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Protein expression in Escherichia coli S17-1 biofilms: impact of indole

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Abstract

Bacteria undergo significant changes during adherence to surfaces and biofilm development. Cell-to-cell signalling molecules are known to be involved in these phenotypic adaptations to the sessile mode of life. We demonstrated previously that indole can act as an extracellular signal to regulate biofilm formation in E. coli. To identify proteins over- or under-expressed in response to E. coli biofilm formation and indole signalling, we compared the proteomes of the E. coli S17-1 wild-type and 3714 (S17-1 tnaA::Tn5) tryptophanase-negative mutant cells (which don’t produce indole) grown as suspensions or biofilms in the presence or absence of exogenous indole. From computer-assisted image analysis, 407 spots were discriminated on two-dimensional electropherograms. Principal component analysis (PCA) of the electropherograms did not discriminate between the proteomes of the wild-type and mutant cells grown as suspensions indicating that indole has a␣limited impact onto protein expression of planktonic cells. The first principal component extracted by PCA, after standardization of the observations, opposed planktonic and biofilm cells confirming the existence of changes in protein expression during E. coli biofilm formation. Among proteins over- or under-expressed by both sessile wild-type and mutant cells, we identified metabolic enzymes, transporters, proteins involved in the translation and transcription machinery, stress response and regulation, and signalling proteins. The wild-type and mutant strains grown as biofilms in the presence of indole were discriminated by the second component. The role of some proteins whose expression was altered in biofilm bacteria compared to suspended counterparts is discussed.

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References

  • Anyanful A, Dolan-Livengood JM, Lewis T, Sheth S, DeZalla MN, Sherman MA, Kalman LV, Benlan GM, Kalman D (2005) Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol Microbiol 57:988–1007

    Article  PubMed  CAS  Google Scholar 

  • Arevalo-Ferro C, Reil G, Gorg A, Eberl L, Riedel K (2005) Biofilm formation of Pseudomonas putida IsoF: the role of quorum sensing as assessed by proteomics. Syst Appl Microbiol 28:87–114

    Article  PubMed  CAS  Google Scholar 

  • Barrios AF, Zuo R, Ren D, Wood TK (2006) Hha, YbaJ and OmpA regulate Escherichia coli K12 biofilm formation and conjugation plasmids abolish motility. Biotechnol Bioeng 93(1):188–200

    Article  PubMed  CAS  Google Scholar 

  • Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagenses JAJ, Molin S, Prensier G, Arbeille B, Ghigo JM (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674

    Article  PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 5:1453–1474

    Article  Google Scholar 

  • Blazer GJ, McLean RJ (2002) The stringent response genes relA and spoT are important for Escherichia coli biofilms under slow-growth conditions. Can J Microbiol 48:675–680

    Article  Google Scholar 

  • Branny P, Pearson JP, Pesci EC, Köhler T, Iglewski BH, Van Delden C (2001) Inhibition of quorum sensing by a Pseudomonas aeruginosa dksA homologue. J Bacteriol 183: 1531–1539

    Article  PubMed  CAS  Google Scholar 

  • Brown L, Gentry D, Elliot T, Cashel M (2002) DksA affects ppGpp induction of RpoS at a translational level. J Bacteriol 184:4455–4465

    Article  PubMed  CAS  Google Scholar 

  • Di Martino P, Merieau A, Phillips R, Orange N, Hulen C (2002) Isolation of an Escherichia coli strain mutant unable to form biofilm on polystyrene and to adhere to human pneumocyte cells: involvement of tryptophanase. Can J Microbiol 48:132–137

    Article  PubMed  CAS  Google Scholar 

  • Di Martino P, Fursy R, Bret L Sundararaju B, Phillips RS (2003) Indole can act as an Extracellular Signal to Regulate Biofilm Formation in Escherichia coli and in other Indole-producing Bacteria. Can J Microbiol 43:443–449

    Article  Google Scholar 

  • Dykes GA, Sampathkumar B, Korber DR (2003) Planktonic or biofilm growth affects survival, hydrophobicity and protein expression patterns of a planktonic Campylobacter jejuni strain. Int J Food Microbiol 89:1–10

    Article  PubMed  CAS  Google Scholar 

  • Ghigo JM (2001) Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442–445

    Article  PubMed  CAS  Google Scholar 

  • Gonzales Barrios AFG, Zuo R, Hashimoto Y, Yang L, Bentley WE, Wood TK (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188:305–316

    Article  CAS  Google Scholar 

  • Gurevich AI, Avakov AE, Kolosov MN (1979) The nucleotide sequence at the proximal end of rpoB gene of Escherichia coli. Bioorg Khim 5:1735–1739

    CAS  Google Scholar 

  • Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A (2005) Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126

    Article  PubMed  CAS  Google Scholar 

  • Joloba ML, Rather PN (2003) Mutations in deoB and deoC alter an extracellular signalling pathway required for activation of the gab operon in Escherichia coli. FEMS Microbiol Lett 228:151–157

    Article  PubMed  CAS  Google Scholar 

  • Jubete Y, Zabala JC, Juarez A, de la Cruz F (1995) hlyM, a transcriptional silencer downstream of the promoter in the hly operon of Escherichia coli. J Bacteriol 177:242–246

    PubMed  CAS  Google Scholar 

  • Lacour S, Landini P (2004) σS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σS-dependent genes and identification of their promoter sequences. J Bacteriol 186:7186–7195

    Article  PubMed  CAS  Google Scholar 

  • Landini P, Zehnder AJB (2002) The global regulatory hns gene negatively affects adhesion to solid surfaces by anaerobically grown Escherichia coli by modulating expression of flagellar genes and lipopolysaccharide production. J Bacteriol 184:1522–1529

    Article  PubMed  CAS  Google Scholar 

  • Nieto JM, Madrid C, Prenafeta A, Miquelay E, Balsalobre C, Carrascal M, Juarez A (2000) Expression of the hemolysin operon in Escherichia coli is modulated by a nucleotid-protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263: 349–358

    Article  PubMed  CAS  Google Scholar 

  • Nyström T, Neidhardt FC (1994) Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol Microbiol 11:537–544

    Article  PubMed  Google Scholar 

  • Olson ER, Dunyak DS, Jurss LM, Poorman RA (1991) Identification and characterization of dppA, an Escherichia coli gene encoding a periplasmic dipeptide transport protein. J Bacteriol 173:234–244

    PubMed  CAS  Google Scholar 

  • Oosthuizen MC, Steyn B, Lindsay D, Brözel VS, von Holy A (2001) Novel method fort he proteomic investigation of a dairy-associated Bacillus cereus biofilm. FEMS Microbiol Methods 194:47–51

    Article  CAS  Google Scholar 

  • Oosthuizen MC, Steyn B, Theron J, Cosette P, Lindsay D, von Holy A, Brözel VS (2002) Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl Environ Microbiol 68:2770–2780

    Article  PubMed  CAS  Google Scholar 

  • O’Toole R, Williams HD (2003) Universal stress proteins and Mycobacterium tuberculosis. Res Microbiol 154:387–392

    Article  PubMed  CAS  Google Scholar 

  • Park SJ, Cotter PA, Gunsalus RP (1995) Regulation of malate dehydrogenase (mdh) gene expression in Escherichia coli in response to oxygen, carbon, and heme availability. J Bacteriol 177:6652–6656

    PubMed  CAS  Google Scholar 

  • Perederina A, Svetlov V, Vassylyeva MN, Tahirov TH, Yokoyama S, Artsimovitch I, Vassylyev DG (2004) Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell 1183:297–309

    Article  Google Scholar 

  • Perrot F, Hebraud M, Charlionet R, Junter GA, Jouenne T (2000) Protein pattern of gel-entrapped Escherichia coli cells differ from those of free-floating organisms. Electrophoresis 21:645–653

    Article  PubMed  CAS  Google Scholar 

  • Perrot F, Hebraud M, Charlionet R, Junter GA, Jouenne T (2001) Cell immobilization induces changes in the protein response of Escherichia coli K-12 to a cold shock. Electrophoresis 22:2110–2119

    Article  PubMed  CAS  Google Scholar 

  • Prigent-Combaret C, Vidal O, Dorel C, Lejeune P (1999) Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181:5993–6002

    PubMed  CAS  Google Scholar 

  • Rabilloud T (1999) Silver staining of 2-D electrophoresis gels. Methods Mol Biol 112:297–305

    PubMed  CAS  Google Scholar 

  • Reisner A, Haagensen JA, Schembri MA, Zechner EL, Molin S (2003) Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol 48:933–946

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524

    Article  PubMed  CAS  Google Scholar 

  • Sauer K (2003) The genomics and proteomics of biofilm formation. Genome Biol 4:219

    Article  PubMed  Google Scholar 

  • Sauer K, Camper AK (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 183:6579–6589

    Article  PubMed  CAS  Google Scholar 

  • Sauer K, Camper AK, Ehrlich G DJW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154

    Article  PubMed  CAS  Google Scholar 

  • Schembri MA, Kjaergaard, Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267

    Article  PubMed  CAS  Google Scholar 

  • Schreiber K, Boes N, Eschbach M, Jaensch L, Wehland J, Bjarnsholt T, Givskov M, Hentzer M, Schobert M (2006) Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J Bacteriol 188:659–668

    Article  PubMed  CAS  Google Scholar 

  • Seefeld MA, Miller WH, Newlander KA, Burgess WJ, Payne DJ, Rittenhouse SF, Moore TD, De Wolf Jr. WE, Keller PM, Qiu X, Janson CA, Vaidya K, Fosberry AP, Smyth MG, Jaworski DD, Slater-Radosti C, Huffman WF (2001) Inhibitors of bacterial enoyl acyl carrier protein reductase (FabI): 2,9-disubstituted 1,2,3,4-tetrahydropyrido[3,4-b]indoles as potential antibacterial agents. Bioorg Med Chem Letters 11:2241–2244

    Article  CAS  Google Scholar 

  • Simon R, Priefer U, Pehle A (1983) A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1:784–890

    Article  CAS  Google Scholar 

  • Steyn B, Oosthuizen MC, MacDonald R, Theron J, Brozel VS (2001) The use of glass wool as an attachment surface for studying phenotypic changes in Pseudomonas aeruginosa biofilms by two-dimensional gel electrophoresis. Proteomics 1:871–879

    Article  PubMed  CAS  Google Scholar 

  • Svensäter G, Welin J, Wilkins JC, Beighton D, Hamilton IR (2001) Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 205:139–146

    PubMed  Google Scholar 

  • Tomlin KL, Malott RJ, Ramage G, Storey DG, Sokol PA, Ceri H (2005) Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Appl Environ Microbiol 71:5208–5218

    Article  PubMed  CAS  Google Scholar 

  • Trémoulet F, Duché O, Namane A, Martinie B, The European Listeria Genome Consortium, Labadie JC (2002a) Comparison of protein patterns of Listeria monocytogenes grown in biofilm or in planktonic mode by proteomic analysis. FEMS Microbiol Lett 210:25–31

  • Trémoulet F, Duché O, Namane A, Martinie B, Labadie JC (2002b) A proteomic study of Escherichia coli O157:H7 NCTC 12900 cultivated in biofilm or in planktonic growth mode. FEMS Microbiol Lett 215:7–14

    Article  Google Scholar 

  • Vilain S, Cosette P, Hubert M, Lange C, Junter GA, Jouenne T (2004a) Proteomic analysis of agar-entrapped Pseudomonas aeruginosa. Proteomics 4:1996–2004

    Article  CAS  Google Scholar 

  • Vilain S, Cosette P, Hubert M, Lange C, Junter GA, Jouenne T (2004b) Comparative proteomic analysis of planktonic and immobilized Pseudomonas aeruginosa cells: a multivariate statistical approach. Anal Biochem 329:120–130

    Article  CAS  Google Scholar 

  • Vilain S, Cosette P, Zimmerlin I, Dupont J-P, Junter G-A, Jouenne T (2004c) The biofilm proteome: homogeneity or versatility? J Prot Res 3:133–136

    Google Scholar 

  • Wang D, Ding X, Rather PN (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183: 4210–4216

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Ni L, Somerville RL (1993) A stationary-phase protein of Escherichia coli that affects the mode of association between the trp repressor protein and operator-bearing DNA. Proc Natl Acad Sci U S A 90:5796–800

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Patrick Di Martino.

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Collet, A., Vilain, S., Cosette, P. et al. Protein expression in Escherichia coli S17-1 biofilms: impact of indole. Antonie van Leeuwenhoek 91, 71–85 (2007). https://doi.org/10.1007/s10482-006-9097-3

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  • DOI: https://doi.org/10.1007/s10482-006-9097-3

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