Letter | Published:

Vanadium pentoxide nanoparticles mimic vanadium haloperoxidases and thwart biofilm formation

Nature Nanotechnology volume 7, pages 530535 (2012) | Download Citation

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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References

  1. 1.

    , & Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv. Mater. 23, 690–718 (2011).

  2. 2.

    & Enzymes on nanotubes thwart fouling. Nature Nanotech. 2, 138–139 (2007).

  3. 3.

    , , & Modern approaches to marine antifouling coatings. Surf. Coat. Technol. 201, 3642–3652 (2006).

  4. 4.

    , & Marine paints: the particular case of antifouling paints. Prog. Org. Coat. 59, 2–20 (2007).

  5. 5.

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

  6. 6.

    , & Pyrithiones as antifoulants: environmental chemistry and preliminary risk assessment. Biofouling 15, 175–182 (2000).

  7. 7.

    , & Resistance of bacterial cultures to nonoxidizing water-treatment bactericides by adaptation. Water Sci. Technol. 31, 169–175 (1995).

  8. 8.

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

  9. 9.

    , , & The role of ‘inert’ surface chemistry in marine biofouling prevention. Phys. Chem. Chem. Phys. 12, 4275–4286 (2010).

  10. 10.

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

  11. 11.

    , , , & Brominating activity of the seaweed Ascophyllum Nodosum: impact on the biosphere. Environ. Sci. Technol. 25, 446–449 (1991).

  12. 12.

    , , , & Recombinant vanadium haloperoxidases and their uses. Patent WO/1995/027046 (1995).

  13. 13.

    , , & Antifouling Paint Containing Haloperoxidase and Method to Determine Halide. Patent WO/1995/027009 (1995).

  14. 14.

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

  15. 15.

    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).

  16. 16.

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

  17. 17.

    , & Inhibition and inactivation of vanadium bromoperoxidase by the substrate, hydrogen peroxide, and further mechanistic studies of vanadium bromoperoxidase. Biochemistry 34, 12689–12696 (1995).

  18. 18.

    , , & The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem. Rev. 104, 849–902 (2004).

  19. 19.

    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).

  20. 20.

    , & A functional mimic of vanadium bromoperoxidase. J. Am. Chem. Soc. 114, 760–767 (1992).

  21. 21.

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

  22. 22.

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

  23. 23.

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

  24. 24.

    , , , & From phosphatases to vanadium peroxidases: a similar architecture of the active site. Proc. Natl Acad. Sci. USA 94, 2145–2149 (1997).

  25. 25.

    & Irreversible inactivation of Caldariomyces fumago chloroperoxidase by hydrogen peroxide. IUBMB Life 39, 665–670 (1996).

  26. 26.

    , & Vanadium peroxide complexes. Chem. Rev. 94, 625–638 (1994).

  27. 27.

    , , & Functional models for vanadium haloperoxidase: reactivity and mechanism of halide oxidation. J. Am. Chem. Soc. 118, 3469–3478 (1996).

  28. 28.

    , & Functional mimic of vanadium bromoperoxidase. J. Am. Chem. Soc. 114, 760–761 (1992).

  29. 29.

    , & Catalytic oxidations by vanadium complexes. Coord. Chem. Rev. 237, 89–101 (2003).

  30. 30.

    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).

  31. 31.

    & 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).

  32. 32.

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

  33. 33.

    & Spectrophotometric methods for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133–140 (1952).

  34. 34.

    & 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).

  35. 35.

    Angewandte Statistik 242 (Springer, 1984).

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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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Affiliations

  1. Institut für Anorganische Chemie und Analytische Chemie, Johannes Gutenberg Universität, Duesbergweg 10-14, 55099 Mainz, 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, 55020 Mainz, Germany

    • Brigitte Stoll
    •  & Klaus Peter Jochum

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Wolfgang Tremel.

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DOI

https://doi.org/10.1038/nnano.2012.91

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