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Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides

Lydia Powell Orcid Logo, Lydia C. Powell, Manon F. Pritchard, Elaine L. Ferguson, Kate A. Powell, Shree U. Patel, Phil D. Rye, Stavroula-Melina Sakellakou, Niklaas J. Buurma, Charles D. Brilliant, Jack M. Copping, Georgina E. Menzies, Paul Lewis, Katja E. Hill, David W. Thomas

npj Biofilms and Microbiomes, Volume: 4, Issue: 1

Swansea University Authors: Lydia Powell Orcid Logo, Paul Lewis

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DOI (Published version): 10.1038/s41522-018-0056-3

Abstract

Acquisition of a mucoid phenotype by Pseudomonas sp. in the lungs of cystic fibrosis (CF) patients, with subsequent over-production of extracellular polymeric substance (EPS), plays an important role in mediating the persistence of multi-drug resistant (MDR) infections. The ability of a low molecula...

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Published in: npj Biofilms and Microbiomes
ISSN: 2055-5008
Published: 2018
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URI: https://cronfa.swan.ac.uk/Record/cronfa40672
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fullrecord <?xml version="1.0"?><rfc1807><datestamp>2020-07-09T15:31:07.1250038</datestamp><bib-version>v2</bib-version><id>40672</id><entry>2018-06-07</entry><title>Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides</title><swanseaauthors><author><sid>0e7e702952672bcbfdfd4974199202fb</sid><ORCID>0000-0002-8641-0160</ORCID><firstname>Lydia</firstname><surname>Powell</surname><name>Lydia Powell</name><active>true</active><ethesisStudent>false</ethesisStudent></author><author><sid>46dfc22d7468f247c390ba0c6cd8fba6</sid><firstname>Paul</firstname><surname>Lewis</surname><name>Paul Lewis</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2018-06-07</date><deptcode>BMS</deptcode><abstract>Acquisition of a mucoid phenotype by Pseudomonas sp. in the lungs of cystic fibrosis (CF) patients, with subsequent over-production of extracellular polymeric substance (EPS), plays an important role in mediating the persistence of multi-drug resistant (MDR) infections. The ability of a low molecular weight (Mn=3200 g mol-1) alginate oligomer (OligoG CF-5/20) to modify biofilm structure of mucoid Pseudomonas aeruginosa (NH57388A) was studied in vitro using scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM) with Texas Red (TxRd&#xAE;)-labelled OligoG and EPS histochemical staining. Structural changes in treated biofilms were quantified using COMSTAT image-analysis software of CLSM z-stack images, and nanoparticle diffusion. Interactions between the oligomers, Ca2+ and DNA were studied using molecular dynamics simulations (MDS), Fourier transform infrared spectroscopy (FTIR) and isothermal titration calorimetry (ITC). Imaging demonstrated that OligoG treatment (&amp;#62;0.5%) inhibited biofilm formation, demonstrating a significant reduction in both biomass and biofilm height (17.8 vs. 5.5 &#xB5;m; P &amp;#60;0.05). TxRd&#xAE;-labelled oligomers readily diffused into established (24 h) biofilms. OligoG treatment (&#x2265;2%) induced alterations in the EPS of established biofilms; significantly reducing the structural quantities of sugar residues, and extracellular (e)DNA (P &amp;#60;0.05) with a corresponding increase in nanoparticle diffusion (P&amp;#60;0.05) and antibiotic efficacy against established biofilms. ITC demonstrated an absence of rapid complex formation between DNA and OligoG and confirmed the interactions of OligoG with Ca2+ evident in FTIR and MDS. The ability of OligoG to diffuse into biofilms, potentiate antibiotic activity, disrupt DNA-Ca2+-DNA bridges and biofilm EPS matrix highlights its potential for the treatment of biofilm-related infections.</abstract><type>Journal Article</type><journal>npj Biofilms and Microbiomes</journal><volume>4</volume><journalNumber>1</journalNumber><publisher/><issnElectronic>2055-5008</issnElectronic><keywords/><publishedDay>29</publishedDay><publishedMonth>6</publishedMonth><publishedYear>2018</publishedYear><publishedDate>2018-06-29</publishedDate><doi>10.1038/s41522-018-0056-3</doi><url>http://orca.cf.ac.uk/110780/</url><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2020-07-09T15:31:07.1250038</lastEdited><Created>2018-06-07T13:30:58.1693335</Created><authors><author><firstname>Lydia</firstname><surname>Powell</surname><orcid>0000-0002-8641-0160</orcid><order>1</order></author><author><firstname>Lydia C.</firstname><surname>Powell</surname><order>2</order></author><author><firstname>Manon F.</firstname><surname>Pritchard</surname><order>3</order></author><author><firstname>Elaine L.</firstname><surname>Ferguson</surname><order>4</order></author><author><firstname>Kate A.</firstname><surname>Powell</surname><order>5</order></author><author><firstname>Shree U.</firstname><surname>Patel</surname><order>6</order></author><author><firstname>Phil D.</firstname><surname>Rye</surname><order>7</order></author><author><firstname>Stavroula-Melina</firstname><surname>Sakellakou</surname><order>8</order></author><author><firstname>Niklaas J.</firstname><surname>Buurma</surname><order>9</order></author><author><firstname>Charles D.</firstname><surname>Brilliant</surname><order>10</order></author><author><firstname>Jack M.</firstname><surname>Copping</surname><order>11</order></author><author><firstname>Georgina E.</firstname><surname>Menzies</surname><order>12</order></author><author><firstname>Paul</firstname><surname>Lewis</surname><order>13</order></author><author><firstname>Katja E.</firstname><surname>Hill</surname><order>14</order></author><author><firstname>David W.</firstname><surname>Thomas</surname><order>15</order></author></authors><documents><document><filename>0040672-03082018152108.pdf</filename><originalFilename>40672.pdf</originalFilename><uploaded>2018-08-03T15:21:08.6300000</uploaded><type>Output</type><contentLength>3439659</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><embargoDate>2018-08-03T00:00:00.0000000</embargoDate><documentNotes>This article is licensed under a Creative Commons Attribution 4.0 International License.</documentNotes><copyrightCorrect>true</copyrightCorrect><language>eng</language></document></documents><OutputDurs/></rfc1807>
spelling 2020-07-09T15:31:07.1250038 v2 40672 2018-06-07 Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides 0e7e702952672bcbfdfd4974199202fb 0000-0002-8641-0160 Lydia Powell Lydia Powell true false 46dfc22d7468f247c390ba0c6cd8fba6 Paul Lewis Paul Lewis true false 2018-06-07 BMS Acquisition of a mucoid phenotype by Pseudomonas sp. in the lungs of cystic fibrosis (CF) patients, with subsequent over-production of extracellular polymeric substance (EPS), plays an important role in mediating the persistence of multi-drug resistant (MDR) infections. The ability of a low molecular weight (Mn=3200 g mol-1) alginate oligomer (OligoG CF-5/20) to modify biofilm structure of mucoid Pseudomonas aeruginosa (NH57388A) was studied in vitro using scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM) with Texas Red (TxRd®)-labelled OligoG and EPS histochemical staining. Structural changes in treated biofilms were quantified using COMSTAT image-analysis software of CLSM z-stack images, and nanoparticle diffusion. Interactions between the oligomers, Ca2+ and DNA were studied using molecular dynamics simulations (MDS), Fourier transform infrared spectroscopy (FTIR) and isothermal titration calorimetry (ITC). Imaging demonstrated that OligoG treatment (&#62;0.5%) inhibited biofilm formation, demonstrating a significant reduction in both biomass and biofilm height (17.8 vs. 5.5 µm; P &#60;0.05). TxRd®-labelled oligomers readily diffused into established (24 h) biofilms. OligoG treatment (≥2%) induced alterations in the EPS of established biofilms; significantly reducing the structural quantities of sugar residues, and extracellular (e)DNA (P &#60;0.05) with a corresponding increase in nanoparticle diffusion (P&#60;0.05) and antibiotic efficacy against established biofilms. ITC demonstrated an absence of rapid complex formation between DNA and OligoG and confirmed the interactions of OligoG with Ca2+ evident in FTIR and MDS. The ability of OligoG to diffuse into biofilms, potentiate antibiotic activity, disrupt DNA-Ca2+-DNA bridges and biofilm EPS matrix highlights its potential for the treatment of biofilm-related infections. Journal Article npj Biofilms and Microbiomes 4 1 2055-5008 29 6 2018 2018-06-29 10.1038/s41522-018-0056-3 http://orca.cf.ac.uk/110780/ COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University 2020-07-09T15:31:07.1250038 2018-06-07T13:30:58.1693335 Lydia Powell 0000-0002-8641-0160 1 Lydia C. Powell 2 Manon F. Pritchard 3 Elaine L. Ferguson 4 Kate A. Powell 5 Shree U. Patel 6 Phil D. Rye 7 Stavroula-Melina Sakellakou 8 Niklaas J. Buurma 9 Charles D. Brilliant 10 Jack M. Copping 11 Georgina E. Menzies 12 Paul Lewis 13 Katja E. Hill 14 David W. Thomas 15 0040672-03082018152108.pdf 40672.pdf 2018-08-03T15:21:08.6300000 Output 3439659 application/pdf Version of Record true 2018-08-03T00:00:00.0000000 This article is licensed under a Creative Commons Attribution 4.0 International License. true eng
title Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
spellingShingle Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
Lydia Powell
Paul Lewis
title_short Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
title_full Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
title_fullStr Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
title_full_unstemmed Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
title_sort Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides
author_id_str_mv 0e7e702952672bcbfdfd4974199202fb
46dfc22d7468f247c390ba0c6cd8fba6
author_id_fullname_str_mv 0e7e702952672bcbfdfd4974199202fb_***_Lydia Powell
46dfc22d7468f247c390ba0c6cd8fba6_***_Paul Lewis
author Lydia Powell
Paul Lewis
author2 Lydia Powell
Lydia C. Powell
Manon F. Pritchard
Elaine L. Ferguson
Kate A. Powell
Shree U. Patel
Phil D. Rye
Stavroula-Melina Sakellakou
Niklaas J. Buurma
Charles D. Brilliant
Jack M. Copping
Georgina E. Menzies
Paul Lewis
Katja E. Hill
David W. Thomas
format Journal article
container_title npj Biofilms and Microbiomes
container_volume 4
container_issue 1
publishDate 2018
institution Swansea University
issn 2055-5008
doi_str_mv 10.1038/s41522-018-0056-3
url http://orca.cf.ac.uk/110780/
document_store_str 1
active_str 0
description Acquisition of a mucoid phenotype by Pseudomonas sp. in the lungs of cystic fibrosis (CF) patients, with subsequent over-production of extracellular polymeric substance (EPS), plays an important role in mediating the persistence of multi-drug resistant (MDR) infections. The ability of a low molecular weight (Mn=3200 g mol-1) alginate oligomer (OligoG CF-5/20) to modify biofilm structure of mucoid Pseudomonas aeruginosa (NH57388A) was studied in vitro using scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM) with Texas Red (TxRd®)-labelled OligoG and EPS histochemical staining. Structural changes in treated biofilms were quantified using COMSTAT image-analysis software of CLSM z-stack images, and nanoparticle diffusion. Interactions between the oligomers, Ca2+ and DNA were studied using molecular dynamics simulations (MDS), Fourier transform infrared spectroscopy (FTIR) and isothermal titration calorimetry (ITC). Imaging demonstrated that OligoG treatment (&#62;0.5%) inhibited biofilm formation, demonstrating a significant reduction in both biomass and biofilm height (17.8 vs. 5.5 µm; P &#60;0.05). TxRd®-labelled oligomers readily diffused into established (24 h) biofilms. OligoG treatment (≥2%) induced alterations in the EPS of established biofilms; significantly reducing the structural quantities of sugar residues, and extracellular (e)DNA (P &#60;0.05) with a corresponding increase in nanoparticle diffusion (P&#60;0.05) and antibiotic efficacy against established biofilms. ITC demonstrated an absence of rapid complex formation between DNA and OligoG and confirmed the interactions of OligoG with Ca2+ evident in FTIR and MDS. The ability of OligoG to diffuse into biofilms, potentiate antibiotic activity, disrupt DNA-Ca2+-DNA bridges and biofilm EPS matrix highlights its potential for the treatment of biofilm-related infections.
published_date 2018-06-29T03:51:46Z
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