Advertisement

Applied Microbiology and Biotechnology

, Volume 101, Issue 11, pp 4683–4690 | Cite as

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

  • Vi Khanh Truong
  • Nipuni Mahanamanam Geeganagamage
  • Vladimir A. Baulin
  • Jitraporn Vongsvivut
  • Mark J. Tobin
  • Pere Luque
  • Russell J. Crawford
  • Elena P. Ivanova
Applied microbial and cell physiology

Abstract

Nanostructured insect wing surfaces have been reported to possess the ability to resist bacterial colonization through the mechanical rupture of bacterial cells coming into contact with the surface. In this work, the susceptibility of physiologically young, mature and old Staphylococcus aureus CIP 65.8 and Pseudomonas aeruginosa ATCC 9721 bacterial cells, to the action of the bactericidal nano-pattern of damselfly Calopteryx haemorrhoidalis wing surfaces, was investigated. The results were obtained using several surface characterization techniques including optical profilometry, scanning electron microscopy, synchrotron-sourced Fourier transform infrared microspectroscopy, water contact angle measurements and antibacterial assays. The data indicated that the attachment propensity of physiologically young S. aureus CIP 65.8T and mature P. aeruginosa ATCC 9721 bacterial cells was greater than that of the cells at other stages of growth. Both the S. aureus CIP 65.8T and P. aeruginosa ATCC 9721 cells, grown at the early (1 h) and late stationary phase (24 h), were found to be most susceptible to the action of the wings, with up to 89.7 and 61.3% as well as 97.9 and 97.1% dead cells resulting from contact with the wing surface, respectively.

Keywords

Black damselfly Calopteryx haemorrhoidalis Nanopillar arrays Bactericidal Physiological growth 

Notes

Acknowledgments

We gratefully acknowledge funding from the Marie Curie Actions research program under the EU FP7 Initial Training Network SNAL 608184. This research was undertaken on the Infrared Microscopectroscopy beamline at the Australian Synchrotron, Victoria, Australia.

Compliance with ethical standards

Human and animal rights and informed consent

This paper does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no competing conflict of interest.

Supplementary material

253_2017_8205_MOESM1_ESM.pdf (862 kb)
ESM 1 (PDF 861 kb)

References

  1. Andersen SO (1979) Biochemistry of insect cuticle. Annu Rev Entomol 24:29–61. doi: 10.1146/annurev.en.24.010179.000333 CrossRefGoogle Scholar
  2. Ashton JL (1921) A revision of the Australian Cicadidae: part 1. Proc Roy Soc Victoria 33:87–107Google Scholar
  3. Bruinsma GM, Rustema-Abbing M, Van Der Mei HC, Busscher HJ (2001) Effects of cell surface damage on surface properties and adhesion of Pseudomonas aeruginosa. J Microbiol Methods 45(2):95–101. doi: 10.1016/S0167-7012(01)00238-X CrossRefPubMedGoogle Scholar
  4. Chandran R, Williams L, Hung A, Nowlin K, LaJeunesse D (2016) SEM characterization of anatomical variation in chitin organization in insect and arthropod cuticles. Micron 82:74–85. doi: 10.1016/j.micron.2015.12.010 CrossRefPubMedGoogle Scholar
  5. Córdoba-Aguilar A (2003) A description of male and female genitalia and a reconstruction of copulatory and fertilisation events in Calopteryx haemorrhoidalis (Vander Linden) (Odonata: Calopterygidae). Odonatologica 32(3):205–214Google Scholar
  6. Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113(6):767–776. doi: 10.1016/S0092-8674(03)00421-5 CrossRefPubMedGoogle Scholar
  7. Egan AJ, Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8–28. doi: 10.1111/j.1749-6632.2012.06818.x CrossRefPubMedGoogle Scholar
  8. Hasan J, Webb HK, Truong VK, Watson GS, Watson JA, Tobin MJ, Gervinskas G, Juodkazis S, Wang JY, Crawford RJ, Ivanova EP (2012) Spatial variations and temporal metastability of the self-cleaning and superhydrophobic properties of damselfly wings. Langmuir 28(50):17404–17409. doi: 10.1021/la303560w CrossRefPubMedGoogle Scholar
  9. Hasan J, Webb HK, Truong VK, Pogodin S, Baulin VA, Watson GS, Watson JA, Crawford RJ, Ivanova EP (2013) Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol 97(20):9257–9262. doi: 10.1007/s00253-012-4628-5 CrossRefPubMedGoogle Scholar
  10. 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 cells by cicada wings. Small 8(16):2489–2494. doi: 10.1002/smll.201200528 CrossRefPubMedGoogle Scholar
  11. Ivanova EP, Hasan J, Webb HK, Gervinskas G, Juodkazis S, Truong VK, Wu AH, Lamb RN, Baulin VA, Watson GS, Watson JA, Mainwaring DE, Crawford RJ (2013a) Bactericidal activity of black silicon. Nat Comm 4:2838. doi: 10.1038/ncomms3838 CrossRefGoogle Scholar
  12. Ivanova EP, Nguyen SH, Webb HK, Hasan J, Truong VK, Lamb RN, Duan X, Tobin MJ, Mahon PJ, Crawford RJ (2013b) Molecular organization of the nanoscale surface structures of the dragonfly Hemianax papuensis wing epicuticle. PLoS One 8(7):e67893. doi: 10.1371/journal.pone.0067893 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kelleher SM, Habimana O, Lawler J, O'Reilly B, Daniels S, Casey E, Cowley A (2016) Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl Mater Interfaces 8(24):14966–14974. doi: 10.1021/acsami.5b08309 CrossRefPubMedGoogle Scholar
  14. Koch AL (1990) Growth and form of the bacterial cell wall. Am Sci 78(4):327–341Google Scholar
  15. Li X, Cheung GS, Watson GS, Watson JA, Lin S, Schwarzkopf L, Green DW (2016) The nanotipped hairs of gecko skin and biotemplated replicas impair and/or kill pathogenic bacteria with high efficiency. Nanoscale 8(45):18860–18869. doi: 10.1039/c6nr05046h CrossRefPubMedGoogle Scholar
  16. Mainwaring DE, Nguyen SH, Webb H, Jakubov T, Tobin M, Lamb RN, Wu AHF, Marchant R, Crawford RJ, Ivanova EP (2016) The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale 8(12):6527–6534. doi: 10.1039/c5nr08542j CrossRefPubMedGoogle Scholar
  17. Nguyen SH, Webb HK, Hasan J, Tobin MJ, Crawford RJ, Ivanova EP (2013) Dual role of outer epicuticular lipids in determining the wettability of dragonfly wings. Colloids Surf B: Biointerfaces 106:126–134. doi: 10.1016/j.colsurfb.2013.01.042 CrossRefPubMedGoogle Scholar
  18. Nowlin K, Boseman A, Covell A, LaJeunesse D (2014) Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces. J R Soc Interface 12(102). doi: 10.1098/rsif.2014.0999
  19. Oikonomou CM, Jensen GJ (2016) A new view into prokaryotic cell biology from electron cryotomography. Nat Rev Microbiol 14(4):205–220. doi: 10.1038/nrmicro.2016.7 CrossRefPubMedGoogle Scholar
  20. 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. doi: 10.1016/j.bpj.2012.12.046 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Scheffers DJ, Pinho MG (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69(4):585–607. doi: 10.1128/MMBR.69.4.585-607.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36(4):407–477PubMedPubMedCentralGoogle Scholar
  23. Shockman GD, Barrett JF (1983) Structure, function and assembly of cell walls of Gram-positive bacteria. Annu Rev Microbiol 37:501–527. doi: 10.1146/annurev.mi.37.100183.002441 CrossRefPubMedGoogle Scholar
  24. Sun M, Watson GS, Zheng Y, Watson JA, Liang A (2009) Wetting properties on nanostructured surfaces of cicada wings. J Exp Biol 212(19):3148–3155. doi: 10.1242/jeb.033373 CrossRefPubMedGoogle Scholar
  25. Tobin MJ, Puskar L, Hasan J, Webb HK, Hirschmugl CJ, Nasse MJ, Gervinskas G, Juodkazis S, Watson GS, Watson JA, Crawford RJ, Ivanova EP (2013) High-spatial-resolution mapping of superhydrophobic cicada wing surface chemistry using infrared microspectroscopy and infrared imaging at two synchrotron beamlines. J Synchrotron Radiat 20(Pt 3):482–489. doi: 10.1107/S0909049513004056 CrossRefPubMedGoogle Scholar
  26. Tobin MJ, Puskar L, Nguyen SH, Hasan J, Webb HK, Hirschmugl CJ, Nasse MJ, Gervinskas G, Juodkazis S, Watson GS, Watson JA, Mainwaring DE, Mahon PJ, Marchant R, Crawford RJ, Ivanova EP (2015) Fourier transform infrared spectroscopy and imaging of dragonfly, damselfly and cicada wing membranes. Spectrosc Eur 27(4):15–18Google Scholar
  27. Vollmer W, Blanot D, de Pedro MA (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32(2):149–167. doi: 10.1111/j.1574-6976.2007.00094.x CrossRefPubMedGoogle Scholar
  28. Walker SL, Hill JE, Redman JA, Elimelech M (2005) Influence of growth phase on adhesion kinetics of Escherichia coli D21g. Appl Environ Microbiol 71(6):3093–3099. doi: 10.1128/AEM.71.6.3093-3099.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Watson GS, Green DW, Schwarzkopf L, Li X, Cribb BW, Myhra S, Watson JA (2015) A gecko skin micro/nano structure—a low adhesion, superhydrophobic, anti-wetting, self-cleaning, biocompatible, antibacterial surface. Acta Biomater 21:109–122. doi: 10.1016/j.actbio.2015.03.007 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Vi Khanh Truong
    • 1
  • Nipuni Mahanamanam Geeganagamage
    • 1
  • Vladimir A. Baulin
    • 2
  • Jitraporn Vongsvivut
    • 3
  • Mark J. Tobin
    • 3
  • Pere Luque
    • 4
  • Russell J. Crawford
    • 5
  • Elena P. Ivanova
    • 1
  1. 1.School of Science, Faculty of Science, Engineering and TechnologySwinburne University of TechnologyHawthornAustralia
  2. 2.Departament d’Enginyeria QuimicaUniversitat Rovira i VirgiliTarragonaSpain
  3. 3.Infrared Microspectroscopy Beamline, Australian SynchrotronClaytonAustralia
  4. 4.Museu de les Terres de l’EbreAmpostaSpain
  5. 5.School of Science, College of Science, Engineering and HealthRMIT UniversityMelbourneAustralia

Personalised recommendations