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Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface

  • Genomics and Proteomics
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Abstract

Biofilm build-up of sulphate-reducing bacteria (SRB) on metal surfaces may lead to severe corrosion of iron. To understand the processes at molecular level, in this study, a whole-genome oligonucleotide microarray was used to examine differential expression patterns between planktonic populations and mature biofilm of Desulfovibrio vulgaris on a steel surface. Statistical analysis revealed that 472 genes were differentially expressed (1.5-fold or more with a q value less than 0.025) by comparing the biofilm cells with the planktonic cells. Among the differentially expressed genes were several that corresponded to genes identified in many aerobic bacterial biofilms (i.e., Pseudomonas species and Escherichia coli) such as genes encoding flagellin, a flagellar motor switch protein, chemotaxis proteins involved in cell motility, as well as genes involved in exopolysaccharide biosynthesis. In addition, the biofilm-bound cells of D. vulgaris exhibited decreased transcription of genes involved in protein synthesis, energy metabolism and sulfate reduction, as well as genes involved in general stress responses. These findings were all consistent with early suggestion that the average physiology of the biofilm cells were similar to cells reduced in growth. Most notably, up-regulation of large number of outer membrane proteins was observed in the D. vulgaris biofilm. Although their function is still unknown, the higher expression of these genes in the biofilm could implicate important roles in the formation and maintenance of multi-cellular consortium on a steel surface. The study provided insights into the metabolic networks associated with the formation and maintenance of a D. vulgaris biofilm on a steel surface.

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References

  • Beech IB, Cheung C, Chan C, Hill M, Franco R, Lino A (1994) Study of parameters implicated in the biodeterioration of mild steel in the presence of different species of sulphate-reducing bacteria. Int Biodeterior Biodegrad 34:289–303

    CAS  Google Scholar 

  • Booth GH, Tiller AK (1968) Cathodic characteristic of mild steel in suspension of sulphate-reducing bacteria. Corros Sci 8:583–600

    CAS  Google Scholar 

  • Caldwell DE, Costerton JW (1996) Are bacterial biofilms constrained to Darwin’s concept of evolution through natural selection? Microbiol 12:347–358

    CAS  Google Scholar 

  • Conlon KM, Humphreys H, O’Gara JP (2002) icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J Bacteriol 184:4400–4440

    CAS  PubMed  PubMed Central  Google Scholar 

  • Danese PN, Pratt LA, Kolter R (2000) EPS production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182:3593–3596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dinh HT, Kuever J, Mussmann M, Hassel AW, Stratmann M, Widdel F (2004) Iron corrosion by novel anaerobic microorganisms. Nature 427:829–832

    CAS  PubMed  Google Scholar 

  • Elkins JG, Hassett DJ, Stewart PS, Schweizer HP, McDermott TR (1999) Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl Environ Microbiol 65:4594–4600

    CAS  PubMed  PubMed Central  Google Scholar 

  • George RP, Muraleedharan P, Sreekumari KR, Khatak HS (2003) Influence of surface characteristics and microstructure on adhesion of bacterial cells onto a type 304 stainless steel. Biofouling 19:1–8

    CAS  PubMed  Google Scholar 

  • Hamilton WA (2003) Microbially influenced corrosion as a model system for the study of metal microbe interactions: a unifying electron transfer hypothesis. Biofouling 19:65–76

    CAS  PubMed  Google Scholar 

  • Hancock LE, Perego M (2004) The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J Bacteriol 186:5629–5639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Fouts D, Haft DH, Selengut J, Peterson JD, Davidsen TM, Zafar N, Zhou L, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback TR, Feldblyum TV, Wall JD, Voordouw G, Fraser CM (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22:554–559

    CAS  PubMed  Google Scholar 

  • Jenney FE, Verhagen MFJM, Cui X, Adams MWW (1999) Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286:306–309

    CAS  PubMed  Google Scholar 

  • Kolter R, Losick R (1998) One for all and all for one. Science 280:226–227

    CAS  PubMed  Google Scholar 

  • Kuchma SL, O’Toole GA (2000) Surface-induced and biofilm-induced changes in gene expression. Curr Opin Biotechnol 11:429–433

    CAS  PubMed  Google Scholar 

  • LaPaglia C, Hartzell PL (1997) Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63:3158–3163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laue H, Schenk A, Li H, Lambertsen L, Neu TR, Molin S, Ullrich MS (2006) Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiol 152:2909–2918

    CAS  Google Scholar 

  • Lazazzera BA (2005) Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8:222–227

    Article  CAS  PubMed  Google Scholar 

  • Lee W, Lewandowski Z, Nielsen PH, Hamilton WA (1995) Role of sulfate-reducing bacteria in corrosion of mild steel: a review. Biofouling 8:165–194

    CAS  Google Scholar 

  • Li Y, Burne RA (2001) Regulation of the gtfBC and ftf genes of Streptococcus mutans in biofilms in response to pH and carbohydrate. Microbiol 147:2841–2848

    CAS  Google Scholar 

  • Li YH, Lau PC, Tang N, Svensater G, Ellen RP, Cvitkovitch DG (2002) Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol 184:6333–6342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Little B, Wagner P, Mansfeld F (1992) An overview of microbiologically influenced corrosion. Electrochim Acta 37:2185–2194

    CAS  Google Scholar 

  • Lopes FA, Morin P, Oliveira R, Melo LF (2005) The influence of nickel on the adhesion ability of Desulfovibrio desulfuricans. Colloids Surf B Biointerfaces 46:127–133

    CAS  PubMed  Google Scholar 

  • McKenney D, Hubner J, Muller E, Wang Y, Goldmann DA, Pier GB (1998) The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun 66:4711–4720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nuwaysir EF, Huang W, Albert TJ, Singh J, Nuwaysir K, Pitas A, Richmond T, Gorski T, Berg JP, Ballin J, McCormick M, Norton J, Pollock T, Sumwalt T, Butcher L, Porter D, Molla M, Hall C, Blattner F, Sussman MR, Wallace RL, Cerrina F, Green RD (2002) Gene expression analysis using oligonucleotide arrays produced by maskless photolithography. Genome Res 12:1749–1755

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    PubMed  Google Scholar 

  • Pankhania IP (1988) Hydrogen metabolism in sulphate-reducing bacteria and its role in anaerobic corrosion. Biofouling 1:27–47

    CAS  Google Scholar 

  • Pankhania IP, Moosavi AN, Hamilton WA (1986) Utilization of cathodic hydrogen by Desullfovibrio vulgaris (Hildenborough). J Gen Microbiol 132:3357–3365

    CAS  Google Scholar 

  • Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185:1942–1950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Penalver-Mellado M, Garcia-Heras F, Padmanabhan S, Garcia-Moreno D, Murillo FJ, Elias-Arnanz M (2006) Recruitment of a novel zinc-bound transcriptional factor by a bacterial HMGA-type protein is required for regulating multiple processes in Myxococcus xanthus. Mol Microbiol 61:910–926

    CAS  PubMed  Google Scholar 

  • Pysz MA, Conners SB, Montero CI, Shockley KR, Johnson MR, Ward DE, Kelly RM (2004) Transcriptional analysis of biofilm formation processes in the anaerobic, hyperthermophilic bacterium Thermotoga maritima. Appl Environ Microbiol 70:6098–6112

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Resch A, Rosenstein R, Nerz C, Gotz F (2005) Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 71:2663–2676

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodionov DA, Dubchak I, Arkin A, Alm E, Gelfand MS (2004) Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Genome Biol 5:R90

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Scholten JC, Conrad R (2000) Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Appl Environ Microbiol 66:2934–2942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scholten JC, Culley DE, Brockman FJ, Wu G, Zhang W (2007) Evolution of syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: an ancient horizontal gene transfer event involved. Biochem Biophys Res Commun 352:48–54

    CAS  PubMed  Google Scholar 

  • Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM (2000) A two-component system involving an HD-GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38:986–1003

    CAS  PubMed  Google Scholar 

  • Søgaard-Andersen L (2004) Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. Curr Opin Microbiol 7:587–593

    PubMed  Google Scholar 

  • Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951–1957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    CAS  PubMed  Google Scholar 

  • Sutherland I (2001) Biofilm EPSs: a strong and sticky framework. Microbiol 147:3–9

    CAS  Google Scholar 

  • Takeda S, Fujisawa Y, Matsubara M, Aiba H, Mizuno T (2001) A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC > YojN > RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol 40:440–450

    CAS  PubMed  Google Scholar 

  • Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, Hayakawa Y, Spormann AM (2006) Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188:2681–2691

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voordouw G (1996) The genus Desulfovibrio: the centennial. Appl Environ Microbiol 61:2813–2819

    Google Scholar 

  • Voordouw JK, Voordouw G (1998) Deletion of the rbo gene increases the oxygen sensitivity of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 64:2882–2887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watnick PI, Kolter R (1999) Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34:586–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teltzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864

    CAS  PubMed  Google Scholar 

  • Zhang W, Culley DE, Scholten JC, Hogan M, Vitiritti L, Brockman FJ (2006a) Global transcript expression in Desulfovibrio vulgaris grown on different electron donors. Antonie van Leeuwenhoek 89:221–237

    CAS  PubMed  Google Scholar 

  • Zhang W, Culley DE, Hogan M, Vitiritti L, Brockman FJ (2006b) Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie van Leeuwenhoek 90:41–55

    CAS  PubMed  Google Scholar 

  • Zhang W, Culley DE, Wu G, Brockman FJ (2006c) Two-component signal transduction systems of Desulfovibrio vulgaris: structural and phylogenetic analysis and deduction of putative cognate pairs. J Mol Evol 62:473–487

    CAS  PubMed  Google Scholar 

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Acknowledgments

The research described in this paper was conducted under the LDRD Program at the Pacific Northwest National Laboratory, a multi-program national laboratory operated by Battelle for the US Department of Energy under Contract DE-AC06-76RLO1830. We thank the Microbial Cell Dynamics Laboratory (MCDL) at PNNL for the use of the controlled cultivation technologies applied in this research.

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Correspondence to Weiwen Zhang or Johannes C. M. Scholten.

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Supplementary Table 1

Responsive genes involved in central intermediary, DNA and energy metabolisms, and protein synthesis (XLS 28 kb)

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Zhang, W., Culley, D.E., Nie, L. et al. Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface. Appl Microbiol Biotechnol 76, 447–457 (2007). https://doi.org/10.1007/s00253-007-1014-9

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