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Vanadium pentoxide nanoparticles mimic vanadium haloperoxidases and thwart biofilm formation

Nature Nanotechnology volume 7, pages 530–535 (2012)Cite this article

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Abstract

Marine biofouling—the colonization of small marine microorganisms on surfaces that are directly exposed to seawater, such as ships' hulls—is an expensive problem that is currently without an environmentally compatible solution1. Biofouling leads to increased hydrodynamic drag, which, in turn, causes increased fuel consumption and greenhouse gas emissions. Tributyltin-free antifouling coatings and paints1,2,3,4 based on metal complexes or biocides have been shown to efficiently prevent marine biofouling. However, these materials can damage5 the environment through metal leaching (for example, of copper and zinc)6 and bacteria resistance7. Here, we show that vanadium pentoxide nanowires act like naturally occurring vanadium haloperoxidases8 to prevent marine biofouling. In the presence of bromide ions and hydrogen peroxide, the nanowires catalyse the oxidation of bromide ions to hypobromous acid (HOBr). Singlet molecular oxygen (1O2) is formed and this exerts strong antibacterial activity, which prevents marine biofouling without being toxic to marine biota. Vanadium pentoxide nanowires have the potential to be an alternative approach to conventional anti-biofouling agents.

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Figure 1: Bactericidal properties of V2O5 nanowires.
Figure 2: TEM image of V2O5 nanowires and concentration dependence of their bromination activity.
Figure 3: Steady-state kinetics of the V2O5 nanowires at pH 8.3.
Figure 4: Representative digital images showing the influence of the catalytic activity of V2O5 nanowires on the growth of Gram-positive (S. aureus) and Gram-negative (E. coli) bacteria.
Figure 5: Application of V2O5 nanowires in paint with antibacterial/antifouling properties.
Figure 6: Effect of nanoparticles on biofouling in situ.

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References

  1. Banerjee, I., Pangule, R. C. & Kane, R. S. Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv. Mater. 23, 690–718 (2011).

    Article  CAS  Google Scholar 

  2. Messersmith, P. B. & Textor, M. Enzymes on nanotubes thwart fouling. Nature Nanotech. 2, 138–139 (2007).

    Article  CAS  Google Scholar 

  3. Chambers, L. D., Stokes, K. R., Walsh, F. C. & Wood, R. J. K. Modern approaches to marine antifouling coatings. Surf. Coat. Technol. 201, 3642–3652 (2006).

    Article  CAS  Google Scholar 

  4. Almeida, E., Diamantino, T. C. & Sousa, O. Marine paints: the particular case of antifouling paints. Prog. Org. Coat. 59, 2–20 (2007).

    Article  CAS  Google Scholar 

  5. Omae, I. General aspects of tin-free antifouling paints. Chem. Rev. 103, 3431–3448 (2003).

    Article  CAS  Google Scholar 

  6. Turley, P. A., Fenn, R. J. & Ritter, J. C. Pyrithiones as antifoulants: environmental chemistry and preliminary risk assessment. Biofouling 15, 175–182 (2000).

    Article  CAS  Google Scholar 

  7. Brozel, V. S., Pietersen, B. & Cloete, T. E. Resistance of bacterial cultures to nonoxidizing water-treatment bactericides by adaptation. Water Sci. Technol. 31, 169–175 (1995).

    Article  CAS  Google Scholar 

  8. Wever, R. & Hemrika, W. in Handbook of Metalloproteins (eds Messerschmidt, A., Huber, R., Poulos, T. & Wieghardt, K.) 1417–1428 (Wiley, 2001).

    Google Scholar 

  9. Rosenhahn, A., Schilp, S., Kreuzer, H. J. & Grunze, M. The role of ‘inert’ surface chemistry in marine biofouling prevention. Phys. Chem. Chem. Phys. 12, 4275–4286 (2010).

    Article  CAS  Google Scholar 

  10. Borchardt, S. A. et al. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67, 3174–3179 (2001).

    Article  CAS  Google Scholar 

  11. Wever, R., Tromp, M. G. M., Krenn, B. E., Marjani, A. & van Tol, M. Brominating activity of the seaweed Ascophyllum Nodosum: impact on the biosphere. Environ. Sci. Technol. 25, 446–449 (1991).

    Article  CAS  Google Scholar 

  12. Barnett, P., Hondmann, D., Simons, L. H., Ter Steeg, P. F. & Wever, R. Recombinant vanadium haloperoxidases and their uses. Patent WO/1995/027046 (1995).

  13. Wever, R., Dekker, H. L., Van Schijndel, J. W. P. M. & Vollenbroek, E. G. M. Antifouling Paint Containing Haloperoxidase and Method to Determine Halide. Patent WO/1995/027009 (1995).

  14. Weller, R. & Schrems, O. H2O2 in the marine troposphere and seawater of the Atlantic Ocean. Geophys. Res. Lett. 20, 125–128 (1993).

    Article  CAS  Google Scholar 

  15. Hasan, Z. et al. Laboratory evolved vanadium chloroperoxidase exhibits 100-fold higher halogenating activity at alkaline pH: catalytic effects from first and second coordination sphere mutations. J. Biol. Chem. 281, 9738–9744 (2006).

    Article  CAS  Google Scholar 

  16. Almeida, M. et al. Vanadium haloperoxidases from brown algae of the Laminariaceae Family. Phytochemistry 57, 633–642 (2001).

    Article  CAS  Google Scholar 

  17. Soedjak, H. S., Walker, J. V. & Butler, A. Inhibition and inactivation of vanadium bromoperoxidase by the substrate, hydrogen peroxide, and further mechanistic studies of vanadium bromoperoxidase. Biochemistry 34, 12689–12696 (1995).

    Article  CAS  Google Scholar 

  18. Crans, D. C., Smee, J. J., Gaidamauskas, E. & Yang, L. The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem. Rev. 104, 849–902 (2004).

    Article  CAS  Google Scholar 

  19. Mimoun, H. et al. Vanadium(V) peroxy complexes. New versatile biomimetic reagents for epoxidation of olefins and hydroxylation of alkanes and aromatic hydrocarbons. J. Am. Chem. Soc. 105, 3101–3110 (1983).

    Article  CAS  Google Scholar 

  20. De la Rosa, R. I., Clague, M. J. & Butler, A. A functional mimic of vanadium bromoperoxidase. J. Am. Chem. Soc. 114, 760–767 (1992).

    Article  CAS  Google Scholar 

  21. André, R. et al. V2O5 nanowires with an intrinsic peroxidase-like activity. Adv. Funct. Mater. 21, 501–509 (2011).

    Article  Google Scholar 

  22. De Boer, E. & Wever, R. The reaction mechanism of the novel vanadium bromoperoxidase. A steady-state kinetic analysis. J. Biol. Chem. 263, 12326–12332 (1988).

    CAS  Google Scholar 

  23. Butler, A. in Bioinorganic Catalysis 2nd edn (eds Reedijk, J. & Bouwman, E.) Ch. 5, 55–79 (Marcel Dekker, 1991).

    Google Scholar 

  24. Hemrika, W., Renirie, R., Dekker, H. L., Barnett, P. & Wever, R. From phosphatases to vanadium peroxidases: a similar architecture of the active site. Proc. Natl Acad. Sci. USA 94, 2145–2149 (1997).

    Article  CAS  Google Scholar 

  25. Shevelkova, A. N. & Ryabov, A. D. Irreversible inactivation of Caldariomyces fumago chloroperoxidase by hydrogen peroxide. IUBMB Life 39, 665–670 (1996).

    Article  CAS  Google Scholar 

  26. Butler, A., Clague, M. J. & Meister, G. E. Vanadium peroxide complexes. Chem. Rev. 94, 625–638 (1994).

    Article  CAS  Google Scholar 

  27. Colpas, G. J., Hamstra, B. J., Kampf, J. W. & Pecoraro, V. L. Functional models for vanadium haloperoxidase: reactivity and mechanism of halide oxidation. J. Am. Chem. Soc. 118, 3469–3478 (1996).

    Article  CAS  Google Scholar 

  28. De la Rosa, R. I., Clague, M. J. & Butler, A. A. Functional mimic of vanadium bromoperoxidase. J. Am. Chem. Soc. 114, 760–761 (1992).

    Article  CAS  Google Scholar 

  29. Ligtenbarg, A. G. J., Hage, R. & Feringa, B. L. Catalytic oxidations by vanadium complexes. Coord. Chem. Rev. 237, 89–101 (2003).

    Article  CAS  Google Scholar 

  30. Renirie, R. et al. Vanadium chloroperoxidase as a catalyst for hydrogen peroxide disproportionation to singlet oxygen in mildly acidic aqueous environment. Adv. Synth. Catal. 345, 849–858 (2003).

    Article  CAS  Google Scholar 

  31. Soedjak, H. S. & Butler, A. Mechanism of dioxygen formation catalyzed by vanadium-bromoperoxidase from Macrocystis pyrifera and Fucus distichus: steady state kinetic analysis and comparison to the mechanism of V-BrPO from Ascophyllum nodosum. Biochim. Biophys. Acta. 1079, 1–7 (1991).

    Article  CAS  Google Scholar 

  32. Butler, A. Acquisition and utilization of transition metal ions by marine organisms. Science 281, 207–210 (1998).

    Article  CAS  Google Scholar 

  33. Beers, R. F. & Sizer, I. W. Spectrophotometric methods for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133–140 (1952).

    CAS  Google Scholar 

  34. Wang, D. & Sañudo-Wilhelmy, S. A. Development of an analytical protocol for the determination of V(IV) and V(V) in seawater: application to coastal environments. Mar. Chem. 112, 72–80 (2008).

    Article  CAS  Google Scholar 

  35. Sachs, L. Angewandte Statistik 242 (Springer, 1984).

    Book  Google Scholar 

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Acknowledgements

This research was supported by the European community through the project BIOMINTEC (PITN-GA-2008215507) and the BMBF center of Excellence BIOTEC Marin. The authors acknowledge partial support from the Center for Complex Matter (COMATT) at the University of Mainz.

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Authors and Affiliations

  1. Institut für Anorganische Chemie und Analytische Chemie, Johannes Gutenberg Universität, Duesbergweg 10-14, Mainz, 55099, Germany

    Filipe Natalio, Rute André & Wolfgang Tremel

  2. Van't Hoff Institute for Molecular Sciences, Universiteit van Amsterdam, Science Park 904 1098 XH, Amsterdam, The Netherlands

    Aloysius F. Hartog & Ron Wever

  3. Max Planck Institute for Chemistry, Postfach 3060, Mainz, 55020, Germany

    Brigitte Stoll & Klaus Peter Jochum

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  1. Filipe Natalio
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Contributions

F.N., R.A. and A.F.H. carried out the experiments. R.W. and W.T. conceived the experiments. B.S. and K.P.J. contributed with the ICP-MS measurements. W.T. wrote the manuscript with contributions from F.N.

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Correspondence to Wolfgang Tremel.

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Natalio, F., André, R., Hartog, A. et al. Vanadium pentoxide nanoparticles mimic vanadium haloperoxidases and thwart biofilm formation. Nature Nanotech 7, 530–535 (2012). https://doi.org/10.1038/nnano.2012.91

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