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RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms

Author

Listed:
  • Sudarsan Mugunthan

    (Nanyang Technological University)

  • Lan Li Wong

    (Nanyang Technological University)

  • Fernaldo Richtia Winnerdy

    (University of California)

  • Stephen Summers

    (Nanyang Technological University
    National University of Singapore)

  • Muhammad Hafiz Ismail

    (Environmental Health Institute, National Environmental Agency)

  • Yong Hwee Foo

    (Nanyang Technological University
    Nanyang Technological University)

  • Tavleen Kaur Jaggi

    (Nanyang Technological University)

  • Oliver W. Meldrum

    (Nanyang Technological University)

  • Pei Yee Tiew

    (Singapore General Hospital)

  • Sanjay H. Chotirmall

    (Nanyang Technological University
    Tan Tock Seng Hospital)

  • Scott A. Rice

    (Nanyang Technological University
    University of Technology Sydney
    CSIRO, Agriculture and Food, Westmead and Microbiomes for One Systems Health)

  • Anh Tuân Phan

    (Nanyang Technological University)

  • Staffan Kjelleberg

    (Nanyang Technological University
    Nanyang Technological University
    University of New South Wales)

  • Thomas Seviour

    (Nanyang Technological University
    Aarhus University)

Abstract

The extracellular matrix of bacterial biofilms consists of diverse components including polysaccharides, proteins and DNA. Extracellular RNA (eRNA) can also be present, contributing to the structural integrity of biofilms. However, technical difficulties related to the low stability of RNA make it difficult to understand the precise roles of eRNA in biofilms. Here, we show that eRNA associates with extracellular DNA (eDNA) to form matrix fibres in Pseudomonas aeruginosa biofilms, and the eRNA is enriched in certain bacterial RNA transcripts. Degradation of eRNA associated with eDNA led to a loss of eDNA fibres and biofilm viscoelasticity. Compared with planktonic and biofilm cells, the biofilm matrix was enriched in specific mRNA transcripts, including lasB (encoding elastase). The mRNA transcripts colocalised with eDNA fibres in the biofilm matrix, as shown by single molecule inexpensive FISH microscopy (smiFISH). The lasB mRNA was also observed in eDNA fibres in a clinical sputum sample positive for P. aeruginosa. Thus, our results indicate that the interaction of specific mRNAs with eDNA facilitates the formation of viscoelastic networks in the matrix of Pseudomonas aeruginosa biofilms.

Suggested Citation

  • Sudarsan Mugunthan & Lan Li Wong & Fernaldo Richtia Winnerdy & Stephen Summers & Muhammad Hafiz Ismail & Yong Hwee Foo & Tavleen Kaur Jaggi & Oliver W. Meldrum & Pei Yee Tiew & Sanjay H. Chotirmall & , 2023. "RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43533-3
    DOI: 10.1038/s41467-023-43533-3
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    References listed on IDEAS

    as
    1. Ankur Jain & Ronald D. Vale, 2017. "RNA phase transitions in repeat expansion disorders," Nature, Nature, vol. 546(7657), pages 243-247, June.
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