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

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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

  1. 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

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

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

  4. 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

  5. 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

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

  7. 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

  8. 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

  9. 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

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

  11. 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

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

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

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

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

  16. 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

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

  18. 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

  19. 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

  20. 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

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

  22. 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

  23. 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

  24. 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

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

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

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

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

  29. 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

  30. 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

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

  32. 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

  33. 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

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

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

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

  37. 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

  38. 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

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

  40. 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

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

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

  43. 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

  44. 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

  45. 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

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

  47. 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

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

  49. 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

  50. 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

  51. 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

  52. 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

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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.

Author information

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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Keywords

  • Transcriptome analysis
  • Biofilm
  • Corrosion
  • Desulfovibrio vulgaris