.1128/mBio.00966-18

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cAMP Receptor Protein Controls Vibrio cholerae Gene Expression in Response to Host Colonization
Jainaba Manneh-Roussel, James R. J. Haycocks, Andrés Magán, Nicolas Perez-Soto, Kerstin Voelz, Andrew Camilli, Anne-Marie Krachler, David C. Grainger
mBio Jul 2018, 9 (4) e00966-18; DOI: 10.1128/mBio.00966-18
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KEYWORDS

Vibrio
biochemistry
gene regulation
genome analysis

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