The exopolysaccharide-eDNA interaction modulates 3D architecture of Bacillus subtilis biofilm.
Bacillus subtilis
Biofilm formation
Exopolysaccharide (EPS)
Extracellular DNA (eDNA)
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
14 05 2020
14 05 2020
Historique:
received:
28
11
2019
accepted:
16
04
2020
entrez:
16
5
2020
pubmed:
16
5
2020
medline:
27
5
2021
Statut:
epublish
Résumé
Bacterial biofilms are surface-adherent microbial communities in which individual cells are surrounded by a self-produced extracellular matrix of polysaccharides, extracellular DNA (eDNA) and proteins. Interactions among matrix components within biofilms are responsible for creating an adaptable structure during biofilm development. However, it is unclear how the interactions among matrix components contribute to the construction of the three-dimensional (3D) biofilm architecture. DNase I treatment significantly inhibited Bacillus subtilis biofilm formation in the early phases of biofilm development. Confocal laser scanning microscopy (CLSM) and image analysis revealed that eDNA was cooperative with exopolysaccharide (EPS) in the early stages of B. subtilis biofilm development, while EPS played a major structural role in the later stages. In addition, deletion of the EPS production gene epsG in B. subtilis SBE1 resulted in loss of the interaction between EPS and eDNA and reduced the biofilm biomass in pellicles at the air-liquid interface. The physical interaction between these two essential biofilm matrix components was confirmed by isothermal titration calorimetry (ITC). Biofilm 3D structures become interconnected through surrounding eDNA and EPS. eDNA interacts with EPS in the early phases of biofilm development, while EPS mainly participates in the maturation of biofilms. The findings of this study provide a better understanding of the role of the interaction between eDNA and EPS in shaping the biofilm 3D matrix structure and biofilm formation.
Sections du résumé
BACKGROUND
Bacterial biofilms are surface-adherent microbial communities in which individual cells are surrounded by a self-produced extracellular matrix of polysaccharides, extracellular DNA (eDNA) and proteins. Interactions among matrix components within biofilms are responsible for creating an adaptable structure during biofilm development. However, it is unclear how the interactions among matrix components contribute to the construction of the three-dimensional (3D) biofilm architecture.
RESULTS
DNase I treatment significantly inhibited Bacillus subtilis biofilm formation in the early phases of biofilm development. Confocal laser scanning microscopy (CLSM) and image analysis revealed that eDNA was cooperative with exopolysaccharide (EPS) in the early stages of B. subtilis biofilm development, while EPS played a major structural role in the later stages. In addition, deletion of the EPS production gene epsG in B. subtilis SBE1 resulted in loss of the interaction between EPS and eDNA and reduced the biofilm biomass in pellicles at the air-liquid interface. The physical interaction between these two essential biofilm matrix components was confirmed by isothermal titration calorimetry (ITC).
CONCLUSIONS
Biofilm 3D structures become interconnected through surrounding eDNA and EPS. eDNA interacts with EPS in the early phases of biofilm development, while EPS mainly participates in the maturation of biofilms. The findings of this study provide a better understanding of the role of the interaction between eDNA and EPS in shaping the biofilm 3D matrix structure and biofilm formation.
Identifiants
pubmed: 32410574
doi: 10.1186/s12866-020-01789-5
pii: 10.1186/s12866-020-01789-5
pmc: PMC7227074
doi:
Substances chimiques
Bacterial Proteins
0
DNA, Bacterial
0
Polysaccharides, Bacterial
0
Deoxyribonuclease I
EC 3.1.21.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
115Subventions
Organisme : National Basic Research Program of China (973 Program)
ID : 2016YFD0800206
Pays : International
Organisme : National Natural Science Foundation of China
ID : 41877029
Pays : International
Organisme : Royal Society-Newton Advanced Fellowship
ID : NAF\R1\191017
Pays : International
Organisme : National Key Research Program of China
ID : 2016YFD0800206
Pays : International
Organisme : Wuhan Science and Technology Bureau
ID : 2019020701011469
Pays : International
Références
Mol Microbiol. 2011 Nov;82(4):1015-37
pubmed: 22032623
Mol Microbiol. 2013 Feb;87(4):802-17
pubmed: 23279213
Acta Biochim Pol. 2007;54(3):495-508
pubmed: 17882321
J Appl Microbiol. 2010 Jun;108(6):2103-13
pubmed: 19941630
Mol Microbiol. 2012 Aug;85(3):418-30
pubmed: 22716461
BMC Microbiol. 2008 Oct 08;8:173
pubmed: 18842140
J Bacteriol. 2001 Nov;183(21):6288-93
pubmed: 11591672
Appl Environ Microbiol. 2010 Apr;76(7):2271-9
pubmed: 20139319
Trends Microbiol. 2005 Jan;13(1):20-6
pubmed: 15639628
FEMS Microbiol Ecol. 2003 May 1;44(2):203-15
pubmed: 19719637
Mol Microbiol. 2006 Feb;59(4):1229-38
pubmed: 16430696
Environ Microbiol. 2013 Mar;15(3):848-864
pubmed: 22934631
PLoS Pathog. 2012;8(4):e1002623
pubmed: 22496649
Mol Microbiol. 2009 Nov;74(3):609-18
pubmed: 19775247
FEMS Microbiol Rev. 2015 Sep;39(5):649-69
pubmed: 25907113
Front Microbiol. 2017 Jul 26;8:1390
pubmed: 28798731
Mol Microbiol. 2013 Nov;90(4):813-23
pubmed: 24102855
PLoS One. 2012;7(11):e48716
pubmed: 23133654
Trends Microbiol. 2008 Mar;16(3):115-25
pubmed: 18289856
Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1506-9
pubmed: 17234808
Biofouling. 2017 Oct;33(9):722-740
pubmed: 28946780
J Bacteriol. 2014 Jul;196(13):2355-66
pubmed: 24748612
J Bacteriol. 2012 Jun;194(11):2781-90
pubmed: 22328672
Biochim Biophys Acta. 1971 Feb 25;232(1):61-71
pubmed: 4995804
Environ Microbiol. 2011 Mar;13(3):710-21
pubmed: 21118344
Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11621-6
pubmed: 11572999
FEBS Open Bio. 2014 May 02;4:432-40
pubmed: 24918058
Mol Gen Genet. 1977 Oct 20;155(2):179-83
pubmed: 412055
Science. 2002 Feb 22;295(5559):1487
pubmed: 11859186
FEMS Microbiol Ecol. 2004 May 1;48(2):119-27
pubmed: 19712395
Environ Microbiol Rep. 2015 Apr;7(2):330-40
pubmed: 25472701
J Microbiol Methods. 2014 Oct;105:102-4
pubmed: 25017901
Genes Dev. 2010 Sep 1;24(17):1893-902
pubmed: 20713508
PLoS Pathog. 2009 Mar;5(3):e1000354
pubmed: 19325879
FEMS Microbiol Lett. 2011 Oct;323(2):113-23
pubmed: 22092710
Nat Rev Microbiol. 2010 Sep;8(9):623-33
pubmed: 20676145
Curr Opin Chem Biol. 2014 Aug;21:73-80
pubmed: 24954689
Environ Microbiol. 2011 Jul;13(7):1705-17
pubmed: 21605307
Mol Microbiol. 2005 Feb;55(3):739-49
pubmed: 15661000
Nat Rev Microbiol. 2008 Mar;6(3):199-210
pubmed: 18264116
FEMS Immunol Med Microbiol. 2010 Aug;59(3):324-36
pubmed: 20602635
Microbiology. 2014 Apr;160(Pt 4):682-691
pubmed: 24493247
Microbiology. 2007 Jul;153(Pt 7):2083-2092
pubmed: 17600053
Environ Sci Technol. 2011 Nov 1;45(21):9224-31
pubmed: 21910500
Appl Environ Microbiol. 2004 Apr;70(4):2349-53
pubmed: 15066831
NPJ Biofilms Microbiomes. 2017 Feb 9;3:4
pubmed: 28649405
PLoS Genet. 2010 Dec 09;6(12):e1001243
pubmed: 21170308
Curr Opin Biotechnol. 2003 Jun;14(3):255-61
pubmed: 12849777
Appl Environ Microbiol. 1997 Apr;63(4):1406-20
pubmed: 9097439
Plant Physiol. 2004 Jan;134(1):307-19
pubmed: 14684838
Proc Natl Acad Sci U S A. 2013 Apr 23;110(17):E1621-30
pubmed: 23569226
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11541-6
pubmed: 23798445
Environ Microbiol. 2007 Apr;9(4):1084-90
pubmed: 17359279