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

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 d...

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প্রধান লেখক: Mugunthan, Sudarsan, Wong, Lan Li, Winnerdy, Fernaldo Richtia, Summers, Stephen, Muhammad Hafiz Bin Ismail, Foo, Yong Hwee, Jaggi, Tavleen Kaur, Meldrum, Oliver W., Tiew, Pei Yee, Chotirmall, Sanjay Haresh, Rice, Scott A., Phan, Anh Tuân, Kjelleberg, Staffan, Seviour, Thomas
অন্যান্য লেখক: Lee Kong Chian School of Medicine (LKCMedicine)
বিন্যাস: Journal Article
ভাষা:English
প্রকাশিত: 2024
বিষয়গুলি:
অনলাইন ব্যবহার করুন:https://hdl.handle.net/10356/172993
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author Mugunthan, Sudarsan
Wong, Lan Li
Winnerdy, Fernaldo Richtia
Summers, Stephen
Muhammad Hafiz Bin Ismail
Foo, Yong Hwee
Jaggi, Tavleen Kaur
Meldrum, Oliver W.
Tiew, Pei Yee
Chotirmall, Sanjay Haresh
Rice, Scott A.
Phan, Anh Tuân
Kjelleberg, Staffan
Seviour, Thomas
author2 Lee Kong Chian School of Medicine (LKCMedicine)
author_facet Lee Kong Chian School of Medicine (LKCMedicine)
Mugunthan, Sudarsan
Wong, Lan Li
Winnerdy, Fernaldo Richtia
Summers, Stephen
Muhammad Hafiz Bin Ismail
Foo, Yong Hwee
Jaggi, Tavleen Kaur
Meldrum, Oliver W.
Tiew, Pei Yee
Chotirmall, Sanjay Haresh
Rice, Scott A.
Phan, Anh Tuân
Kjelleberg, Staffan
Seviour, Thomas
author_sort Mugunthan, Sudarsan
collection NTU
description 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.
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spelling ntu-10356/1729932024-01-14T15:38:38Z RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms Mugunthan, Sudarsan Wong, Lan Li Winnerdy, Fernaldo Richtia Summers, Stephen Muhammad Hafiz Bin Ismail Foo, Yong Hwee Jaggi, Tavleen Kaur Meldrum, Oliver W. Tiew, Pei Yee Chotirmall, Sanjay Haresh Rice, Scott A. Phan, Anh Tuân Kjelleberg, Staffan Seviour, Thomas Lee Kong Chian School of Medicine (LKCMedicine) School of Physical and Mathematical Sciences School of Biological Sciences St John’s Island National Marine Laboratory Tan Tock Seng Hospital Singapore Centre for Environmental Life Sciences and Engineering (SCELSE) Institute for Digital Molecular Analytics and Science (IDMxS) Science::Biological sciences Pseudomonas Aeruginosa Biofilm 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. Ministry of Education (MOE) Nanyang Technological University National Research Foundation (NRF) Published version The Singapore Centre for Environmental Life Sciences Engineering (SCELSE) is funded by the Ministry of Education, Singapore, the National Research Foundation of Singapore, Nanyang Technological University Singapore (NTU) and National University of Singapore (NUS), and hosted by NTU in partnership with NUS (S.K.). 2024-01-08T05:12:36Z 2024-01-08T05:12:36Z 2023 Journal Article Mugunthan, S., Wong, L. L., Winnerdy, F. R., Summers, S., Muhammad Hafiz Bin Ismail, Foo, Y. H., Jaggi, T. K., Meldrum, O. W., Tiew, P. Y., Chotirmall, S. H., Rice, S. A., Phan, A. T., Kjelleberg, S. & Seviour, T. (2023). RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms. Nature Communications, 14(1), 7772-. https://dx.doi.org/10.1038/s41467-023-43533-3 2041-1723 https://hdl.handle.net/10356/172993 10.1038/s41467-023-43533-3 38012164 2-s2.0-85177888820 1 14 7772 en Nature Communications © 2023 The Author(s). Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/ licenses/by/4.0/. application/pdf
spellingShingle Science::Biological sciences
Pseudomonas Aeruginosa
Biofilm
Mugunthan, Sudarsan
Wong, Lan Li
Winnerdy, Fernaldo Richtia
Summers, Stephen
Muhammad Hafiz Bin Ismail
Foo, Yong Hwee
Jaggi, Tavleen Kaur
Meldrum, Oliver W.
Tiew, Pei Yee
Chotirmall, Sanjay Haresh
Rice, Scott A.
Phan, Anh Tuân
Kjelleberg, Staffan
Seviour, Thomas
RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title_full RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title_fullStr RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title_full_unstemmed RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title_short RNA is a key component of extracellular DNA networks in Pseudomonas aeruginosa biofilms
title_sort rna is a key component of extracellular dna networks in pseudomonas aeruginosa biofilms
topic Science::Biological sciences
Pseudomonas Aeruginosa
Biofilm
url https://hdl.handle.net/10356/172993
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