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

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, Scott A. Rice, Anh Tuân Phan, Staffan Kjelleberg () and Thomas Seviour ()
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Sudarsan Mugunthan: Nanyang Technological University
Lan Li Wong: Nanyang Technological University
Fernaldo Richtia Winnerdy: University of California
Stephen Summers: Nanyang Technological University
Muhammad Hafiz Ismail: Environmental Health Institute, National Environmental Agency
Yong Hwee Foo: 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
Scott A. Rice: Nanyang Technological University
Anh Tuân Phan: Nanyang Technological University
Staffan Kjelleberg: Nanyang Technological University
Thomas Seviour: Nanyang Technological University

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43533-3

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