The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms

Bacteria within biofilms secrete and surround themselves with an extracellular matrix, which serves as a first line of defense against antibiotic attack. Polysaccharides constitute major elements of the biofilm matrix and are implied in surface adhesion and biofilm organization, but their contributi...

Full description

Bibliographic Details
Main Authors: Ramirez Millan, Maria, Caldara, Marina, Rusconi, Roberto, Tarasova, Yekaterina, Stocker, Roman, Ribbeck, Katharina, Billings, Amanda Nicole
Other Authors: Massachusetts Institute of Technology. Department of Biological Engineering
Format: Article
Language:en_US
Published: Public Library of Science 2013
Online Access:http://hdl.handle.net/1721.1/81214
https://orcid.org/0000-0002-4593-5606
https://orcid.org/0000-0001-8260-338X
https://orcid.org/0000-0002-3199-0508
_version_ 1811096883897040896
author Ramirez Millan, Maria
Caldara, Marina
Rusconi, Roberto
Tarasova, Yekaterina
Stocker, Roman
Ribbeck, Katharina
Billings, Amanda Nicole
author2 Massachusetts Institute of Technology. Department of Biological Engineering
author_facet Massachusetts Institute of Technology. Department of Biological Engineering
Ramirez Millan, Maria
Caldara, Marina
Rusconi, Roberto
Tarasova, Yekaterina
Stocker, Roman
Ribbeck, Katharina
Billings, Amanda Nicole
author_sort Ramirez Millan, Maria
collection MIT
description Bacteria within biofilms secrete and surround themselves with an extracellular matrix, which serves as a first line of defense against antibiotic attack. Polysaccharides constitute major elements of the biofilm matrix and are implied in surface adhesion and biofilm organization, but their contributions to the resistance properties of biofilms remain largely elusive. Using a combination of static and continuous-flow biofilm experiments we show that Psl, one major polysaccharide in the Pseudomonas aeruginosa biofilm matrix, provides a generic first line of defense toward antibiotics with diverse biochemical properties during the initial stages of biofilm development. Furthermore, we show with mixed-strain experiments that antibiotic-sensitive “non-producing” cells lacking Psl can gain tolerance by integrating into Psl-containing biofilms. However, non-producers dilute the protective capacity of the matrix and hence, excessive incorporation can result in the collapse of resistance of the entire community. Our data also reveal that Psl mediated protection is extendible to E. coli and S. aureus in co-culture biofilms. Together, our study shows that Psl represents a critical first bottleneck to the antibiotic attack of a biofilm community early in biofilm development.
first_indexed 2024-09-23T16:50:53Z
format Article
id mit-1721.1/81214
institution Massachusetts Institute of Technology
language en_US
last_indexed 2024-09-23T16:50:53Z
publishDate 2013
publisher Public Library of Science
record_format dspace
spelling mit-1721.1/812142022-10-03T08:40:12Z The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms Ramirez Millan, Maria Caldara, Marina Rusconi, Roberto Tarasova, Yekaterina Stocker, Roman Ribbeck, Katharina Billings, Amanda Nicole Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Billings, Amanda Nicole Ramirez Millan, Maria Caldara, Marina Tarasova, Yekaterina Ribbeck, Katharina Rusconi, Roberto Stocker, Roman Bacteria within biofilms secrete and surround themselves with an extracellular matrix, which serves as a first line of defense against antibiotic attack. Polysaccharides constitute major elements of the biofilm matrix and are implied in surface adhesion and biofilm organization, but their contributions to the resistance properties of biofilms remain largely elusive. Using a combination of static and continuous-flow biofilm experiments we show that Psl, one major polysaccharide in the Pseudomonas aeruginosa biofilm matrix, provides a generic first line of defense toward antibiotics with diverse biochemical properties during the initial stages of biofilm development. Furthermore, we show with mixed-strain experiments that antibiotic-sensitive “non-producing” cells lacking Psl can gain tolerance by integrating into Psl-containing biofilms. However, non-producers dilute the protective capacity of the matrix and hence, excessive incorporation can result in the collapse of resistance of the entire community. Our data also reveal that Psl mediated protection is extendible to E. coli and S. aureus in co-culture biofilms. Together, our study shows that Psl represents a critical first bottleneck to the antibiotic attack of a biofilm community early in biofilm development. National Institutes of Health (U.S.). National Institute of Environmental Health Sciences (Training Grant in Toxicology 5 T32 ES7020-37) 2013-09-27T15:11:05Z 2013-09-27T15:11:05Z 2013-08 2012-11 Article http://purl.org/eprint/type/JournalArticle 1553-7374 1553-7366 http://hdl.handle.net/1721.1/81214 Billings, Nicole, Maria Ramirez Millan, Marina Caldara, Roberto Rusconi, Yekaterina Tarasova, Roman Stocker, and Katharina Ribbeck. “The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms.” Edited by Matthew R. Parsek. PLoS Pathogens 9, no. 8 (August 8, 2013): e1003526. https://orcid.org/0000-0002-4593-5606 https://orcid.org/0000-0001-8260-338X https://orcid.org/0000-0002-3199-0508 en_US http://dx.doi.org/10.1371/journal.ppat.1003526 PLoS Pathogens Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS
spellingShingle Ramirez Millan, Maria
Caldara, Marina
Rusconi, Roberto
Tarasova, Yekaterina
Stocker, Roman
Ribbeck, Katharina
Billings, Amanda Nicole
The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title_full The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title_fullStr The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title_full_unstemmed The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title_short The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms
title_sort extracellular matrix component psl provides fast acting antibiotic defense in pseudomonas aeruginosa biofilms
url http://hdl.handle.net/1721.1/81214
https://orcid.org/0000-0002-4593-5606
https://orcid.org/0000-0001-8260-338X
https://orcid.org/0000-0002-3199-0508
work_keys_str_mv AT ramirezmillanmaria theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT caldaramarina theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT rusconiroberto theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT tarasovayekaterina theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT stockerroman theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT ribbeckkatharina theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT billingsamandanicole theextracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT ramirezmillanmaria extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT caldaramarina extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT rusconiroberto extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT tarasovayekaterina extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT stockerroman extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT ribbeckkatharina extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms
AT billingsamandanicole extracellularmatrixcomponentpslprovidesfastactingantibioticdefenseinpseudomonasaeruginosabiofilms