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Xenogeneic silencing strategies in bacteria are dictated by RNA polymerase promiscuity

Author

Listed:
  • David Forrest

    (University of Birmingham)

  • Emily A. Warman

    (University of Birmingham)

  • Amanda M. Erkelens

    (Leiden University)

  • Remus T. Dame

    (Leiden University
    Leiden University)

  • David C. Grainger

    (University of Birmingham)

Abstract

Horizontal gene transfer facilitates dissemination of favourable traits among bacteria. However, foreign DNA can also reduce host fitness: incoming sequences with a higher AT content than the host genome can misdirect transcription. Xenogeneic silencing proteins counteract this by modulating RNA polymerase binding. In this work, we compare xenogeneic silencing strategies of two distantly related model organisms: Escherichia coli and Bacillus subtilis. In E. coli, silencing is mediated by the H-NS protein that binds extensively across horizontally acquired genes. This prevents spurious non-coding transcription, mostly intragenic in origin. By contrast, binding of the B. subtilis Rok protein is more targeted and mostly silences expression of functional mRNAs. The difference reflects contrasting transcriptional promiscuity in E. coli and B. subtilis, largely attributable to housekeeping RNA polymerase σ factors. Thus, whilst RNA polymerase specificity is key to the xenogeneic silencing strategy of B. subtilis, transcriptional promiscuity must be overcome to silence horizontally acquired DNA in E. coli.

Suggested Citation

  • David Forrest & Emily A. Warman & Amanda M. Erkelens & Remus T. Dame & David C. Grainger, 2022. "Xenogeneic silencing strategies in bacteria are dictated by RNA polymerase promiscuity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28747-1
    DOI: 10.1038/s41467-022-28747-1
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    1. F. Kunst & N. Ogasawara & I. Moszer & A. M. Albertini & G. Alloni & V. Azevedo & M. G. Bertero & P. Bessières & A. Bolotin & S. Borchert & R. Borriss & L. Boursier & A. Brans & M. Braun & S. C. Brigne, 1997. "The complete genome sequence of the Gram-positive bacterium Bacillus subtilis," Nature, Nature, vol. 390(6657), pages 249-256, November.
    2. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    3. Stefan M. Gaida & Nicholas R. Sandoval & Sergios A. Nicolaou & Yili Chen & Keerthi P. Venkataramanan & Eleftherios T. Papoutsakis, 2015. "Expression of heterologous sigma factors enables functional screening of metagenomic and heterologous genomic libraries," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
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    Cited by:

    1. Nara Figueroa-Bossi & Rocío Fernández-Fernández & Patricia Kerboriou & Philippe Bouloc & Josep Casadesús & María Antonia Sánchez-Romero & Lionello Bossi, 2024. "Transcription-driven DNA supercoiling counteracts H-NS-mediated gene silencing in bacterial chromatin," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Fatema-Zahra M. Rashid & Frédéric G. E. Crémazy & Andreas Hofmann & David Forrest & David C. Grainger & Dieter W. Heermann & Remus T. Dame, 2023. "The environmentally-regulated interplay between local three-dimensional chromatin organisation and transcription of proVWX in E. coli," Nature Communications, Nature, vol. 14(1), pages 1-25, December.

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