Abstract
We established that Escherichia coli strain 15 (ATCC 9723) produces both curli and cellulose, and forms robust biofilms. Since this strain is wild type with respect to the phosphoenolpyruvate:sugar phosphotransferase system (PTS), it is an ideal strain in which to investigate the effects of the PTS on the biofilm growth of E. coli. We began by looking into the effects of PTS and non-PTS sugars on the biofilm growth of this strain. All the sugars tested tended to activate biofilm growth at low concentrations but to inhibit biofilm growth at high concentrations. Acidification of the medium was an inhibitory factor in the absence of buffer, but buffering to prevent a pH drop did not prevent the inhibitory effects of the sugars. The concentration at which inhibition set in varied from sugar to sugar. For most sugars, cyclic (c)AMP counteracted the inhibition at the lowest inhibitory concentrations but became ineffective at higher concentrations. Our results suggest that cAMP-dependent catabolite repression, which is mediated by the PTS in E. coli, plays a role in the regulation of biofilm growth in response to sugars. cAMP-independent processes, possibly including Cra, also appear to be involved, in addition to pH effects.
Journal Section:
Research Article
References
1.
Adams JL, McClean RJC: Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol 1999;65:4285-4287.
[PubMed]
2.
Barnhart MM, Lynem J, Chapman MR: GlcNAc-6P levels modulate the expression of curli fibers by Escherichia coli. J Bacteriol 2006;188:5212-5219.
[PubMed]
3.
Bettenbrock K, Sauter T, Jahreis K, Kremling A, Lengeler JW, Gilles E-D: Correlation between growth rates, EIIACrr phosphorylation, and intracellular cyclic AMP levels in Escherichia coli K-12. J Bacteriol 2007;189:6891-6900.
[PubMed]
4.
Chin AM, Feucht BU, Saier MH Jr: Evidence for regulation of gluconeogenesis by the fructose phosphotransferase system in Salmonella typhimurium. J Bacteriol 1987;169:897-899.
[PubMed]
5.
Corona-Izquierdo FP, Membrillo-Hernández J: A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiol Lett 2002;211:105-110.
[PubMed]
6.
Crasnier-Mednansky M, Park MC, Studley WK, Saier MH Jr: Cra-mediated regulation of Escherichia coli adenylate cyclase. Microbiology 1997;143:785-792.
[PubMed]
7.
Deutscher J, Franke C, Postma PW: How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 2006;70:939-1031.
[PubMed]
8.
Domka J, Lee J, Wood TK: YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signalling. Appl Environ Microbiol 2006;72:2449-2459.
[PubMed]
9.
Ferrières L, Thompson A, Clarke DJ: Elevated levels of σs inhibit biofilm formation in Escherichia coli: a role for the Rcs phosphorelay. Microbiology 2009;155:3544-3553.
[PubMed]
10.
Gerstel U, Römling U: Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 2001;3:638-648.
[PubMed]
11.
González Barrios AF, Zuo R, Hashimoto Y, Yang L, Bentley WE, Wood TK: Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 2006;188:305-316.
[PubMed]
12.
Görke B, Stülke J: Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 2008;6:613-624.
[PubMed]
13.
Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U: Bistable expression of CsgD in biofilm development of Salmonella enterica Serovar Typhimurium. J Bacteriol 2010;192:456-466.
[PubMed]
14.
Harwood JP, Gazdar C, Prasad C, Peterkofsky A, Curtis SJ, Epstein W: Involvement of the glucose Enzymes II of the sugar phosphotransferase system in the regulation of adenylate cyclase by glucose in Escherichiacoli. J Biol Chem 1976;251:2462-2468.
[PubMed]
15.
Hengge-Aronis R: Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 2002;66:373-395.
[PubMed]
16.
Hogema BM, Arents JC, Bader R, Eijekemans K, Yoshida H, Takahishi H, Aiba, H, Postma PW: Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of Enzyme IIAGlc. Mol Microbiol 1998;30:487-498.
[PubMed]
17.
Houot L, Chang S, Absalon C, Watnick PI: Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine. Infect Immun 2010a;78:1482-1494.
[PubMed]
18.
Houot L, Chang S, Pickering BS, Absalon C, Watnick PI: The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways. J Bacteriol 2010b;192:3055-3067.
[PubMed]
19.
Houot L, Watnick PI: A novel role for Enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. J Bacteriol 2008;190:311-320.
[PubMed]
20.
Isaacs H Jr, Chao D, Yanofsky C, Saier MH Jr: Mechanism of catabolite repression of tryptophanase synthesis in Escherichia coli. Microbiology 1994;140:2125-2134.
[PubMed]
21.
Jackson DW, Simecka JW, Romeo T: Catabolite repression of Escherichia coli biofilm formation. J Bacteriol 2002;184:3406-3410.
[PubMed]
22.
Karatan E, Watnick P: Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 2009;73:310-347.
[PubMed]
23.
Lee S-J, Boos W, Bouche J-P, Plumbridge J: Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J 2000;19:5353-5361.
[PubMed]
24.
Li J, Attila C, Wang L, Wood TK, Valdes JJ, Bentley WE: Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 2007;189:6011-6020.
[PubMed]
25.
Mika F, Busse S, Possling A, Berkholtz J, Tschowri N, Sommerfeldt N, Pruteanu M, Hengge R: Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 2012;84:51-65.
[PubMed]
26.
Mondragón V, Franco B, Jonas K, Suzuki K, Romeo T, Melefors Ö, Georgellis D: pH-dependent activation of the BarA-UvrY two-component system in Escherichia coli. J Bacteriol 2006;188:8303-8306.
[PubMed]
27.
Mukai FH: Interrelationship between colicin sensitivity and phage resistance. J Gen Microbiol 1960;23:539-551.
[PubMed]
28.
Ogasawara H, Yamamoto K, Ishihama A: Regulatory role of MlrA in transcriptional activation of csgD, the master regulator of biofilm formation in Escherichia coli. FEMS Microbiol Lett 2010;312:160-168.
[PubMed]
29.
Park Y-H, Lee BR, Seok Y-J, Peterkofsky A: In vitro reconstitution of catabolite repression in Escherichia coli. J Biol Chem 2006;281:6448-6454.
[PubMed]
30.
Pereira CS, Santos AJM, Bejerano-Sagie M, Correia PB, Marques JC, Xavier KB: Phosphoenolpyruvate phosphotransferase system regulates detection and processing of the quorum sensing signal autoinducer-2. Mol Microbiol 2012;84:93-104.
[PubMed]
31.
Pickering BS, Lopilato JE, Smith DR, Watnick PI: The transcription factor Mlc promotes Vibrio cholerae biofilm formation through repression of phosphotransferase system components. J Bacteriol 2014;196:2423-2430.
[PubMed]
32.
Pickering BS, Smith DR, Watnick PI: Glucose-specific Enzyme IIA has unique binding partners in the Vibrio cholerae biofilm. mBio 2012;3:e00228-12.
[PubMed]
33.
Plumbridge J: Expression of ptsG, the gene for the major glucose PTS transporter in Escherichia coli, is repressed by Mlc and induced by growth on glucose. Mol Microbiol 1998;29:1053-1063.
[PubMed]
34.
Plumbridge J: Expression of the phosphotransferase system both mediates and is mediated by Mlc regulation in Escherichia coli. Mol Microbiol 1999;33:260-273.
[PubMed]
35.
Postma PW, Lengeler JW, Jacobson GR: Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 1993;57:543-594.
[PubMed]
36.
Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P, Dorel C: Complex regulatory network controls adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 2001;183:7213-7223.
[PubMed]
37.
Prüss BM, Besemann C, Denton A, Wolfe AJ: A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol 2006;188:3731-3739.
[PubMed]
38.
Reshamwala SMS, Noronha SB: Biofilm formation in Escherichia colicra mutants is impaired due to down-regulation of curli biosynthesis. Arch Microbiol 2011;193:711-722.
[PubMed]
39.
Römling U, Rohde M, Olsén A, Normark S, Reinköster J: AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonellatyphimurium regulates at least two independent pathways. Mol Microbiol 2000;36:10-23.
[PubMed]
40.
Römling U, Sierralta WD, Ericksson K, Normark S: Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 1998;28:249-264.
[PubMed]
41.
Ryall B, Eydallin G, Ferenci T: Culture history and population heterogeneity as determinants of bacterial adaptation: the adaptomics of a single environmental transition. Microbiol Mol Biol Rev 2012;76:597-625.
[PubMed]
42.
Saier MH Jr, Ramseier TM: The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol 1996;178:3411-3417.
[PubMed]
43.
Saier MH Jr, Simoni RD, Roseman S: The physiological behavior of Enzyme I and heat-stable protein mutants of a bacterial phosphotransferase system. J Biol Chem 1970;245:5870-5873.
[PubMed]
44.
Stanley NR, Britton RA, Grossman AD, Lazazzera BA: Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 2003;185:1951-1957.
[PubMed]
45.
Stanley NR, Lazazzera BA: Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol 2004;52:917-924.
[PubMed]
46.
Ueguchi C, Misonou N, Mizuno T: Negative control of rpoS expression by phosphoenolpyruvate:carbohydrate phosphotransferase system in Escherichia coli. J Bacteriol 2001;183:520-527.
[PubMed]
47.
Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R: Cyclic-di-GMP-mediated signalling within the σs network of Escherichia coli. Mol Microbiol 2006;62:1014-1034.
[PubMed]
48.
Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R: Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 2005;187:1591-1603.
[PubMed]
49.
Zhang X-S, García-Contreras R, Wood TK: YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol 2007;189:3051-3062.
[PubMed]
50.
Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U: The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 2001;39:1452-1463.
[PubMed]
© 2015 S. Karger AG, Basel
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
2015
You do not currently have access to this content.
