Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin

Darja Ivanova, Toni Taylor, Sarah L Smith, Juachi U Dimude, Amy L Upton, Mana M Mehrjouy, Ole Skovgaard, David J Sherratt, Renata Retkute, Christian J Rudolph

    Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

    Resumé

    Each cell division requires the unwinding of millions of DNA base pairs to allow chromosome duplication and gene transcription. As DNA replication and transcription share the same template, conflicts between both processes are unavoidable and head-on collisions are thought to be particularly problematic. Surprisingly, a recent study reported unperturbed cell cycle progression in Escherichia coli cells with an ectopic replication origin in which highly transcribed rrn operons were forced to be replicated opposite to normal. In this study we have re-generated a similar strain and found the doubling time to be twice that of normal cells. Replication profiles of this background revealed significant deviations in comparison to wild-type profiles, particularly in highly transcribed regions and the termination area. These deviations were alleviated bymutations that either inactivate the termination area or destabilise RNA polymerase complexes and allow their easier displacement by replication forks. Our data demonstrate that head-on replication-transcription conflicts are highly problematic. Indeed, analysis of the replication profile of the previously published E. coli construct revealed a chromosomal rearrangement that alleviates replication-transcription conflicts in an intriguingly simple way. Our data support the idea that avoiding head-on collisions has significantly contributed to shaping the distinct architecture of bacterial chromosomes.
    OriginalsprogEngelsk
    TidsskriftNucleic Acids Research
    Vol/bind43
    Udgave nummer16
    Sider (fra-til)7865-7877
    Antal sider13
    ISSN0305-1048
    DOI
    StatusUdgivet - 2015

    Citer dette

    Ivanova, D., Taylor, T., Smith, S. L., Dimude, J. U., Upton, A. L., Mehrjouy, M. M., ... Rudolph, C. J. (2015). Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin. Nucleic Acids Research, 43(16), 7865-7877. https://doi.org/10.1093/nar/gkv704
    Ivanova, Darja ; Taylor, Toni ; Smith, Sarah L ; Dimude, Juachi U ; Upton, Amy L ; Mehrjouy, Mana M ; Skovgaard, Ole ; Sherratt, David J ; Retkute, Renata ; Rudolph, Christian J. / Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin. I: Nucleic Acids Research. 2015 ; Bind 43, Nr. 16. s. 7865-7877.
    @article{87914a8dc16e4d21af79734d075166f9,
    title = "Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin",
    abstract = "Each cell division requires the unwinding of millions of DNA base pairs to allow chromosome duplication and gene transcription. As DNA replication and transcription share the same template, conflicts between both processes are unavoidable and head-on collisions are thought to be particularly problematic. Surprisingly, a recent study reported unperturbed cell cycle progression in Escherichia coli cells with an ectopic replication origin in which highly transcribed rrn operons were forced to be replicated opposite to normal. In this study we have re-generated a similar strain and found the doubling time to be twice that of normal cells. Replication profiles of this background revealed significant deviations in comparison to wild-type profiles, particularly in highly transcribed regions and the termination area. These deviations were alleviated by mutations that either inactivate the termination area or destabilise RNA polymerase complexes and allow their easier displacement by replication forks. Our data demonstrate that head-on replication-transcription conflicts are highly problematic. Indeed, analysis of the replication profile of the previously published E. coli construct revealed a chromosomal rearrangement that alleviates replication-transcription conflicts in an intriguingly simple way. Our data support the idea that avoiding head-on collisions has significantly contributed to shaping the distinct architecture of bacterial chromosomes",
    author = "Darja Ivanova and Toni Taylor and Smith, {Sarah L} and Dimude, {Juachi U} and Upton, {Amy L} and Mehrjouy, {Mana M} and Ole Skovgaard and Sherratt, {David J} and Renata Retkute and Rudolph, {Christian J}",
    year = "2015",
    doi = "10.1093/nar/gkv704",
    language = "English",
    volume = "43",
    pages = "7865--7877",
    journal = "Nucleic Acids Research",
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    Ivanova, D, Taylor, T, Smith, SL, Dimude, JU, Upton, AL, Mehrjouy, MM, Skovgaard, O, Sherratt, DJ, Retkute, R & Rudolph, CJ 2015, 'Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin', Nucleic Acids Research, bind 43, nr. 16, s. 7865-7877. https://doi.org/10.1093/nar/gkv704

    Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin. / Ivanova, Darja; Taylor, Toni; Smith, Sarah L; Dimude, Juachi U; Upton, Amy L; Mehrjouy, Mana M; Skovgaard, Ole; Sherratt, David J; Retkute, Renata; Rudolph, Christian J.

    I: Nucleic Acids Research, Bind 43, Nr. 16, 2015, s. 7865-7877.

    Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

    TY - JOUR

    T1 - Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin

    AU - Ivanova, Darja

    AU - Taylor, Toni

    AU - Smith, Sarah L

    AU - Dimude, Juachi U

    AU - Upton, Amy L

    AU - Mehrjouy, Mana M

    AU - Skovgaard, Ole

    AU - Sherratt, David J

    AU - Retkute, Renata

    AU - Rudolph, Christian J

    PY - 2015

    Y1 - 2015

    N2 - Each cell division requires the unwinding of millions of DNA base pairs to allow chromosome duplication and gene transcription. As DNA replication and transcription share the same template, conflicts between both processes are unavoidable and head-on collisions are thought to be particularly problematic. Surprisingly, a recent study reported unperturbed cell cycle progression in Escherichia coli cells with an ectopic replication origin in which highly transcribed rrn operons were forced to be replicated opposite to normal. In this study we have re-generated a similar strain and found the doubling time to be twice that of normal cells. Replication profiles of this background revealed significant deviations in comparison to wild-type profiles, particularly in highly transcribed regions and the termination area. These deviations were alleviated by mutations that either inactivate the termination area or destabilise RNA polymerase complexes and allow their easier displacement by replication forks. Our data demonstrate that head-on replication-transcription conflicts are highly problematic. Indeed, analysis of the replication profile of the previously published E. coli construct revealed a chromosomal rearrangement that alleviates replication-transcription conflicts in an intriguingly simple way. Our data support the idea that avoiding head-on collisions has significantly contributed to shaping the distinct architecture of bacterial chromosomes

    AB - Each cell division requires the unwinding of millions of DNA base pairs to allow chromosome duplication and gene transcription. As DNA replication and transcription share the same template, conflicts between both processes are unavoidable and head-on collisions are thought to be particularly problematic. Surprisingly, a recent study reported unperturbed cell cycle progression in Escherichia coli cells with an ectopic replication origin in which highly transcribed rrn operons were forced to be replicated opposite to normal. In this study we have re-generated a similar strain and found the doubling time to be twice that of normal cells. Replication profiles of this background revealed significant deviations in comparison to wild-type profiles, particularly in highly transcribed regions and the termination area. These deviations were alleviated by mutations that either inactivate the termination area or destabilise RNA polymerase complexes and allow their easier displacement by replication forks. Our data demonstrate that head-on replication-transcription conflicts are highly problematic. Indeed, analysis of the replication profile of the previously published E. coli construct revealed a chromosomal rearrangement that alleviates replication-transcription conflicts in an intriguingly simple way. Our data support the idea that avoiding head-on collisions has significantly contributed to shaping the distinct architecture of bacterial chromosomes

    U2 - 10.1093/nar/gkv704

    DO - 10.1093/nar/gkv704

    M3 - Journal article

    VL - 43

    SP - 7865

    EP - 7877

    JO - Nucleic Acids Research

    JF - Nucleic Acids Research

    SN - 0305-1048

    IS - 16

    ER -