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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Autores principales: 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
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Publicado: Nature Portfolio 2021
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Acceso en línea:https://doaj.org/article/70e8aa33fa1741feb38ae9235c2d9402
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spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Microbial ecology
QR100-130
spellingShingle 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
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