The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures
Abstract Extracellular DNA, or eDNA, is recognised as a critical biofilm component; however, it is not understood how it forms networked matrix structures. Here, we isolate eDNA from static-culture Pseudomonas aeruginosa biofilms using ionic liquids to preserve its biophysical signatures of fluid vi...
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2021
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oai:doaj.org-article:70e8aa33fa1741feb38ae9235c2d94022021-12-02T13:18:03ZThe biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures10.1038/s41522-021-00197-52055-5008https://doaj.org/article/70e8aa33fa1741feb38ae9235c2d94022021-03-01T00:00:00Zhttps://doi.org/10.1038/s41522-021-00197-5https://doaj.org/toc/2055-5008Abstract Extracellular DNA, or eDNA, is recognised as a critical biofilm component; however, it is not understood how it forms networked matrix structures. Here, we isolate eDNA from static-culture Pseudomonas aeruginosa biofilms using ionic liquids to preserve its biophysical signatures of fluid viscoelasticity and the temperature dependency of DNA transitions. We describe a loss of eDNA network structure as resulting from a change in nucleic acid conformation, and propose that its ability to form viscoelastic structures is key to its role in building biofilm matrices. Solid-state analysis of isolated eDNA, as a proxy for eDNA structure in biofilms, reveals non-canonical Hoogsteen base pairs, triads or tetrads involving thymine or uracil, and guanine, suggesting that the eDNA forms G-quadruplex structures. These are less abundant in chromosomal DNA and disappear when eDNA undergoes conformation transition. We verify the occurrence of G-quadruplex structures in the extracellular matrix of intact static and flow-cell biofilms of P. aeruginosa, as displayed by the matrix to G-quadruplex-specific antibody binding, and validate the loss of G-quadruplex structures in vivo to occur coincident with the disappearance of eDNA fibres. Given their stability, understanding how extracellular G-quadruplex structures form will elucidate how P. aeruginosa eDNA builds viscoelastic networks, which are a foundational biofilm property.Thomas SeviourFernaldo Richtia WinnerdyLan Li WongXiangyan ShiSudarsan MugunthanYong Hwee FooRemi CastaingSunil S. AdavSujatha SubramoniGurjeet Singh KohliHeather M. ShewanJason R. StokesScott A. RiceAnh Tuân PhanStaffan KjellebergNature PortfolioarticleMicrobial ecologyQR100-130ENnpj Biofilms and Microbiomes, Vol 7, Iss 1, Pp 1-12 (2021) |
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Microbial ecology QR100-130 |
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Microbial ecology QR100-130 Thomas Seviour Fernaldo Richtia Winnerdy Lan Li Wong Xiangyan Shi Sudarsan Mugunthan Yong Hwee Foo Remi Castaing Sunil S. Adav Sujatha Subramoni Gurjeet Singh Kohli Heather M. Shewan Jason R. Stokes Scott A. Rice Anh Tuân Phan Staffan Kjelleberg The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
description |
Abstract Extracellular DNA, or eDNA, is recognised as a critical biofilm component; however, it is not understood how it forms networked matrix structures. Here, we isolate eDNA from static-culture Pseudomonas aeruginosa biofilms using ionic liquids to preserve its biophysical signatures of fluid viscoelasticity and the temperature dependency of DNA transitions. We describe a loss of eDNA network structure as resulting from a change in nucleic acid conformation, and propose that its ability to form viscoelastic structures is key to its role in building biofilm matrices. Solid-state analysis of isolated eDNA, as a proxy for eDNA structure in biofilms, reveals non-canonical Hoogsteen base pairs, triads or tetrads involving thymine or uracil, and guanine, suggesting that the eDNA forms G-quadruplex structures. These are less abundant in chromosomal DNA and disappear when eDNA undergoes conformation transition. We verify the occurrence of G-quadruplex structures in the extracellular matrix of intact static and flow-cell biofilms of P. aeruginosa, as displayed by the matrix to G-quadruplex-specific antibody binding, and validate the loss of G-quadruplex structures in vivo to occur coincident with the disappearance of eDNA fibres. Given their stability, understanding how extracellular G-quadruplex structures form will elucidate how P. aeruginosa eDNA builds viscoelastic networks, which are a foundational biofilm property. |
format |
article |
author |
Thomas Seviour Fernaldo Richtia Winnerdy Lan Li Wong Xiangyan Shi Sudarsan Mugunthan Yong Hwee Foo Remi Castaing Sunil S. Adav Sujatha Subramoni Gurjeet Singh Kohli Heather M. Shewan Jason R. Stokes Scott A. Rice Anh Tuân Phan Staffan Kjelleberg |
author_facet |
Thomas Seviour Fernaldo Richtia Winnerdy Lan Li Wong Xiangyan Shi Sudarsan Mugunthan Yong Hwee Foo Remi Castaing Sunil S. Adav Sujatha Subramoni Gurjeet Singh Kohli Heather M. Shewan Jason R. Stokes Scott A. Rice Anh Tuân Phan Staffan Kjelleberg |
author_sort |
Thomas Seviour |
title |
The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
title_short |
The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
title_full |
The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
title_fullStr |
The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
title_full_unstemmed |
The biofilm matrix scaffold of Ps eudomonas aeruginosa contains G-quadruplex extracellular DNA structures |
title_sort |
biofilm matrix scaffold of ps eudomonas aeruginosa contains g-quadruplex extracellular dna structures |
publisher |
Nature Portfolio |
publishDate |
2021 |
url |
https://doaj.org/article/70e8aa33fa1741feb38ae9235c2d9402 |
work_keys_str_mv |
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