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Dual RNA-seq unveils noncoding RNA functions in host–pathogen interactions

Author

Listed:
  • Alexander J. Westermann

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology)

  • Konrad U. Förstner

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology
    University of Würzburg, Core Unit Systems Medicine)

  • Fabian Amman

    (University of Leipzig
    University of Vienna, Theoretical Biochemistry Group, Institute for Theoretical Chemistry)

  • Lars Barquist

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology)

  • Yanjie Chao

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology)

  • Leon N. Schulte

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology)

  • Lydia Müller

    (University of Leipzig)

  • Richard Reinhardt

    (Max Planck Genome Centre Cologne, Max Planck Institute for Plant Breeding Research)

  • Peter F. Stadler

    (University of Leipzig
    University of Vienna, Theoretical Biochemistry Group, Institute for Theoretical Chemistry
    Max Planck Institute for Mathematics in the Sciences
    Santa Fe Institute)

  • Jörg Vogel

    (University of Würzburg, RNA Biology Group, Institute for Molecular Infection Biology
    Research Centre for Infectious Diseases (ZINF), University of Würzburg)

Abstract

Bacteria express many small RNAs for which the regulatory roles in pathogenesis have remained poorly understood due to a paucity of robust phenotypes in standard virulence assays. Here we use a generic ‘dual RNA-seq’ approach to profile RNA expression simultaneously in pathogen and host during Salmonella enterica serovar Typhimurium infection and reveal the molecular impact of bacterial riboregulators. We identify a PhoP-activated small RNA, PinT, which upon bacterial internalization temporally controls the expression of both invasion-associated effectors and virulence genes required for intracellular survival. This riboregulatory activity causes pervasive changes in coding and noncoding transcripts of the host. Interspecies correlation analysis links PinT to host cell JAK–STAT signalling, and we identify infection-specific alterations in multiple long noncoding RNAs. Our study provides a paradigm for a sensitive RNA-based analysis of intracellular bacterial pathogens and their hosts without physical separation, as well as a new discovery route for hidden functions of pathogen genes.

Suggested Citation

  • Alexander J. Westermann & Konrad U. Förstner & Fabian Amman & Lars Barquist & Yanjie Chao & Leon N. Schulte & Lydia Müller & Richard Reinhardt & Peter F. Stadler & Jörg Vogel, 2016. "Dual RNA-seq unveils noncoding RNA functions in host–pathogen interactions," Nature, Nature, vol. 529(7587), pages 496-501, January.
    • Handle: RePEc:nat:nature:v:529:y:2016:i:7587:d:10.1038_nature16547
    DOI: 10.1038/nature16547
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    Cited by:

    1. Kejing Wu & Xingyu Lin & Yujie Lu & Rui Dong & Hongnian Jiang & Sarah L. Svensson & Jiajia Zheng & Ning Shen & Andrew Camilli & Yanjie Chao, 2024. "RNA interactome of hypervirulent Klebsiella pneumoniae reveals a small RNA inhibitor of capsular mucoviscosity and virulence," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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