Reproducible biofilm cultivation of chemostat-grown escherichia coli and investigation of bacterial adhesion on biomaterials using a non-constant-depth film fermenter

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lüdecke, Claudia ^a,b   Jandt, Klaus D ^b   Siegismund, Daniel ^b   Kujau, Marian J ^a,c   Zang, Emerson ^a   Rettenmayr, Markus ^b   Bossert, Jörg ^b   Roth, Martin ^a  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c Wacker Biotech GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL; GLASS; POLITEF; POLYSTYRENE; TITANIUM DIOXIDE;

ARTICLE; BACTERIAL CELL; BACTERIUM ADHERENCE; BIOFILM; BIOREACTOR; CHEMOSTAT; CONTINUOUS CULTURE; CONTROLLED STUDY; ESCHERICHIA COLI; HYDROPHOBICITY; NON CONSTANT DEPTH FILM FERMENTER; NONHUMAN; SURFACE PROPERTY;

BACTERIAL ADHESION; BATCH CELL CULTURE TECHNIQUES; BIOCOMPATIBLE MATERIALS; BIOFILMS; ESCHERICHIA COLI; FERMENTATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; SURFACE PROPERTIES; TITANIUM;

EID: 84896792647     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084837     Document Type: Article

References (59)

1. Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Ann Rev Med 59: 415-428. (Pubitemid 351287946)
2. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: A common cause of persistent infections. Science 284: 1318-1322. (Pubitemid 29289651)
3. Christensen GD, Simpson WA, Anglen JO, Gainor BJ (2000) Methods for evaluating attached bacteria and biofilms. In: An YH, Friedman RJ, editors. Handbook of Bacterial Adhesion. Totowa: Humana Press. 213-233.
4. Coenye T, Nelis HJ (2010) In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Meth 83: 89-105.
5. Heersink J, Goeres D (2003) Reactor design considerations. In: Hamilton M, Heersink J, Buckingham-Meyer K, Goeres D, editors. The Biofilm Laboratory: Step-by-step Protocols for Experimental Design, Analysis, and Data Interpretation. Bozeman: Cytergy Publishing. 13-15.
6. Gilbert P, Caplan F, Brown MRW (1991) Centrifugation injury of Gramnegative bacteria. J Antimicrob Chemoth 27: 550-551.
7. Peterson WB, Sharma PK, van der Mei HC, Busscher HJ (2012) Bacterial cell surface damage due to centrifugal compaction. Appl Environ Microb 78: 120-125.
8. Bruinsma GM, van der Mei HC, Busscher HJ (2001) Bacterial adhesion to surface hydrophilic and hydrophobic contact lenses. Biomaterials 22: 3217-3224. (Pubitemid 32923328)
9. Bakker DP, Busscher HJ, van Zanten J, de Vries J, Klijnstra JW, et al. (2004) Multiple linear regression analysis of bacterial deposition to polyurethane coating after conditioning film formation in the marine environment. Microbiology-SGM 150: 1779-1784. (Pubitemid 38923676)
10. McCoy WF, Bryers JD, Robbins J, Costerton JW (1981) Observations of fouling biofilm formation. Can J Microbiol 27: 910-917. (Pubitemid 12215180)
11. Jass J, Costerton JW, Lappin-Scott HM (1995) Assessment of a chemostatcoupled modified Robbins device to study biofilms. J Ind Microbiol 15: 283-289. (Pubitemid 26018955)
12. Stewart PS, Rayner J, Roe F, Rees WM (2001) Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol 91: 525-532. (Pubitemid 34205766)
13. Goeres DM, Hamilton MA, Beck NA, Buckingham-Meyer K, Hilyard JD, et al. (2009) A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nat Protoc 4: 783-788.
14. Honraet K, Goetghebeur E, Nelis HJ (2005) Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J Microbiol Meth 63: 287-295. (Pubitemid 41597373)
15. Buckingham-Meyer K, Heersink J, Pitts B, Rayner J, Werner E (2003) Alternative biofilm growth reactors. In: Hamilton M, Heersink J, Buckingham-Meyer K, Goeres D, editors. The Biofilm Laboratory: Step-by-step Protocols for Experimental Design, Analysis, and Data Interpretation. Bozeman: Cytergy Publishing. 31-51.
16. Noimark S, Dunnill CW, Wilson M, Parkin IP (2009) The role of surfaces in catheter-associated infections. Chem Soc Rev 38: 3435-3448.
17. Peters AC, Wimpenny JWT (1988) A constant-depth laboratory model film fermenter. Biotechnol Bioeng 32: 263-270. (Pubitemid 18647647)
18. Kinniment SL, Wimpenny JWT, Adams D, Marsh PD (1996) The effect of chlorhexidine on defined, mixed culture oral biofilms grown in a novel model system. J Appl Bacteriol 81: 120-125. (Pubitemid 26337035)
19. Kinniment SL, Wimpenny JWT, Adams D, Marsh PD (1996) Development of a steady-state oral microbial biofilm community using the constant-depth-film fermenter. Microbiology+ 142: 631-638. (Pubitemid 26093649)
20. Morgan TD, Wilson M (2001) The effects of surface roughness and type of denture acrylic on biofilm formation by Streptococcus oralis in a constant depth film fermentor. J Appl Microbiol 91: 47-53. (Pubitemid 32623349)
21. McBain AJ, Bartolo RG, Catrenich CE, Charbonneau D, Ledder RG, et al. (2003) Growth and molecular characterization of dental plaque microcosms. J Appl Microbiol 94: 655-664. (Pubitemid 36459554)
22. Zanin ICJ, Goncalves RB, Brugnera A, Hope CK, Pratten J (2005) Susceptibility of Streptococcus mutans biofilms to photodynamic therapy: an in vitro study. J Antimicrob Chemoth 56: 324-330. (Pubitemid 41158520)
23. Hope CK, Bakht K, Burnside G, Martin GC, Burnett G, et al. (2012) Reducing the variability between constant-depth film fermenter experiments when modelling oral biofilm. J Appl Microbiol 113: 601-608.
24. Pratten J (2007) Growing oral biofilms in a constant depth film fermentor (CDFF). Curr Prot Microbiol 6: 1B.5.1-1B.5.18.
25. Hoskisson PA, Hobbs G (2005) Continuous culture-making a comeback? Microbiology+ 151: 3153-3159.
26. Geetha M, Singh AK, Asokamani R, Gogia AK (2009) Ti based biomaterials, the ultimate choice for orthopaedic implants-A review. Prog Mater Sci 54: 397-425.
27. Gristina AG (1987) Biomaterial-centered infection-Microbial adhesion versus tissue integration. Science 237: 1588-1595. (Pubitemid 17134883)
28. Subbiahdoss G, Fernandez ICS, Domingues JFD, Kuijer R, van der Mei HC, et al. (2011) In Vitro Interactions between Bacteria, Osteoblast-Like Cells and Macrophages in the Pathogenesis of Biomaterial-Associated Infections. PLoS ONE 9: e24827.
29. Busscher HJ, van der Mei HC, Subbiahdoss G, Jutte PC, van den Dungen JJAM, et al. (2012) Biomaterial-Associated Infection: Locating the Finish Line in the Race for the Surface. Sci transl med DOI: 10.1126/scitranslmed.3004528.
30. Ivanova EP, Truong VK, Wang JY, Berndt CC, Jones RT, et al. (2010) Impact of Nanoscale Roughness of Titanium Thin Film Surfaces on Bacterial Retention. Langmuir 26: 1973-1982.
31. Lüdecke C, Bossert J, Roth M, Jandt KD (2013) Physical vapor deposited titanium thin films for biomedical applications: Reproducibility of nanoscale surface roughness and microbial adhesion properties. Appl Surf Sci 280: 578-589.
32. Wu Y, Zitelli JP, TenHuisen KS, Yu XJ, Libera MR (2011) Differential response of Staphylococci and osteoblasts to varying titanium surface roughness. Biomaterials 32: 951-960.
33. Truong VK, Lapovok R, Estrin YS, Rundell S, Wang JY, et al. (2010) The influence of nano-scale surface roughness on bacterial adhesion to ultrafinegrained titanium. Biomaterials 31: 3674-3683.
34. Mitik-Dineva N, Wang J, Truong VK, Stoddart P, Malherbe F, et al. (2009) Escherichia coli, Pseudomonas aeruginosa, and Staphylococcus aureus Attachment Patterns on Glass Surfaces with Nanoscale Roughness. Curr Microbiol 58: 268-273.
35. Puckett SD, Taylor E, Raimondo T, Webster TJ (2010) The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials 31: 706-713.
36. Bayoudh S, Othmane A, Bettaieb F, Bakhrouf A, Ben Ouada H, et al. (2006) Quantification of the adhesion free energy between bacteria and hydrophobic and hydrophilic substrata. Mat Sci Eng C-Bio S 26: 300-305. (Pubitemid 43254797)
37. Boks NP, Norde W, van der Mei HC, Busscher HJ (2008) Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. Microbiology-SGM 154: 3122-3133.
38. Poncin-Epaillard F, Herry JM, Marmey P, Legeay G, Debarnot D, et al. (2013) Elaboration of highly hydrophobic polymeric surface-a potential strategy to reduce the adhesion of pathogenic bacteria? Mat Sci Eng C-Bio Appl 33: 1152-1161.
39. Maurer R, Meyer BJ, Ptashne M (1980) Gene regulation at the right operator (OR) of bacteriophage lambda. I. OR3 and autogenous negative control by repressor. J Mol Biol 139: 147-161. (Pubitemid 10057781)
40. Crameri A, Whitehorn EA, Tate E, Stemmer WPC (1996) Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol 14: 315-319.
41. Cai KY, Müller M, Bossert J, Rechtenbach A, Jandt KD (2005) Surface structure and composition of flat titanium thin films as a function of film thickness and evaporation rate. Appl Surf Sci 250: 252-267. (Pubitemid 41162306)
42. Necas D, Klapetek P (2012) Gwyddion: an open-source software for SPM data analysis. Cent Eur J Phys 10: 181-188.
43. de Paz LC (2009) Image Analysis Software Based on Color Segmentation for Characterization of Viability and Physiological Activity of Biofilms. Appl Environ Microb 75: 1734-1739.
44. Taylor JR (1997) An introduction to error analysis: The studies of uncertainties in physical measurements. Sausalito: University Science Books. 327 p.
45. Katsikogianni M, Missirlis YF (2004) Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cells Mater 8: 37-57. (Pubitemid 40132321)
46. Boland T, Latour RA, Stutzenberger FJ (2000) Molecular Basis of Bacterial Adhesion. In: An YH, Friedman RJ, editors. Handbook of Bacterial Adhesion. Totowa: Humana Press. 29-41.
47. Lorite GS, Rodrigues CM, de Souza AA, Kranz C, Mizaikoff B, et al. (2011) The role of conditioning film formation and surface chemical changes on Xylella fastidiosa adhesion and biofilm evolution. J Colloid Interf Sci 359: 289-295.
48. Chen MY, Chen MJ, Lee PF, Cheng LH, Huang LJ, et al. (2010) Towards realtime observation of conditioning film and early biofilm formation under laminar flow conditions using a quartz crystal microbalance. Biochem Eng J 53: 121-130.
49. Hoffman AS, Ratner BD (2004) Nonfouling surfaces. In: Ratner BD, Hoffman AS, Schoen FJ, Lemons JE, editors. An Introduction to Materials in Medicine. London: Elsevier Academic Press. 197-201.
50. Ong YL, Razatos A, Georgiou G, Sharma MM (1999) Adhesion forces between E. coli bacteria and biomaterial surfaces. Langmuir 15: 2719-2725.
51. Singh AV, Galluzzi M, Borghi F, Indrieri M, Vyas V, et al. (2013) Interaction of Bacterial Cells with Cluster-Assembled Nanostructured Titania Surfaces: An Atomic Force Microscopy Study. J Nanosci Nanotechno 13: 77-85.
52. Webb HK, Boshkovikj V, Fluke CJ, Truong VK, Hasan J, et al. (2013) Bacterial attachment on sub-nanometrically smooth titanium substrata. Biofouling 29: 163-170.
53. Siegismund D, Undisz A, Germeroth S, Schuster S, Rettenmayr M (2014) Quantification of the interaction between biomaterial surfaces and bacteria by 3-D-modeling. Acta Biomater 10: 267-275.
54. Gadelmawla ES, Koura MM, Maksoud TMA, Elewa IM, Soliman HH (2002) Roughness parameters. J Mater Process Tech 123: 133-145. (Pubitemid 34249719)
55. Webb HK, Truong VK, Hasan J, Fluke CJ, Crawford RJ, et al. (2012) Roughness parameters for standard description of surface nanoarchitecture. Scanning 34: 257-263.
56. Mitik-Dineva N, Wang J, Mocanasu RC, Stoddart PR, Crawford RJ, et al. (2008) Impact of nano-topography on bacterial attachment. Biotechnol J 3: 536-544. (Pubitemid 351618739)
57. Wenzel RN (1949) Surface roughness and contact angle. J Phys Colloid Chem 53: 1466-1467.
58. Lin FYH, Neumann AW (1993) Effect of surface-roughness on the dependence of contact angles on drop size. J Colloid Interf Sci 159: 86-95.
59. Cai KY, Bossert J, Jandt KD (2006) Does the nanometre scale topography of titanium influence protein adsorption and cell proliferation? Colloid Surface B 49: 136-144. (Pubitemid 44304399)