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Self-organised nanoarchitecture of titanium surfaces influences the attachment of Staphylococcus aureus and Pseudomonas aeruginosa bacteria

  • Applied microbial and cell physiology
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Abstract

The surface nanotopography and architecture of medical implant devices are important factors that can control the extent of bacterial attachment. The ability to prevent bacterial attachment substantially reduces the possibility of a patient receiving an implant contracting an implant-borne infection. We now demonstrated that two bacterial strains, Staphylococcus aureus and Pseudomonas aeruginosa, exhibited different attachment affinities towards two types of molecularly smooth titanium surfaces each possessing a different nanoarchitecture. It was found that the attachment of S. aureus cells was not restricted on surfaces that had an average roughness (S a) less than 0.5 nm. In contrast, P. aeruginosa cells were found to be unable to colonise surfaces possessing an average roughness below 1 nm, unless sharp nanoprotrusions of approximately 20 nm in size and spaced 35.0 nm apart were present. It is postulated that the enhanced attachment of P. aeruginosa onto the surfaces possessing these nanoprotrusions was facilitated by the ability of the cell membrane to stretch over the tips of the nanoprotrusions as confirmed through computer simulation, together with a concomitant increase in the level of extracellular polymeric substance (EPS) being produced by the bacterial cells.

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References

  • Aicheler M, Sgobba S, Arnau-Izquierdo G, Taborelli M, Calatroni S, Neupert H, Wuensch W (2011) Evolution of surface topography in dependence on the grain orientation during surface thermal fatigue of polycrystalline copper. Int J Fatigue 33(3):396–402

    Article  CAS  Google Scholar 

  • An YH, Friedman RJ, Draughn RA, Smith EA, Nicholson JH, John JF (1995) Rapid quantification of staphylococci adhered to titanium surfaces using image analyzed epifluorescence microscopy. J Microbiol Methods 24(1):29–40

    Article  Google Scholar 

  • Anselme K, Davidson P, Popa AM, Giazzon M, Liley M, Ploux L (2010) The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater 6(10):3824–3846

    Article  CAS  PubMed  Google Scholar 

  • Assender H, Bliznyuk V, Porfyrakis K (2002) How surface topography relates to materials’ properties. Science 297(5583):973–976

    Article  CAS  PubMed  Google Scholar 

  • Bos R, Van Der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microbiol Rev 23(2):179–229

    Article  CAS  PubMed  Google Scholar 

  • Boulangé-Petermann L, Rault J, Bellon-Fontaine MN (1997) Adhesion of Streptococcus thermophilus to stainless steel with different surface topography and roughness. Biofouling 11(3):201–216

    Article  Google Scholar 

  • Chai L, Klein J (2007) Large area, molecularly smooth (0.2 nm rms) gold films for surface forces and other studies. Langmuir 23(14):7777–7783

    Article  CAS  PubMed  Google Scholar 

  • Colon G, Ward BC, Webster TJ (2006) Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. J Biomed Mater Res A 78:595–604

    Article  PubMed  Google Scholar 

  • Crawford RJ, Webb HK, Truong VK, Hasan J, Ivanova EP (2012) Surface topographical factors influencing bacterial attachment. Adv Colloid Interf Sci 179–182:142–149

    Article  Google Scholar 

  • Decuzzi P, Ferrari M (2010) Modulating cellular adhesion through nanotopography. Biomaterials 31(1):173–179

    Article  CAS  PubMed  Google Scholar 

  • Díaz C, Schilardi PL, Salvarezza RC, De Mele MFL (2007) Nano/microscale order affects the early stages of biofilm formation on metal surfaces. Langmuir 23(22):11206–11210

    Article  PubMed  Google Scholar 

  • Fadeeva E, Truong VK, Stiesch M, Chichkov BN, Crawford RJ, Wang J, Ivanova EP (2011) Bacterial retention on superhydrophobic titanium surfaces fabricated by femtosecond laser ablation. Langmuir 27(6):3012–3019

    Article  CAS  PubMed  Google Scholar 

  • Gentile F, Tirinato L, Battista E, Causa F, Liberale C, di Fabrizio EM, Decuzzi P (2010) Cells preferentially grow on rough substrates. Biomaterials 31(28):7205–7212

    Article  CAS  PubMed  Google Scholar 

  • Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146(10):2395–2407

    CAS  PubMed  Google Scholar 

  • Irie Y, Borlee BR, O'Connor JR, Hill PJ, Harwood CS, Wozniak DJ, Parsek MR (2012) Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 109(50):20632–20636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ivanova EP, Pham DK, Wright JP, Nicolau DV (2002) Detection of coccoid forms of Sulfitobacter mediterraneus using atomic force microscopy. FEMS Microbiol Lett 214(2):177–181

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Mitik-Dineva N, Wang J, Pham DK, Wright JP, Nicolau DV, Mocanasu RC, Crawford RJ (2008) Staleya guttiformis attachment on poly(tert-butylmethacrylate) polymeric surfaces. Micron 39(8):1197–1204

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Truong VK, Wang J, Berndt CC, Jones TR, Yusuf II, Peake I, Schmidt HW, Fluke C, Barnes D, Crawford RJ (2010) Impact of nanoscale roughness of titanium thin films surfaces on bacterial retention. Langmuir 26(3):1973–1982

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Truong VK, Webb HK, Baulin VA, Wang JY, Mohammodi N, Wang F, Fluke C, Crawford RJ (2011) Differential attraction and repulsion of Staphylococcus aureus and Pseudomonas aeruginosa on molecularly smooth titanium films. Sci Rep 1:165

    Article  PubMed Central  PubMed  Google Scholar 

  • Li B, Logan BE (2004) Bacterial adhesion to glass and metal-oxide surfaces. Colloid Surf B 36(2):81–90

    Article  CAS  Google Scholar 

  • Medilanski E, Kaufmann K, Wick LY, Wanner O, Harms H (2002) Influence of the surface topography of stainless steel on bacterial adhesion. Biofouling 18(3):193–203

    Article  Google Scholar 

  • Misra G, Rojas ER, Gopinathan A, Huang KC (2013a) Mechanical consequences of cell-wall turnover in the elongation of a gram-positive bacterium. Biophys J 104(11):2342–2352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Misra RDK, Nune C, Pesacreta TC, Somani MC, Karjalainen LP (2013b) Understanding the impact of grain structure in austenitic stainless steel from a nanograined regime to a coarse-grained regime on osteoblast functions using a novel metal deformation-annealing sequence. Acta Biomater 9(4):6245–6258

    Article  CAS  PubMed  Google Scholar 

  • Mitik-Dineva N, Wang J, Truong VK, Stoddart P, Malherbe F, Crawford RJ, Ivanova EP (2009) Escherichia coli, Pseudomonas aeruginosa, and Staphylococcus aureus attachment patterns on glass surfaces with nanoscale roughness. Curr Microbiol 58(3):268–273

    Article  CAS  PubMed  Google Scholar 

  • Park MR, Banks MK, Applegate B, Webster TJ (2008) Influence of nanophase titania topography on bacterial attachment and metabolism. Int J Nanomedicine 3(4):497–504

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peltonen J, Järn M, Areva S, Linden M, Rosenholm JB (2004) Topographical parameters for specifying a three-dimensional surface. Langmuir 20(22):9428–9431

    Article  CAS  PubMed  Google Scholar 

  • Ploux L, Anselme K, Dirani A, Ponche A, Soppera O, Roucoules V (2009) Opposite responses of cells and bacteria to micro/nanopatterned surfaces prepared by pulsed plasma polymerization and UV-irradiation. Langmuir 25(14):8161–8169

    Article  CAS  PubMed  Google Scholar 

  • Ploux L, Ponche A, Anselme K (2010) Bacteria/material interfaces: role of the material and cell wall properties. J Adhes Sci Technol 24(13-14):2165–2201

    Article  CAS  Google Scholar 

  • Pogodin S, Hasan J, Baulin VA, Webb HK, Truong VK, Phong Nguyen TH, Boshkovikj V, Fluke CJ, Watson GS, Watson JA, Crawford RJ, Ivanova EP (2013) Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J 104(4):835–840

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Puckett SD, Taylor E, Raimondo T, Webster TJ (2010) The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials 31(4):706–713

    Article  CAS  PubMed  Google Scholar 

  • Rowan B, Wheeler MA, Crooks RM (2002) Patterning bacteria within hyperbranched polymer film templates. Langmuir 18(25):9914–9917

    Article  CAS  Google Scholar 

  • Rozhok S, Fan Z, Nyamjav D, Liu C, Mirkin CA, Holz RC (2006) Attachment of motile bacterial cells to prealigned holed microarrays. Langmuir 22(26):11251–11254

    Article  CAS  PubMed  Google Scholar 

  • Ryder C, Byrd M, Wozniak DJ (2007) Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 10(6):644–648

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scardino AJ, Guenther J, de Nys R (2008) Attachment point theory revisited: the fouling response to a microtextured matrix. Biofouling 24(1):45–53

    Article  CAS  PubMed  Google Scholar 

  • Siegismund D, Undisz A, Germerodt S, Schuster S, Rettenmayr M (2014) Quantification of the interaction between biomaterial surfaces and bacteria by 3-D modeling. Acta Biomater 10(1):267–275

    Article  CAS  PubMed  Google Scholar 

  • Tay CY, Irvine SA, Boey FYC, Tan LP, Venkatraman S (2011) Micro-/nano-engineered cellular responses for soft tissue engineering and biomedical applications. Small 7(10):1361–1378

    Article  CAS  PubMed  Google Scholar 

  • Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 17(SUPPL 2):68–81

    Article  PubMed  Google Scholar 

  • Torres AJ, Wu M, Holowka D, Baird B (2008) Nanobiotechnology and cell biology: micro- and nanofabricated surfaces to investigate receptor-mediated signaling. Annu Rev Biophys 37:265–288

    Article  CAS  PubMed  Google Scholar 

  • Truong VK, Lapovok R, Estrin YS, Rundell S, Wang JY, Fluke CJ, Crawford RJ, Ivanova EP (2010) The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31(13):3674–3683

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Song R, Li Y, Shen J (2003) Understanding tapping-mode atomic force microscopy data on the surface of soft block copolymers. Surf Sci 530(3):136–148

    Article  CAS  Google Scholar 

  • Webb HK, Crawford RJ, Sawabe T, Ivanova EP (2009) Poly(ethylene terephthalate) polymer surfaces as a substrate for bacterial attachment and biofilm formation. Microbes Environ 24(1):39–42

    Article  PubMed  Google Scholar 

  • Webb HK, Truong VK, Hasan J, Crawford RJ, Ivanova EP (2011) Physico-mechanical characterisation of cells using atomic force microscopy—current research and methodologies. J Microbiol Methods 86(2):131–139

    Article  PubMed  Google Scholar 

  • Webb HK, Boshkovikj V, Fluke CJ, Truong VK, Hasan J, Baulin VA, Lapovok R, Estrin Y, Crawford RJ, Ivanova EP (2013) Bacterial attachment on sub-nanometrically smooth titanium substrata. Biofouling 29(2):163–170

    Article  CAS  PubMed  Google Scholar 

  • Whitehead KA, Colligon J, Verran J (2005) Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloid Surf B 41(2-3):129–138

    Article  CAS  Google Scholar 

  • Whitehead KA, Rogers D, Colligon J, Wright C, Verran J (2006) Use of the atomic force microscope to determine the effect of substratum surface topography on the ease of bacterial removal. Colloid Surf B 51(1):44–53

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported in part by Australian Research Council through an ARC Linkage grant.

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Correspondence to Elena P. Ivanova.

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Truong, V.K., Pham, V.T.H., Medvedev, A. et al. Self-organised nanoarchitecture of titanium surfaces influences the attachment of Staphylococcus aureus and Pseudomonas aeruginosa bacteria. Appl Microbiol Biotechnol 99, 6831–6840 (2015). https://doi.org/10.1007/s00253-015-6572-7

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  • DOI: https://doi.org/10.1007/s00253-015-6572-7

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