Abstract
The nanopattern on the surface of Clanger cicada (Psaltoda claripennis) wings represents the first example of a new class of biomaterials that can kill bacteria on contact based solely on its physical surface structure. As such, they provide a model for the development of novel functional surfaces that possess an increased resistance to bacterial contamination and infection. Their effectiveness against a wide spectrum of bacteria, however, is yet to be established. Here, the bactericidal properties of the wings were tested against several bacterial species, possessing a range of combinations of morphology and cell wall type. The tested species were primarily pathogens, and included Bacillus subtilis, Branhamella catarrhalis, Escherichia coli, Planococcus maritimus, Pseudomonas aeruginosa, Pseudomonas fluorescens, and Staphylococcus aureus. The wings were found to consistently kill Gram-negative cells (i.e., B. catarrhalis, E. coli, P. aeruginosa, and P. fluorescens), while Gram-positive cells (B. subtilis, P. maritimus, and S. aureus) remained resistant. The morphology of the cells did not appear to play any role in determining cell susceptibility. The bactericidal activity of the wing was also found to be quite efficient; 6.1 ± 1.5 × 106 P. aeruginosa cells in suspension were inactivated per square centimeter of wing surface after 30-min incubation. These findings demonstrate the potential for the development of selective bactericidal surfaces incorporating cicada wing nanopatterns into the design.
Similar content being viewed by others
References
Bhushan B, Jung YC (2011) Natural and biomimetic artificial surfaces for superhydrophobicity, self-cleaning, low adhesion, and drag reduction. Prog Mater Sci 56:1–108
Choi CH, Kim CJ (2006) Fabrication of a dense array of tall nanostructures over a large sample area with sidewall profile and tip sharpness control. Nanotechnology 17:5326–5333
Díaz C, Schilardi PL, Salvarezza RC, De Mele MFL (2007) Nano/microscale order affects the early stages of biofilm formation on metal surfaces. Langmuir 23:11206–11210
Díaz C, Schilardi PL, dos Santos Claro PC, Salvarezza RC, Fernández Lorenzo de Mele MA (2009) Submicron trenches reduce the Pseudomonas fluorescens colonization rate on solid surfaces. ACS Appl Mater Interfaces 1:136–143
Díaz C, Salvarezza RC, Fernández Lorenzo De Mele MA, Schilardi PL (2010) Organization of Pseudomonas fluorescens on chemically different nano/microstructured surfaces. ACS Appl Mater Interfaces 2:2530–2539
Díaz C, Fernández Lorenzo De Mele MA, Schilardi PL (2011) Comment on “the interaction of cells and bacteria with surfaces structured at the nanometre scale”. Acta Biomater 7:1934–1935
Epstein AK, Wong TS, Belisle RA, Boggs EM, Aizenberg J (2012) Liquid-infused structured surfaces with exceptional anti-biofouling performance. Proc Natl Acad Sci USA 109:13182–13187
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 27:3012–3019
Food and Drug Administration (FDA) (2009) Microbiological challenge testing, evaluation and definition of potentially hazardous foods. Accessed 25 Oct 2012.
Food and Drug Administration (FDA), Center for Food Safety and Applied Nutrition (2001) The “Bad Bug Book” [Foodborne pathogenic microorganisms and natural toxins handbook]. http://www.cfsan.fda.gov/~mow/intro.html. Accessed 10 Dec 2001.
Green DW, Watson GS, Watson J, Abraham SJK (2012) New biomimetic directions in regenerative ophthalmology. Adv Healthcare Mater 1:140–148
Guo Z, Liu W, Su B-L (2011) Superhydrophobic surfaces: from natural to biomimetic to functional. J Colloid Interf Sci 353:335–355
Harbarth S, Cosgrove S, Carmeli Y (2002) Effects of antibiotics on nosocomial epidemiology of vancomycin-resistant enterococci. Antimicrob Agents Chemother 46:1619–1628
Harris AD, Furuno JP, Roghmann M-C, Johnson JK, Conway LJ, Venezia RA, Standiford HC, Schweizer ML, Hebden JN, Moore AC, Perencevich EN (2010) Targeted surveillance of Methicillin-resistant Staphylococcus aureus and its potential use to guide empiric antibiotic therapy. Antimicrob Agents Chemother 54:3143–3148
Hook AL, Chang CY, Yang J, Luckett J, Cockayne A, Atkinson S, Mei Y, Bayston R, Irvine DJ, Langer R, Anderson DG, Williams P, Davies MC, Alexander MR (2012) Combinatorial discovery of polymers resistant to bacterial attachment. Nat Biotech 30:868–875
Ivanova EP, Hasan J, Webb HK, Truong VK, Watson GS, Watson JA, Baulin VA, Pogodin S, Wang JY, Tobin MJ, Löbbe C, Crawford RJ (2012) Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa by cicada wings. Small 8:2489–2494
Kietzig AM, Hatzikiriakos SG, Englezos P (2009) Patterned superhydrophobic metallic surfaces. Langmuir 25:4821–4827
Koch K, Bhushan B, Barthlott W (2008) Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4:1943–1963
Kostovski G, Chinnasamy U, Jayawardhana S, Stoddart PR, Mitchell A (2010) Sub-15 nm optical fiber nanoimprint lithography: a parallel, self-aligned and portable approach. Adv Mater 23:531–535
Lim H, Jund DH, Noh JH, Choi GR, Kim WD (2009) Simple nanofabrication of a superhydrophobic and transparent biomimetic surface. Chin Sci Bull 54:3613–3616
Marmur A (2004) The lotus effect: superhydrophobicity and metastability. Langmuir 20:3517–3519
Mischensko L, Hatton B, Bahadur V, Taylor JA, Krupenkin T, Aizenberg J (2010) Design of ice-free nanostructured surfaces based on repulsion of impacting water droplets. ACS Nano 4:7699–7707
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 58:268–273
Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA (2007) Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 51:3471–3484
Postgate JR (1969) Viable counts and viability. Methods Microbiol 1:611–628
Rubin RJ, Harrington CA, Poon A, Dietrich K, Greene JA, Moiduddin A (1999) The economic impact of Staphylococcus aureus infection in New York City hospitals. Emerg Infect Dis 5:9–17
Schierholz JM, Lucas LJ, Rump A, Pulverer G (1998) Efficacy of silver coated medical devices. J Hosp Infect 40:257–262
Shamis Y, Patel S, Taube A, Morsi Y, Sbarski I, Shramkov Y, Croft RJ, Crawford RJ, Ivanova EP (2009) A new sterilization technique of bovine pericardial biomaterial using microwave radiation. Tissue Eng Part C Methods 15:445–454
Shao W, Zhao Q (2010) Influence of reducers on nanostructure and surface energy of silver coatings and bacterial adhesion. Surf Coat Technol 204:1288–1294
Stamm LV (2010) Global challenge of antibiotic-resistant Treponema pallidum. Antimicrob Agents Chemother 54:583–589
Su Y, Ji B, Huang Y, Hwang K-C (2010) Nature’s design of hierarchical superhydrophobic surfaces of a water strider for low adhesion and low-energy dissipation. Langmuir 26:18926–18937
Tiller JC, Liao C-J, Lewis K, Klibanov AM (2001) Designing surfaces that kill bacteria on contact. Proc Natl Acad Sci USA 98:5981–5985
Truong VK, Rundell S, Lapovok R, Estrin Y, Wang JY, Berndt CC, Barnes DG, Fluke CJ, Crawford RJ, Ivanova EP (2009) Effect of ultrafine-grained titanium surfaces on adhesion of bacteria. Appl Microbiol Biot 83:925–937
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 31:3674–3683
Webb HK, Hasan J, Truong VK, Crawford RJ, Ivanova EP (2011) Nature inspired structured surfaces for biomedical applications. Curr Med Chem 18:3367–3375
Zhang G, Zhang J, Xie G, Liu Z, Shao H (2006) Cicada wings: a stamp from nature for nanoimprint lithography. Small 2:1440–1443
Acknowledgments
This research was funded in part by the Advanced Manufacturing Cooperative Research Centre.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hasan, J., Webb, H.K., Truong, V.K. et al. Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol 97, 9257–9262 (2013). https://doi.org/10.1007/s00253-012-4628-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-012-4628-5