The structural role of bacterial eDNA in the formation of biofilm streamers.

Pseudomonas aeruginosa bacterial biofilms biofilm rheology extracellular DNA fluid flow

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
22 03 2022
Historique:
entrez: 15 3 2022
pubmed: 16 3 2022
medline: 21 4 2022
Statut: ppublish

Résumé

Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhance bacterial recalcitrance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric constraints such as corners or constrictions, biofilms can take the form of long, suspended filaments (streamers), which bear important consequences in industrial and clinical settings by causing clogging and fouling. The formation of streamers is thought to be driven by the viscoelastic nature of the biofilm matrix. Yet, little is known about the structural composition of streamers and how it affects their mechanical properties. Here, using a microfluidic platform that allows growing and precisely examining biofilm streamers, we show that extracellular DNA (eDNA) constitutes the backbone and is essential for the mechanical stability of Pseudomonas aeruginosa streamers. This finding is supported by the observations that DNA-degrading enzymes prevent the formation of streamers and clear already formed ones and that the antibiotic ciprofloxacin promotes their formation by increasing the release of eDNA. Furthermore, using mutants for the production of the exopolysaccharide Pel, an important component of P. aeruginosa EPS, we reveal an concurring role of Pel in tuning the mechanical properties of the streamers. Taken together, these results highlight the importance of eDNA and of its interplay with Pel in determining the mechanical properties of P. aeruginosa streamers and suggest that targeting the composition of streamers can be an effective approach to control the formation of these biofilm structures.

Identifiants

pubmed: 35290120
doi: 10.1073/pnas.2113723119
pmc: PMC8944759
doi:

Substances chimiques

DNA, Bacterial 0
Polysaccharides, Bacterial 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2113723119

Références

ISME J. 2019 Jul;13(7):1700-1710
pubmed: 30833685
Clin Microbiol Rev. 2022 Jan 19;:e0022120
pubmed: 35044203
NPJ Biofilms Microbiomes. 2021 Mar 19;7(1):27
pubmed: 33741996
J R Soc Interface. 2010 Sep 6;7(50):1293-9
pubmed: 20356880
Antimicrob Agents Chemother. 2005 Aug;49(8):3222-7
pubmed: 16048929
Nat Rev Microbiol. 2008 Mar;6(3):199-210
pubmed: 18264116
Biofilm. 2019 Dec 19;2:100017
pubmed: 33447803
J Colloid Interface Sci. 2021 Jul 15;594:265-278
pubmed: 33765646
FEMS Microbiol Rev. 2012 Jul;36(4):893-916
pubmed: 22212072
mBio. 2014 Aug 05;5(4):e01536-14
pubmed: 25096883
FEMS Microbiol Ecol. 2013 Dec;86(3):394-403
pubmed: 23786537
mBio. 2018 Sep 25;9(5):
pubmed: 30254118
J Bacteriol. 2015 Dec;197(24):3779-87
pubmed: 26416831
Microbiology (Reading). 2007 Jul;153(Pt 7):2083-2092
pubmed: 17600053
Proc Natl Acad Sci U S A. 2019 Dec 10;116(50):25068-25077
pubmed: 31767757
J Bacteriol. 2020 Sep 8;202(19):
pubmed: 32661078
Water Res. 2018 Apr 1;132:211-221
pubmed: 29331909
PLoS Pathog. 2008 Nov;4(11):e1000213
pubmed: 19023416
Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7907-12
pubmed: 12810959
PLoS One. 2013 Jun 14;8(6):e67629
pubmed: 23799151
Nat Commun. 2020 Jun 5;11(1):2851
pubmed: 32503979
Front Microbiol. 2017 Jul 26;8:1390
pubmed: 28798731
Soft Matter. 2017 Nov 29;13(46):8698-8705
pubmed: 28960016
Antimicrob Agents Chemother. 2013 May;57(5):2352-61
pubmed: 23478967
BMC Microbiol. 2020 May 14;20(1):115
pubmed: 32410574
Cell Rep. 2021 Feb 23;34(8):108782
pubmed: 33626358
Environ Microbiol. 2014 Jul;16(7):1961-81
pubmed: 24592823
Front Microbiol. 2011 Aug 22;2:167
pubmed: 21991261
J Bacteriol. 2003 Aug;185(15):4585-92
pubmed: 12867469
Sci Rep. 2014 Nov 20;4:7126
pubmed: 25410423
PLoS One. 2012;7(12):e51905
pubmed: 23300576
Int J Med Microbiol. 2018 Aug;308(6):675-682
pubmed: 28867522
Proc Natl Acad Sci U S A. 2013 Mar 12;110(11):4345-50
pubmed: 23401501
Front Microbiol. 2019 Apr 02;10:677
pubmed: 31001240
Nature. 2012 Sep 6;489(7414):133-6
pubmed: 22955625
FEMS Microbiol Rev. 2015 Mar;39(2):234-45
pubmed: 25725015
Int J Mol Sci. 2020 Sep 15;21(18):
pubmed: 32942569
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Bacteriol. 2004 Jul;186(14):4457-65
pubmed: 15231777
Nat Rev Microbiol. 2004 Feb;2(2):95-108
pubmed: 15040259
FEMS Immunol Med Microbiol. 2012 Jul;65(2):127-45
pubmed: 22469292
Elife. 2017 Jan 13;6:
pubmed: 28084994
Phys Rev Lett. 2004 Aug 27;93(9):098102
pubmed: 15447143
Br J Dermatol. 2007 Jun;156(6):1342-5
pubmed: 17459041
Environ Microbiol. 2011 Mar;13(3):710-21
pubmed: 21118344
FEMS Microbiol Lett. 2006 Sep;262(1):31-8
pubmed: 16907736
Soft Matter. 2013 Apr 14;9(14):3871-3876
pubmed: 23894249
Prog Mol Biol Transl Sci. 2016;142:193-239
pubmed: 27571696
Science. 2002 Feb 22;295(5559):1487
pubmed: 11859186
Mol Microbiol. 2004 Feb;51(3):675-90
pubmed: 14731271
Sci Rep. 2015 Aug 14;5:13081
pubmed: 26272750
Biophys J. 2000 Sep;79(3):1530-6
pubmed: 10969014
Nat Rev Microbiol. 2010 Sep;8(9):623-33
pubmed: 20676145
Nat Rev Microbiol. 2016 Aug 11;14(9):563-75
pubmed: 27510863
J Bacteriol. 2019 Jun 10;201(18):
pubmed: 31182499
Biophys J. 2011 Mar 16;100(6):1392-9
pubmed: 21402020
Biomicrofluidics. 2018 Aug 20;12(4):044116
pubmed: 30174775
Proc Natl Acad Sci U S A. 2019 Oct 22;116(43):21392-21400
pubmed: 31591228
Appl Environ Microbiol. 2008 Jan;74(2):470-6
pubmed: 18039822
Appl Microbiol Biotechnol. 2002 Sep;59(6):629-40
pubmed: 12226718
Sci Rep. 2015 Aug 17;5:13070
pubmed: 26278133
Drugs. 2007;67(3):351-68
pubmed: 17335295
Mol Microbiol. 2003 Oct;50(1):61-8
pubmed: 14507363
Soft Matter. 2016 Jun 29;12(26):5718-26
pubmed: 27273453
Int J Artif Organs. 2011 Sep;34(9):824-31
pubmed: 22094562
Front Oral Health. 2021 Mar 22;2:640129
pubmed: 35047995
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11541-6
pubmed: 23798445
Proc Natl Acad Sci U S A. 2007 May 8;104(19):8113-8
pubmed: 17452642
Nat Rev Microbiol. 2019 Apr;17(4):247-260
pubmed: 30760902
J Chem Phys. 2005 May 8;122(18):184905
pubmed: 15918763
Clin Microbiol Rev. 2002 Apr;15(2):167-93
pubmed: 11932229
Proc Natl Acad Sci U S A. 2015 Sep 8;112(36):11353-8
pubmed: 26311845
Environ Microbiol. 2012 Aug;14(8):1913-28
pubmed: 22176658
Mol Microbiol. 2006 Feb;59(4):1114-28
pubmed: 16430688
Nat Commun. 2016 Apr 14;7:11220
pubmed: 27075392
PLoS Pathog. 2013;9(8):e1003526
pubmed: 23950711
PLoS Pathog. 2011 Jan 27;7(1):e1001264
pubmed: 21298031

Auteurs

Eleonora Secchi (E)

Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zürich, 8093 Zürich, Switzerland.

Giovanni Savorana (G)

Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zürich, 8093 Zürich, Switzerland.

Alessandra Vitale (A)

Department of Plant and Microbial Biology, University of Zürich, 8008 Zürich, Switzerland.

Leo Eberl (L)

Department of Plant and Microbial Biology, University of Zürich, 8008 Zürich, Switzerland.

Roman Stocker (R)

Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zürich, 8093 Zürich, Switzerland.

Roberto Rusconi (R)

Department of Biomedical Sciences, Humanitas University, 20072 Pieve Emanuele, Italy.
IRCCS Humanitas Research Hospital, 20089 Rozzano, Italy.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH