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Mechano-bactericidal actions of nanostructured surfaces

Nature Reviews Microbiology volume 19, pages 8–22 (2021)Cite this article

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Abstract

Antibiotic resistance is a global human health threat, causing routine treatments of bacterial infections to become increasingly difficult. The problem is exacerbated by biofilm formation by bacterial pathogens on the surfaces of indwelling medical and dental devices that facilitate high levels of tolerance to antibiotics. The development of new antibacterial nanostructured surfaces shows excellent prospects for application in medicine as next-generation biomaterials. The physico-mechanical interactions between these nanostructured surfaces and bacteria lead to bacterial killing or prevention of bacterial attachment and subsequent biofilm formation, and thus are promising in circumventing bacterial infections. This Review explores the impact of surface roughness on the nanoscale in preventing bacterial colonization of synthetic materials and categorizes the different mechanisms by which various surface nanopatterns exert the necessary physico-mechanical forces on the bacterial cell membrane that will ultimately result in cell death.

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Fig. 1: Comparison of biomimetic antibiofouling and mechano-bactericidal nanostructured surfaces.
Fig. 2: Two classes of mechano-bactericidal action of nanostructured surfaces.
Fig. 3: Differential attachment of bacteria to micro–nanostructured surfaces.
Fig. 4: Variation in the topographic dimensions of mechano-bactericidal surface nanopatterns.

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References

  1. Campoccia, D., Montanaro, L. & Arciola, C. R. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27, 2331–2339 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Bhushan, B. in Biomimetics 23–33 (Springer International Publishing, 2016).

  3. Ventola, C. L. The antibiotic resistance crisis: part 1: causes and threats. P T 40, 277–283 (2015).

    PubMed  PubMed Central  Google Scholar 

  4. Montanaro, L. et al. Future microbiology. Was. Med. 6, 1329–1349 (2011).

    CAS  Google Scholar 

  5. Campoccia, D., Montanaro, L. & Arciola, C. R. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials 34, 8533–8554 (2013). This is a thorough review of antibacterial surface modifications.

    Article  CAS  PubMed  Google Scholar 

  6. Gimeno, M. et al. A controlled antibiotic release system to prevent orthopaedic-implant associated infections: an in vitro study. Eur. J. Pharm. Biopharm. 96, 264-271 (2015).

  7. Lee, K. K., Bhushan, B. & Hansford, D. Nanotribological characterization of fluoropolymer thin films for biomedical micro/nanoelectromechanical system applications. J. Vac. Sci. Technol. A 23, 804–810 (2005).

    Article  CAS  Google Scholar 

  8. Bhushan, B., Hansford, D. & Lee, K. K. Surface modification of silicon and polydimethylsiloxane surfaces with vapor-phase-deposited ultrathin fluorosilane films for biomedical nanodevices. J. Vac. Sci. Technol. A 24, 1197–1202 (2006).

    Article  CAS  Google Scholar 

  9. Li, X. et al. Recent developments in smart antibacterial surfaces to inhibit biofilm formation and bacterial infections. J. Mater. Chem. B 6, 4274–4292 (2018).

    Article  CAS  PubMed  Google Scholar 

  10. Spriano, S., Yamaguchi, S., Baino, F. & Ferraris, S. A critical review of multifunctional titanium surfaces: new frontiers for improving osseointegration and host response, avoiding bacteria contamination. Acta Biomater. 79, 1–22 (2018). This is thorough review of antibacterial surface modifications for titanium implants.

    Article  CAS  PubMed  Google Scholar 

  11. Ferraris, S. & Spriano, S. Antibacterial titanium surfaces for medical implants. Mater. Sci. Eng. C. 61, 965–978 (2016).

    Article  CAS  Google Scholar 

  12. Chouirfa, H., Bouloussa, H., Migonney, V. & Falentin-Daudré, C. Review of titanium surface modification techniques and coatings for antibacterial applications. Acta Biomater. 83, 37–54 (2019).

    Article  CAS  PubMed  Google Scholar 

  13. Westberg, M. et al. Effectiveness of gentamicin-containing collagen sponges for prevention of surgical site infection after hip arthroplasty: a multicenter randomized trial. Clin. Infect. Dis. 60, 1752–1759 (2015).

    Article  PubMed  Google Scholar 

  14. Belt, et al. Gentamicin release from polymethylmethacrylate bone cements and staphylococcus aureus biofilm formation. Acta Orthop. Scand. 71, 625–629 (2000).

    Article  PubMed  Google Scholar 

  15. Puckett, S. D., Taylor, E., Raimondo, T. & Webster, T. J. The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials 31, 706–713 (2010). This article demonstrates the decreased adhesion of bacteria to nanostructured titanium.

    Article  CAS  PubMed  Google Scholar 

  16. Linklater, D. P., Juodkazis, S. & Ivanova, E. P. Nanofabrication of mechano-bactericidal surfaces. Nanoscale 9, 16564–16585 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Crawford, R. J., Webb, H. K., Truong, V. K., Hasan, J. & Ivanova, E. P. Surface topographical factors influencing bacterial attachment. Adv. Colloid Interface Sci. 179–182, 142–149 (2012).

    Article  PubMed  CAS  Google Scholar 

  18. Sengstock, C. et al. Structure-related antibacterial activity of a titanium nanostructured surface fabricated by glancing angle sputter deposition. Nanotechnology 25, 195101 (2014).

    Article  PubMed  CAS  Google Scholar 

  19. Stolzoff, M. et al. Decreased bacterial growth on titanium nanoscale topographies created by ion beam assisted evaporation. Int. J. Nanomed. 12, 1161–1169 (2017).

    Article  CAS  Google Scholar 

  20. Truong, V. K. 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).

    Article  CAS  PubMed  Google Scholar 

  21. Narendrakumar, K. et al. Adherence of oral streptococci to nanostructured titanium surfaces. Dent. Mater. 31, 1460–1468 (2015).

    Article  CAS  PubMed  Google Scholar 

  22. Bierbaum, S. et al. Osteogenic nanostructured titanium surfaces with antibacterial properties under conditions that mimic the dynamic situation in the oral cavity. Biomater. Sci. 6, 1390–1402 (2018).

    Article  CAS  PubMed  Google Scholar 

  23. James, S. A., Hilal, N. & Wright, C. J. Atomic force microscopy studies of bioprocess engineering surfaces - imaging, interactions and mechanical properties mediating bacterial adhesion. Biotechnol. J. 12, 1600698 (2017).

    Article  CAS  Google Scholar 

  24. Quirynen, M. et al. An in vivo study of the influence of the surface roughness of implants on the microbiology of supra- and subgingival plaque. J. Dent. Res. 72, 1304–1309 (1993).

    Article  CAS  PubMed  Google Scholar 

  25. Almaguer-Flores, A. et al. Influence of topography and hydrophilicity on initial oral biofilm formation on microstructured titanium surfaces in vitro. Clin. Oral. Implant. Res. 23, 301–307 (2011).

    Article  Google Scholar 

  26. Harris, L. G., Meredith, D. O., Eschbach, L. & Richards, R. G. Staphylococcus aureus adhesion to standard micro-rough and electropolished implant materials. J. Mater. Sci. Mater. Med. 18, 1151–1156 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Ivanova, E. P. et al. Impact of nanoscale roughness of titanium thin film surfaces on bacterial retention. Langmuir 26, 1973–1982 (2010).

    Article  CAS  PubMed  Google Scholar 

  28. Mei, L., Busscher, H. J., van der Mei, H. C. & Ren, Y. Influence of surface roughness on streptococcal adhesion forces to composite resins. Dent. Mater. 27, 770–778 (2011).

    Article  CAS  PubMed  Google Scholar 

  29. Truong, V. K. et al. The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31, 3674–3683 (2010).

    Article  CAS  PubMed  Google Scholar 

  30. Fröjd, V. et al. In situ analysis of multispecies biofilm formation on customized titanium surfaces. Mol. Oral. Microbiol. 26, 241–252 (2011).

    Article  PubMed  CAS  Google Scholar 

  31. Arnold, J. W. & Bailey, G. W. Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: scanning electron and atomic force microscopy study. Poult. Sci. 79, 1839–1845 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Medilanski, E., Kaufmann, K., Wick, L. Y., Wanner, O. & Harms, H. Influence of the surface topography of stainless steel on bacterial adhesion. Biofouling 18, 193–203 (2002).

    Article  Google Scholar 

  33. Carlén, A., Nikdel, K., Wennerberg, A., Holmberg, K. & Olsson, J. Surface characteristics and in vitro biofilm formation on glass ionomer and composite resin. Biomaterials 22, 481–487 (2001).

    Article  PubMed  Google Scholar 

  34. Gharechahi, M., Moosavi, H. & Forghani, M. Effect of surface roughness and materials composition. J. Biomater. Nanobiotechnol. 3, 541–546 (2012).

    Article  CAS  Google Scholar 

  35. Lu, A. et al. Effects of surface roughness and texture on the bacterial adhesion on the bearing surface of bio-ceramic joint implants: an in vitro study. Ceram. Int. 46, 6550–6559 (2020).

    Article  CAS  Google Scholar 

  36. Vasudevan, R., Kennedy, A. J., Merritt, M., Crocker, F. H. & Baney, R. H. Microscale patterned surfaces reduce bacterial fouling-microscopic and theoretical analysis. Colloids Surf. B Biointerfaces 117, 225–232 (2014).

    Article  CAS  PubMed  Google Scholar 

  37. Truong, V. K. et al. Air-directed attachment of coccoid bacteria to the surface of superhydrophobic lotus-like titanium. Biofouling 28, 539–550 (2012).

    Article  CAS  PubMed  Google Scholar 

  38. Fadeeva, E. et al. Bacterial retention on superhydrophobic titanium surfaces fabricated by femtosecond laser ablation. Langmuir 27, 3012–3019 (2011).

    Article  CAS  PubMed  Google Scholar 

  39. Gu, H. et al. How Escherichia coli lands and forms cell clusters on a surface: a new role of surface topography. Sci. Rep. 6, 29516 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hou, S., Gu, H., Smith, C. & Ren, D. Microtopographic patterns affect Escherichia coli biofilm formation on poly(dimethylsiloxane) surfaces. Langmuir 27, 2686–2691 (2011).

    Article  CAS  PubMed  Google Scholar 

  41. Vadillo-Rodríguez, V., Guerra-García-Mora, A. I., Perera-Costa, D., Gónzalez-Martín, M. L. & Fernández-Calderón, M. C. Bacterial response to spatially organized microtopographic surface patterns with nanometer scale roughness. Colloids Surf. B Biointerfaces 169, 340–347 (2018). This article demonstrates that bacteria can identify nanotopographic cues and preferential spatial organization.

    Article  PubMed  CAS  Google Scholar 

  42. Perera-Costa, D., Bruque, J. M., González-Martín, M. L., Gómez-García, A. C. & Vadillo-Rodríguez, V. Studying the influence of surface topography on bacterial adhesion using spatially organized microtopographic surface patterns. Langmuir 30, 4633–4641 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Whitehead, K. A., Colligon, J. & Verran, J. Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf. B Biointerfaces 41, 129–138 (2005).

    Article  CAS  PubMed  Google Scholar 

  44. Ploux, L. et al. Opposite responses of cells and bacteria to micro/nanopatterned surfaces prepared by pulsed plasma polymerization and UV-irradiation. Langmuir 25, 8161–8169 (2009).

    Article  CAS  PubMed  Google Scholar 

  45. Díaz, C., Schilardi, P. L., Salvarezza, R. C. & Fernández Lorenzo de Mele, M. Nano/microscale order affects the early stages of biofilm formation on metal surfaces. Langmuir 23, 11206–11210 (2007).

    Article  PubMed  CAS  Google Scholar 

  46. Cunha, A. et al. Femtosecond laser surface texturing of titanium as a method to reduce the adhesion of Staphylococcus aureus and biofilm formation. Appl. Surf. Sci. 360, 485–493 (2016).

    Article  CAS  Google Scholar 

  47. Kelleher, S. M. et al. Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl. Mater. Interfaces 8, 14966–14974 (2016).

    Article  CAS  PubMed  Google Scholar 

  48. Linklater, D. P., Juodkazis, S., Rubanov, S. & Ivanova, E. P. Comment on “Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli”. ACS Appl. Mater. Interfaces 9, 29387–29393 (2017).

    Article  CAS  PubMed  Google Scholar 

  49. Encinas, N. et al. Submicrometer-sized roughness suppresses bacteria adhesion. ACS Appl. Mater. Interfaces 12, 21192–21200 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Peter, A. et al. Direct laser interference patterning of stainless steel by ultrashort pulses for antibacterial surfaces. Opt. Laser Technol. 123, 105954 (2020).

    Article  CAS  Google Scholar 

  51. Koishi, T., Yasuoka, K., Fujikawa, S., Ebisuzaki, T. & Zeng, X. C. Coexistence and transition between cassie and wenzel state on pillared hydrophobic surface. Proc. Natl Acad. Sci. USA 106, 8435–8440 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Zhang, B. et al. Fabrication of biomimetically patterned surfaces and their application to probing plant–bacteria interactions. ACS Appl. Mater. Interfaces 6, 12467–12478 (2014).

    Article  CAS  PubMed  Google Scholar 

  53. Ge, X. et al. Bacterial responses to periodic micropillar array. J. Biomed. Mater. Res. A 103, 384–396 (2014).

    Article  PubMed  CAS  Google Scholar 

  54. Zhang, X., Wang, L. & Levänen, E. Superhydrophobic surfaces for the reduction of bacterial adhesion. RSC Adv. 3, 12003 (2013).

    Article  CAS  Google Scholar 

  55. Ensikat, HJ, Ditsche-Kuru, P., Neinhuis, C. & Barthlott, W. Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Beilstein J. Nanotechnol. 2, 152–161 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zeiger, C. et al. Microstructures of superhydrophobic plant leaves - inspiration for efficient oil spill cleanup materials. Bioinspir. Biomim. 11, 056003 (2016).

    Article  PubMed  Google Scholar 

  57. Sakamoto, A. et al. Antibacterial effects of protruding and recessed shark skin micropatterned surfaces of polyacrylate plate with a shallow groove. FEMS Microbiol. Lett. 361, 10–16 (2014).

    Article  CAS  PubMed  Google Scholar 

  58. Wagner, T., Neinhuis, C. & Barthlott, W. Wettability and contaminability of insect wings as a function of their surface sculptures. Acta Zool. 77, 213–225 (1996).

    Article  Google Scholar 

  59. Webb, H. K., Hasan, J., Truong, V. K., Crawford, R. & Ivanova, E. P. Nature Inspired Structured Surfaces for Biomedical Applications. Curr. Med. Chem. 18, 3367–3375 (2011).

    Article  CAS  PubMed  Google Scholar 

  60. Lima, A. C. & Mano, J. F. Micro-/nano-structured superhydrophobic surfaces in the biomedical field: part I: basic concepts and biomimetic approaches. Nanomedicine 10, 103–119 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Hwang, G. B. et al. The anti-biofouling properties of superhydrophobic surfaces are short-lived. ACS Nano 12, 6050–6058 (2018). This article shows that prolonged immersion of superhydrophobic surfaces results in loss of air entrapment and subsequent bacterial attachment.

    Article  CAS  PubMed  Google Scholar 

  62. Zhang, H., Lamb, R. & Lewis, J. Engineering nanoscale roughness on hydrophobic surface — preliminary assessment of fouling behaviour. Sci. Technol. Adv. Mater. 6, 236–239 (2005).

    Article  CAS  Google Scholar 

  63. Harris, L. G. & Richards, R. G. Staphylococci and implant surfaces: a review. Injury 37, S3–S14 (2006).

    Article  PubMed  Google Scholar 

  64. Bazaka, K., Crawford, R. J. & Ivanova, E. P. Do bacteria differentiate between degrees of nanoscale surface roughness? Biotechnol. J. 6, 1103–1114 (2011).

    Article  CAS  PubMed  Google Scholar 

  65. Graham, M. V., Mosier, A. P., Kiehl, T. R., Kaloyeros, A. E. & Cady, N. C. Development of antifouling surfaces to reduce bacterial attachment. Soft Matter 9, 6235 (2013).

    Article  CAS  Google Scholar 

  66. Ivanova, E. P. et al. Natural bactericidal surfaces: mechanical rupture of pseudomonas aeruginosa cells by cicada wings. Small 8, 2489–2494 (2012). This is the original article demonstrating the rupture of bacteria on insect wing surfaces.

    Article  CAS  PubMed  Google Scholar 

  67. Ivanova, E. P. et al. Bactericidal activity of black silicon. Nat. Commun. 4, 2838 (2013). This is the work to show the mechanical rupture of bacteria on a biomimetic synthetic surface topography.

  68. Hasan, J. et al. Selective bactericidal activity of nanopatterned superhydrophobic Cicada psaltoda claripennis wing surfaces. Appl. Microbiol. Biotechnol. 97, 9257–9262 (2012).

    Article  PubMed  CAS  Google Scholar 

  69. Mainwaring, D. E. et al. The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale 8, 6527–6534 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Pogodin, S. et al. Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys. J. 104, 835–840 (2013). This is a theoretical demonstration of the biophysical principles underpinning the mechanism of the mechanical rupture of bacteria on nanostructured surfaces.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Xue, F., Liu, J., Guo, L., Zhang, L. & Li, Q. Theoretical study on the bactericidal nature of nanopatterned surfaces. J. Theor. Biol. 385, 1–7 (2015).

    Article  CAS  PubMed  Google Scholar 

  72. Li, X. Bactericidal mechanism of nanopatterned surfaces. Phys. Chem. Chem. Phys. 18, 1311–1316 (2016).

    Article  CAS  PubMed  Google Scholar 

  73. Arnoldi, M. et al. Bacterial turgor pressure can be measured by atomic force microscopy. Phys. Rev. E 62, 1034–1044 (2000).

    Article  CAS  Google Scholar 

  74. Deng, Y., Sun, M. & Shaevitz, J. W. Measuring peptidoglycan elasticity and stress-stiffening of live bacterial cells. Biophys. J. 100, 514a–515a (2011).

    Article  Google Scholar 

  75. Truong, V. K. et al. The susceptibility of Staphylococcus aureus CIP 65.8 and pseudomonas aeruginosa ATCC 9721 cells to the bactericidal action of nanostructured Calopteryx haemorrhoidalis damselfly wing surfaces. Appl. Microbiol. Biotechnol. 101, 4683–4690 (2017).

    Article  CAS  PubMed  Google Scholar 

  76. Bhadra, C. M. et al. Subtle variations in surface properties of black silicon surfaces influence the degree of bactericidal efficiency. Nano-Micro Lett. 10, 36 (2018).

  77. Dickson, M. N., Liang, E. I., Rodriguez, L. A., Vollereaux, N. & Yee, A. F. Nanopatterned polymer surfaces with bactericidal properties. Biointerphases 10, 021010 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Diu, T. et al. Cicada-inspired cell-instructive nanopatterned arrays. Sci. Rep. 4, 7122 (2014).

  79. Modaresifar, K. et al. Deciphering the roles of interspace and controlled disorder in the bactericidal properties of nanopatterns against Staphylococcus aureus. Nanomaterials 10, 347 (2020).

    Article  CAS  PubMed Central  Google Scholar 

  80. Michalska, M. et al. Tuning antimicrobial properties of biomimetic nanopatterned surfaces. Nanoscale https://doi.org/10.1039/C8NR00439K (2018).

    Article  PubMed  Google Scholar 

  81. Modaresifar, K., Azizian, S., Ganjian, M., Fratila-Apachitei, L. E. & Zadpoor, A. A. Bactericidal effects of nanopatterns: a systematic review. Acta Biomater. 83, 29–36 (2018). This is a systematic review of the reported mechano-bactericidal nanopatterns.

    Article  PubMed  CAS  Google Scholar 

  82. Linklater, D. P., Nguyen, H. K. D., Bhadra, C. M., Juodkazis, S. & Ivanova, E. P. Influence of nanoscale topology on bactericidal efficiency of black silicon surfaces. Nanotechnology 28, 245301 (2017).

    Article  PubMed  CAS  Google Scholar 

  83. Nguyen, D. H. K. et al. The idiosyncratic self-cleaning cycle of bacteria on regularly arrayed mechano-bactericidal nanostructures. Nanoscale 11, 16455–16462 (2019).

    Article  CAS  PubMed  Google Scholar 

  84. Bauchau, O. A. & Craig, J. I. in Structural Analysis 173–221 (Springer, 2009).

  85. Linklater, D. P. et al. High aspect ratio nanostructures kill bacteria via storage and release of mechanical energy. ACS Nano 12, 6657–6667 (2018). This article reveals the role of pillar elasticity in the mechano-bactericidal action of high-aspect-ratio surface structures.

    Article  CAS  PubMed  Google Scholar 

  86. Pogodin, S. & Baulin, V. A. Can a carbon nanotube pierce through a phospholipid bilayer? ACS Nano 4, 5293–5300 (2010).

    Article  CAS  PubMed  Google Scholar 

  87. Ivanova, E. P. et al. A new facet to the mechano-bactericidal mechanism of nanostructured surfaces. Proc. Natl Acad. Sci. USA 117, 12598–12605 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Bhadra, C. M. et al. Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci. Rep. 5, 16817 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Wandiyanto, J. et al. Outsmarting superbugs: bactericidal activity of nanostructured titanium surfaces against methicillin- and gentamicin-resistant Staphylococcus aureus ATCC 33592. J. Mater. Chem. B 7, 4424–4431 (2019).

    Article  CAS  Google Scholar 

  90. Reed, J. H. et al. Ultrascalable multifunctional nanoengineered copper and aluminum for antiadhesion and bactericidal applications. ACS Appl. Bio. Mater. 2, 2726–2737 (2019).

    Article  CAS  PubMed  Google Scholar 

  91. Wang, X. et al. Electrophoresis deposited mesoporous graphitic carbon nitride surfaces with efficient bactericidal properties. ACS Appl. Bio. Mater. 3, 2255–2262 (2020).

    Article  CAS  PubMed  Google Scholar 

  92. Hu, W. et al. Graphene-based antibacterial paper. ACS Nano 4, 4317–4323 (2010).

    Article  CAS  PubMed  Google Scholar 

  93. Liu, S. et al. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5, 6971–6980 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Akhavan, O. & Ghaderi, E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4, 5731–5736 (2010). Graphene oxide nanowalls are observed to kill bacteria through direct membrane contact.

    Article  CAS  PubMed  Google Scholar 

  95. Farid, M. U., Guo, J. & An, A. K. Bacterial inactivation and in situ monitoring of biofilm development on graphene oxide membrane using optical coherence tomography. J. Membr. Sci. 564, 22–34 (2018).

    Article  CAS  Google Scholar 

  96. Perreault, F., de Faria, A. F., Nejati, S. & Elimelech, M. Antimicrobial properties of graphene oxide nanosheets: why size matters. ACS Nano 9, 7226–7236 (2015).

    Article  CAS  PubMed  Google Scholar 

  97. Sengupta, I. et al. Bactericidal effect of graphene oxide and reduced graphene oxide: influence of shape of bacteria. Colloid Interface Sci. Commun. 28, 60–68 (2019).

    Article  CAS  Google Scholar 

  98. Chen, J. et al. Graphene oxide exhibits broad-spectrum antimicrobial activity against bacterial phytopathogens and fungal conidia by intertwining and membrane perturbation. Nanoscale 6, 1879–1889 (2014).

    Article  CAS  PubMed  Google Scholar 

  99. Linklater, D. P., Baulin, V. A., Juodkazis, S. & Ivanova, E. P. Mechano-bactericidal mechanism of graphene nanomaterials. Interface Focus. 8, 20170060 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Pham, V. T. H. et al. Graphene induces formation of pores that kill spherical and rod-shaped bacteria. ACS Nano 9, 8458–8467 (2015). This article demonstrates the formation of pores in bacterial membranes by vertically oriented graphene nanosheets.

    Article  CAS  PubMed  Google Scholar 

  101. Yi, X. & Gao, H. Cell interaction with graphene microsheets: near-orthogonal cutting versus parallel attachment. Nanoscale 7, 5457–5467 (2015).

    Article  CAS  PubMed  Google Scholar 

  102. Tan, K. H. et al. Thermoresponsive amphiphilic functionalization of thermally reduced graphene oxide to study graphene/bacteria hydrophobic interactions. Langmuir 35, 4736–4746 (2019).

    Article  CAS  PubMed  Google Scholar 

  103. Lu, X. et al. Enhanced antibacterial activity through the controlled alignment of graphene oxide nanosheets. Proc. Natl Acad. Sci. USA 114, E9793–E9801 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Pandit, S. et al. Precontrolled alignment of graphite nanoplatelets in polymeric composites prevents bacterial attachment. Small 16, 1904756 (2020).

    Article  CAS  Google Scholar 

  105. Ivanova, E. P. et al. Bactericidal activity of self-assembled palmitic and stearic fatty acid crystals on highly ordered pyrolytic graphite. Acta Biomater. 59, 148–157 (2017).

    Article  CAS  PubMed  Google Scholar 

  106. Gonzalez Arellano, D. L. et al. Gecko-inspired biocidal organic nanocrystals initiated from a pencil-drawn graphite template. Sci. Rep. 8, 11618 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Guo, Y., Werner, M., Seemann, R., Baulin, V. A. & Fleury, J.-B. Tension-induced translocation of an ultrashort carbon nanotube through a phospholipid bilayer. ACS Nano 12, 12042–12049 (2018).

    Article  CAS  PubMed  Google Scholar 

  108. Ziegler, N. et al. Glancing-angle deposition of nanostructures on an implant material surface. Nanomaterials 9, 60 (2019).

    Article  PubMed Central  CAS  Google Scholar 

  109. Wandiyanto, J. V. et al. Tunable morphological changes of asymmetric titanium nanosheets with bactericidal properties. J. Colloid Interface Sci. 560, 572–580 (2020).

    Article  CAS  PubMed  Google Scholar 

  110. Luo, Y. et al. Anti‐infective application of graphene‐like silicon nanosheets via membrane destruction. Adv. Healthc. Mater. 9, 1901375 (2020). This article demonstrates the excellent in vivo performance of nanostructured silicon for mitigation of implant-related infections.

    Article  CAS  Google Scholar 

  111. Trichet, L. et al. Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. Proc. Natl Acad. Sci. USA 109, 6933–6938 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Pham, V. T. H. et al. “Race for the surface”: eukaryotic cells can win. ACS Appl. Mater. Interfaces 8, 22025–22031 (2016). This article demonstrates the promotion of eukaryotic cell attachment and proliferation on mechano-bactericidal surfaces pre-infected with bacteria.

    Article  CAS  PubMed  Google Scholar 

  113. Sjöström, T. et al. Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. Acta Biomater. 5, 1433–1441 (2009).

    Article  PubMed  CAS  Google Scholar 

  114. Wilkinson, C. D. W., Riehle, M., Wood, M., Gallagher, J. & Curtis, A. S. G. The use of materials patterned on a nano- and micro-metric scale in cellular engineering. Mater. Sci. Eng. C. 19, 263–269 (2002).

    Article  Google Scholar 

  115. Driscoll, M. K., Sun, X., Guven, C., Fourkas, J. T. & Losert, W. Cellular contact guidance through dynamic sensing of nanotopography. ACS Nano 8, 3546–3555 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Cavalcanti-Adam, E. A. et al. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92, 2964–2974 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Tsimbouri, P. et al. Nanotopographical effects on mesenchymal stem cell morphology and phenotype. J. Cell. Biochem. 115, 380–390 (2013).

    Article  CAS  Google Scholar 

  118. Biggs, M. J. P. et al. The use of nanoscale topography to modulate the dynamics of adhesion formation in primary osteoblasts and Erk/Mapk signalling in Stro-1+ enriched skeletal stem cells. Biomaterials 30, 5094–5103 (2009).

    Article  CAS  PubMed  Google Scholar 

  119. Biggs, M. J. P., Richards, R. G. & Dalby, M. J. Nanotopographical modification: a regulator of cellular function through focal adhesions. Nanomedicine 6, 619–633 (2010).

    Article  CAS  PubMed  Google Scholar 

  120. Jahed, Z. et al. Cell responses to metallic nanostructure arrays with complex geometries. Biomaterials 35, 9363–9371 (2014).

    Article  CAS  PubMed  Google Scholar 

  121. Bucaro, M. A., Vasquez, Y., Hatton, B. D. & Aizenberg, J. Fine-tuning the degree of stem cell polarization and alignment on ordered arrays of high-aspect-ratio nanopillars. ACS Nano 6, 6222–6230 (2012).

    Article  CAS  PubMed  Google Scholar 

  122. Brammer, K. S., Choi, C., Frandsen, C. J., Oh, S. & Jin, S. Hydrophobic nanopillars initiate mesenchymal stem cell aggregation and osteo-differentiation. Acta Biomater. 7, 683–690 (2011).

    Article  CAS  PubMed  Google Scholar 

  123. Wang, Q., Huang, Y. & Qian, Z. Nanostructured surface modification to bone implants for bone regeneration. J. Biomed. Nanotechnol. 14, 628–648 (2018).

    Article  CAS  PubMed  Google Scholar 

  124. Hao, J. et al. Biological and mechanical effects of micro-nanostructured titanium surface on an osteoblastic cell line in vitro and osteointegration in vivo. Appl. Biochem. Biotechnol. 183, 280–292 (2017).

    Article  CAS  PubMed  Google Scholar 

  125. Ravanetti, F. et al. Osteogenic response and osteoprotective effects in vivo of a nanostructured titanium surface with antibacterial properties. J. Mater. Sci. Mater. Med. 27 (2016).

  126. Vassallo, E. et al. Bactericidal performance of nanostructured surfaces by fluorocarbon plasma. Mater. Sci. Eng. C. 80, 117–121 (2017).

    Article  CAS  Google Scholar 

  127. Hasan, J., Jain, S. & Chatterjee, K. Nanoscale topography on black titanium imparts multi-biofunctional properties for orthopedic applications. Sci. Rep. 7, 41118 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Wu, S., Zuber, F., Brugger, J., Maniura-Weber, K. & Ren, Q. Antibacterial Au nanostructured surfaces. Nanoscale 8, 2620–2625 (2016).

    Article  CAS  PubMed  Google Scholar 

  129. Yuan, Y. & Zhang, Y. Enhanced biomimic bactericidal surfaces by coating with positively-charged ZIF nano-dagger arrays. Nanomedicine 13, 2199–2207 (2017).

    Article  CAS  PubMed  Google Scholar 

  130. Wu, S., Zuber, F., Maniura-Weber, K., Brugger, J. & Ren, Q. Nanostructured surface topographies have an effect on bactericidal activity. J. Nanobiotechnol. 16 (2018).

  131. Cao, Y. et al. Nanostructured titanium surfaces exhibit recalcitrance towards Staphylococcus epidermidis biofilm formation. Sci. Rep. 8 (2018).

  132. Hizal, F. et al. Impact of 3D hierarchical nanostructures on the antibacterial efficacy of a bacteria-triggered self-defensive antibiotic coating. ACS Appl. Mater. Interfaces 7, 20304–20313 (2015).

    Article  CAS  PubMed  Google Scholar 

  133. Hasan, J., Raj, S., Yadav, L. & Chatterjee, K. Engineering a nanostructured “super surface” with superhydrophobic and superkilling properties. RSC Adv. 5, 44953–44959 (2015).

    Article  CAS  PubMed  Google Scholar 

  134. Yick, S. et al. The effects of plasma treatment on bacterial biofilm formation on vertically-aligned carbon nanotube arrays. RSC Adv. 5, 5142–5148 (2015).

    Article  CAS  Google Scholar 

  135. Guo, Z.-G., Liu, W.-M. & Su, B.-L. A stable lotus-leaf-like water-repellent copper. Appl. Phys. Lett. 92, 063104 (2008).

    Article  CAS  Google Scholar 

  136. Li, X. et al. Dual-biomimetic superhydrophobic electrospun polystyrene nanofibrous membranes for membrane distillation. ACS Appl. Mater. Interfaces 6, 2423–2430 (2014).

    Article  CAS  PubMed  Google Scholar 

  137. Chaudhary, A. & Barshilia, H. C. Nanometric multiscale rough CuO/Cu(OH)2 superhydrophobic surfaces prepared by a facile one-step solution-immersion process: transition to superhydrophilicity with oxygen plasma treatment. J. Phys. Chem. C. 115, 18213–18220 (2011).

    Article  CAS  Google Scholar 

  138. Li, Y., Jia, W.-Z., Song, Y.-Y. & Xia, X.-H. Superhydrophobicity of 3D porous copper films prepared using the hydrogen bubble dynamic template. Chem. Mater. 19, 5758–5764 (2007).

    Article  CAS  Google Scholar 

  139. Li, Y., Lee, E. J. & Cho, S. O. Superhydrophobic coatings on curved surfaces featuring remarkable supporting force. J. Phys. Chem. C. 111, 14813–14817 (2007).

    Article  CAS  Google Scholar 

  140. Sun, M. et al. Artificial lotus leaf by nanocasting. Langmuir 21(19), 8978–8981 (2005).

    Article  CAS  PubMed  Google Scholar 

  141. Tu, Y. et al. Destructive extraction of phospholipids from Escherichia coli membranes by graphene Nanosheets. Nat. nanotechnol. 8, 594–601 (2013).

    Article  CAS  PubMed  Google Scholar 

  142. Zhang et al. Rapidly probing antibacterial activity of graphene oxide by mass spectrometry-based metabolite fingerprinting. Sci. Rep. 6, 28045 (2015).

    Article  CAS  Google Scholar 

  143. Chrcanovic, B. R., Pedrosa, A. R. & Martins, M. D. Chemical and topographic analysis of treated surfaces of five different commercial dental titanium implants. Mater. Res. 15, 372–382 (2012).

    Article  CAS  Google Scholar 

  144. Ganjian, M. et al. Nature helps: toward bioinspired bactericidal nanopatterns. Adv. Mater. Interfaces https://doi.org/10.1002/admi.201900640 (2019).

  145. Loya, M. C., Brammer, K. S., Choi, C., Chen, L.-H. & Jin, S. Plasma-induced nanopillars on bare metal coronary stent surface for enhanced endothelialization. Acta Biomater. 6, 4589–4595 (2010).

    Article  CAS  PubMed  Google Scholar 

  146. Sekiguchi, H. et al. Fabrication and optical properties of regularly arranged GaN-based nanocolumns on Si substrate. J. Vac. Sci. Technol. B 37, 031207 (2019).

    Article  CAS  Google Scholar 

  147. Peng, K. et al. Aligned single-crystalline Si nanowire arrays for photovoltaic applications. Small 1, 1062–1067 (2005).

  148. Green, D. W. et al. High quality bioreplication of intricate nanostructures from a Fragile Gecko skin surface with bactericidal properties. Sci. Rep. 7 (2017).

  149. Yu, R. et al. Strong light absorption of self-organized 3-D nanospike arrays for photovoltaic applications. ACS Nano 5, 9291–9298 (2011).

    Article  CAS  PubMed  Google Scholar 

  150. Zhu, J. et al. Optical absorption enhancement in amorphous silicon nanowire and nanocone arrays. Nano Lett. 9, 279–282 (2009).

    Article  PubMed  CAS  Google Scholar 

  151. Hermansson, M. The DLVO theory in microbial adhesion. Colloids Surf. B Biointerfaces 14, 105–119 (1999).

    Article  CAS  Google Scholar 

  152. Dickinson, R. B., Clapp, A. R. & Truesdail, S. E. in Handbook of Bacterial Adhesion (eds An, Y. H. & Friedman, R. J.) 297–306 (Humana Press, 2000).

  153. Chen, Y., Harapanahalli, A. K., Busscher, H. J., Norde, W. & van der Mei, H. C. Nanoscale cell wall deformation impacts long-range bacterial adhesion forces on surfaces. Appl. Environ. Microbiol. 80, 637–643 (2013).

    Article  PubMed  CAS  Google Scholar 

  154. Yadav, A. K., Espaillat, A. & Cava, F. Bacterial strategies to preserve cell wall integrity against environmental threats. Front. Microbiol. 9 (2018).

  155. Li, X. & Chen, T. Enhancement and suppression effects of a nanopatterned surface on bacterial adhesion. Phys. Rev. E 93 (2016).

  156. Xie, X. et al. Mechanical model of vertical nanowire cell penetration. Nano Lett. 13, 6002–6008 (2013).

    Article  CAS  PubMed  Google Scholar 

  157. Werner, M., Sommer, J.-U. & Baulin, V. A. Homo-polymers with balanced hydrophobicity translocate through lipid bilayers and enhance local solvent permeability. Soft Matter 8, 11714 (2012).

    Article  CAS  Google Scholar 

  158. Pogodin, S., Slater, N. K. H. & Baulin, V. A. Surface patterning of carbon nanotubes can enhance their penetration through a phospholipid bilayer. ACS Nano 5, 1141–1146 (2011).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Funding from the Australian Research Council (ARC) Industrial Transformation Research Hubs scheme (project number IH130100017) and the ARC Industrial Transformation Training Centre scheme (project number IC180100005) to E.P.I. and NIH grant R01GM124436 to P.S. are gratefully acknowledged.

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Authors and Affiliations

  1. Optical Sciences Centre, School of Science, Swinburne University of Technology, Hawthorn, VIC, Australia

    Denver P. Linklater & Saulius Juodkazis

  2. ARC Industrial Transformation Training Centre in Surface Engineering for Advanced Materials, School of Science, Swinburne University of Technology, Hawthorn, VIC, Australia

    Denver P. Linklater, Russell J. Crawford & Elena P. Ivanova

  3. School of Science, RMIT University, Melbourne, VIC, Australia

    Denver P. Linklater

  4. Department of Chemical Engineering, Rovira i Virgili University, Tarragona, Spain

    Vladimir A. Baulin

  5. Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH, USA

    Paul Stoodley

  6. Department of Orthopaedics, The Ohio State University, Columbus, OH, USA

    Paul Stoodley

  7. National Centre of Advanced Tribology at Southampton (nCATS), National Biofilms Innovation Centre (NBIC), Department of Mechanical Engineering, University of Southampton, Southampton, UK

    Paul Stoodley

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  1. Denver P. Linklater
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Contributions

D.P.L. and E.P.I. researched data for the article. P.S., D.P.L., S.J., V.A.B., R.J.C. and E.P.I. substantially contributed to discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Paul Stoodley or Elena P. Ivanova.

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Related links

Biophysical model of the cicada wing nanopillar-bacterial cell interactions: https://www.youtube.com/watch?v=KSdMYX4gqp8

Supplementary information

Glossary

Antibiofouling

Describes specially designed materials and coatings to prevent or remove biofouling by any number of organisms on wetted surfaces.

Hydrophobic

The physical property of having no affinity with water (that is, water repellent).

Bactericidal

Destroys bacteria.

Biocidal

The action of a chemical substance or microorganism to destroy a harmful organism or to prevent or control its effects.

Osseointegration

Functional bone adherence to the implant surface.

Osseoconduction

Guiding the reparative growth of the natural bone.

Micro–nanostructuring

A technique used to impart physical patterns onto a surface with surface features (protrusions or depressions) on the scale of micrometres or nanometres. The size and shapes of such patterns determine the overall topography of the surface at these scales. Such patterns can be made by depositing material onto a surface, removing material from a surface, or both.

Nanotopographies

The specific surface features that form or are generated at the nanoscale.

Surface roughness

Irregularities of the surface, either random or repetitive, that make up the 3D topography of the surface.

Nanoscale

Physical dimensions less than 1 μm.

Mechano-bactericidal

The action of natural or synthetic nanomaterials that can physically induce bacterial cell death through the application of physical forces.

Hydrophilic

The physical property of a molecule and/or surface the interactions of which with water are thermodynamically favourable; that is, it can form ionic or hydrogen bonds with water.

Microscale

Physical dimensions less than 1 mm.

Stretching modulus

Also known as Young’s modulus. The modulus of elasticity: a measure of the ability of a material to withstand changes in length when under lengthwise tension or compression.

Turgor pressure

The force (hydrostatic pressure) within the cell, caused by the osmotic flow of water, that pushes the cell membrane against the cell wall.

Biomimetic

Imitating the models, systems and elements found in nature.

Aspect ratio

The ratio of feature width to feature height. ‘High aspect ratio’ refers to a structure that is exceedingly tall in comparison with its width.

Cytotoxic

Causing cell damage or death.

Lipophilicity

The degree to which an organic molecule can dissolve in fat, oil or other non-polar solvents.

Amphiphilicity

The physical property of a molecule or compound that possesses both hydrophilic (water-loving) and hydrophobic (water-repellent) characteristics.

Biomaterials

Engineered substances that can be introduced into body tissues as part of an implanted medical, therapeutic or diagnostic device.

Biocompatibility

The ability of a biomaterial to perform its desired function without eliciting detrimental local or systemic effects when implanted within the body.

Cytocompatibility

Supportive of the common functions of all cells, including basal functions such as viability and proliferation as well as functions specific to the phenotype of each cell type defined by morphology of the cytoskeleton and expression of proteins and specific enzymes.

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Linklater, D.P., Baulin, V.A., Juodkazis, S. et al. Mechano-bactericidal actions of nanostructured surfaces. Nat Rev Microbiol 19, 8–22 (2021). https://doi.org/10.1038/s41579-020-0414-z

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