Investigating the Interaction Between Streptomyces sp. and Titania/Silica Nanospheres

  • Adrian Augustyniak
  • Krzysztof Cendrowski
  • Paweł Nawrotek
  • Martyna Barylak
  • Ewa Mijowska
Article

Abstract

Titania/silica nanomaterials have many possible applications; however, they can be toxic to living organisms, particularly if the material accumulates in niche environments, e.g. areas colonised by actinomycetes. This study therefore investigated the effect of non-activated and UV light-activated titania/silica nanospheres on an environmental Streptomyces strain. The bacteria were incubated with the nanospheres and subsequently cultured on solid medium. The morphology and elemental composition were analysed using optical and electron microscopy (TEM, STEM) and energy-dispersive X-ray spectroscopy (EDX). The appearance of Streptomyces sp. in the experimental and control samples demonstrated that the nanospheres did not have bactericidal properties in the used dose. Furthermore, the observed strain not only survived in the presence of the nanomaterial but also appeared to play a role in its dissolution with an accumulation of the titanium in the intracellular globules of polyphosphate (volutin). Additionally, it was discovered that the UV light-activated titanium dioxide altered the ability of the bacteria to secrete humic acid. The reported phenomenon might be made possible through an accumulation of titanium in the volutin compounds. These findings suggest that streptomycetes could be employed to participate in the dissolution of nanomaterials which enter the natural environment.

Keywords

Streptomyces sp. Nanomaterials Titania/silica nanospheres Stimulation Dissolution 

Supplementary material

11270_2016_2922_MOESM1_ESM.pdf (355 kb)
ESM 1(PDF 354 kb)

References

  1. Achbergerová, L., Nahálka, J. (2011). Polyphosphate—an ancient energy source and active metabolic regulator. Microbial Cell Factories 10. doi: 10.1186/1475-2859-10-63
  2. Borm, P. J. A., Robbins, D., Haubold, S., Kuhibusch, T., Fissan, H., Donaldson, K., Schins, R., Stone, V., Kreyling, W., Lademann, J., Hartmann, J., Warheit, D., & Oberdorfer, J. (2006). The potential risk of nanomaterials: a review carried out for ECETOC. Particle and Fibre Toxicology, 3, 1–25. doi:10.1186/1743-8977-3-11.CrossRefGoogle Scholar
  3. Cauda, V., Schlossbauer, A., & Bein, T. (2010). Bio-degradation study of colloidal mesoporous silica nanoparticles: effect of surface functionalization with organo-silanes and poly(ethylene glycol). Microporous and Mesoporous Materials, 132, 60–71. doi:10.1016/j.micromeso.2009.11.015.CrossRefGoogle Scholar
  4. Cendrowski, K., Chen, X., Zielinska, B., Kalenczuk, R. J., Rümmeli, M. H., Büchner, B., Klingeler, R., & Borowiak-Palen, E. (2011). Synthesis, characterization, and photocatalytic properties of core/shell mesoporous silica nanospheres supporting nanocrystalline titania. Journal of Nanoparticle Research, 13, 5899–5908. doi:10.1007/s11051-011-0307-1.CrossRefGoogle Scholar
  5. Cendrowski, K., Peruzynska, M., Markowska-Szczupak, A., Chen, X., Wajda, A., Lapczuk, J., Kurzawski, M., Kalenczuk, R., Drozdzik, M., Mijowska, E. (2013) Mesoporous silica nanospheres functionalized by TiO2 as a photoactive antibacterial agent. Journal of Nanomedicine Nanotechnology 4. doi: 10.4172/2157-7439.1000182.
  6. Cendrowski, K., Jedrzejczak, M., Dybus, A., Peruzynska, M., Drozdzik, M., & Mijowska, E. (2014a). Preliminary study towards enhancement of photoactivity performance using biocompatible titanium dioxide/carbon nanotubes composite. Journal of Alloys and Compounds, 605(25), 173–178. doi:10.1016/j.jallcom.2014.03.112.CrossRefGoogle Scholar
  7. Cendrowski, K., Peruzynska, M., Markowska-Szczupak, A., Chen, X., Wajda, A., Lapczuk, J., Kurzawski, M., Kalenczuk, R. J., Drozdzik, M., & Mijowska, E. (2014b). Antibacterial performance of nanocrystallined titania confined in mesoporous silica nanotubes. Biomedical Microdevices, 16, 449–458. doi:10.1007/s10544-014-9847-3.CrossRefGoogle Scholar
  8. Christian, P., von der Kammer, F., Baalousha, M., & Hofmann, T. (2008). Nanoparticles: structure, properties, preparation and behaviour in environmental media. Ecotoxicology, 17, 326–343. doi:10.1007/s10646-008-0213-1.CrossRefGoogle Scholar
  9. Dong-Wook, L., Son-Ki, I., & Kew-Ho, L. (2005). Mesostructure control using a titania-coated silica nanosphere framework with extremely high thermal stability. Chemistry of Materials, 17, 4461–4467. doi:10.1021/cm050485w.CrossRefGoogle Scholar
  10. Finnie, K. S., Waller, D. J., Perret, F. L., Krause-Heuer, A. M., Lin, H. Q., Hanna, J. V., & Barbe, C. J. (2009). Biodegradability of sol–gel silica microparticles for drug delivery. Journal of Sol-Gel Science and Technology, 49, 12–18. doi:10.1007/s10971-008-1847-4.CrossRefGoogle Scholar
  11. Ge, Y., Schimel, J. P., & Holden, P. A. (2012). Identification of soil bacteria susceptible to TiO2 and ZnO nanoparticles. Applied and Environmental Microbiology, 78, 6749–6758. doi:10.1128/AEM.00941-12.CrossRefGoogle Scholar
  12. Hannah, W., & Thompson, P. B. (2008). Nanotechnology risk and the environment: a review. Journal of Environmental Monitoring, 10, 291–300. doi:10.1039/b718127m.CrossRefGoogle Scholar
  13. Hu, K. W., Hsu, K. C., & Yeh, C. S. (2010). pH-dependent biodegradable silica nanotubes derived from Gd(OH)3 nanorods and their potential for oral drug delivery and MR imaging. Biomaterials, 31, 6843–6848. doi:10.1016/j.biomaterials.2010.05.046.CrossRefGoogle Scholar
  14. Imamura, S., Tarumoto, H., & Ishida, S. (1989). Decomposition of 1,2-dichloroethane on titanium dioxide/silica. Industrial & Engineering Chemistry Research, 28(10), 1449–1452. doi:10.1021/ie00094a001.CrossRefGoogle Scholar
  15. Knauss, K. G., Dibley, M. J., Bourcier, W. L., & Shaw, H. F. (2001). Ti(IV) hydrolysis constants derived from rutile solubility measurements made from 100 to 300 C. Applied Geochemistry, 16, 1115–1128. doi:10.1016/S0883-2927(00)00081-0.CrossRefGoogle Scholar
  16. Kunzmann, A., Andersson, B., Thurnherr, T., Krug, H., Scheynius, A., & Fadeel, B. (2011). Toxicology of engineered nanomaterials: focus on biocompatibility, biodistribution and biodegradation. Biochimica et Biophysica Acta, 1810, 361–373. doi:10.1016/j.bbagen.2010.04.007.CrossRefGoogle Scholar
  17. Küster, E., & Williams, S. T. (1964). Selection of media for isolation of Streptomycetes. Nature, 202, 928–929. doi:10.1038/202928a0.CrossRefGoogle Scholar
  18. Lai, W., Ducheyne, P., Garino, J. (1998). Removal pathway of silicon released from bioactive glass granules in vivo. In: R.Z. LeGeros, L. LeGeros, (Ed.) (pp. 383–386). Bioceramics. World Scientific Publishing Co., Singapore.Google Scholar
  19. Li, X., Zhang, L., Dong, X., Liang, J., & Shi, J. (2007). Preparation of mesoporous calcium doped silica spheres with narrow size dispersion and their drug loading and degradation behaviour. Journal of Microporous and Mesoporous Materials, 102, 151–158. doi:10.1016/j.micromeso.2006.12.048.CrossRefGoogle Scholar
  20. Li, Z., Hou, B., Xu, Y., Wu, D., & Sun, Y. (2005). Hydrothermal synthesis, characterization, and photocatalytic performance of silica-modified titanium dioxide nanoparticles. Journal of Colloid and Interface Science, 288, 149–154. doi:10.1016/j.jcis.2005.02.082.CrossRefGoogle Scholar
  21. Linley, S., Liu, Y. Y., Ptacek, C. J., Blowes, D. W., & Gu, F. X. (2014). Recyclable graphene oxide-supported titanium dioxide photocatalysts with tunable properties. ACS Applied Materials & Interfaces, 6, 4658–4668. doi:10.1021/am4039272.CrossRefGoogle Scholar
  22. Liu, H., Deng, L., Sun, C., Li, J., & Zhu, Z. (2015). Titanium dioxide encapsulation of supported Ag nanoparticles on the porous silica bead for increased photocatalytic activity. Applied Surface Science, 326, 82–90. doi:10.1016/j.apsusc.2014.11.110.CrossRefGoogle Scholar
  23. Liu, K., Lin, X., & Zhao, J. (2013). Toxic effects of the interaction of titanium dioxide nanoparticles with chemicals or physical factors. International Journal of Nanomedicine, 8, 2509–2520. doi:10.2147/IJN.S46919.Google Scholar
  24. Maurer-Jones, M. A., Gunsolus, I. L., Meyer, B. M., Christenson, C. J., & Haynes, C. L. (2013). Impact of TiO2 nanoparticles on growth, biofilm formation, and flavin secretion in Shewanella oneidensis. Analytical Chemistry, 85, 5810–5818. doi:10.1021/ac400486u.CrossRefGoogle Scholar
  25. Navarro, E., Baun, A., Behra, R., Hartmann, N. B., Filser, J., Miao, A. J., Quigg, A., Santschi, P. H., & Sigg, L. (2008). Environmental behaviour and ecotoxicity of engineered nanoparticles to algae, plants and fungi. Ecotoxicology, 17, 372–386. doi:10.1007/s10646-008-0214-0.CrossRefGoogle Scholar
  26. Negoda, A., Negoda, E., Xian, M., & Reusch, R. N. (2009). Role of polyphosphate in regulation of the Streptomyces lividans KcsA channel. Biochimica et Biophysica Acta, 1788, 608–614. doi:10.1016/j.bbamem.2008.12.017.CrossRefGoogle Scholar
  27. Oguma, J., Kakuma, Y., Murayama, S., & Nosaka, Y. (2013). Effects of silica coating on photocatalytic reactions of anatase titanium dioxide studied by quantitative detection of reactive oxygen species. Applied Catalysis B: Environmental, 129(17), 282–286. doi:10.1016/j.apcatb.2012.09.034.CrossRefGoogle Scholar
  28. Ortiz, D., & Groves, M. R. (2009). The three-component signalling system HbpS–SenS–SenR as an example of a redox sensing pathway in bacteria. Amino Acids, 37, 479–486.CrossRefGoogle Scholar
  29. Palanichamy, V., Hundet, A., Mitra, B., & Reddy, N. (2011). Optimization of cultivation parameters for growth and pigment production by Streptomyces spp. isolated from marine sediment and rhizosphere soil. The International Journal of Plant, Animal and Environmental Sciences, 1, 158–170.Google Scholar
  30. Paredes, D., Ortiz, C., & Torres, R. (2014). Synthesis, characterization, and evaluation of antibacterial effect of Ag nanoparticles against Escherichia coli O157:H7 and methicillin-resistant Staphylococcus aureus (MRSA). International Journal of Nanomedicine, 9, 1717–1729. doi:10.2147/IJN.S57156.Google Scholar
  31. Petković, J., Küzma, T., Rade, K., Novak, S., & Filipi, M. (2011). Pre-irradiation of anatase TiO2 particles with UV enhances their cytotoxic and genotoxic potential in human hepatoma HepG2 cells. Journal of Hazardous Materials, 196, 145–152.CrossRefGoogle Scholar
  32. Piccinno F., Gottschalk F., Seeger S., Nowack B. (2012). Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. Journal of Nanoparticle Research 14. doi:10.1007/s11051-012-1109-9
  33. Schmidt, J., & Vogelsberger, W. (2006). Dissolution kinetics of titanium dioxide nanoparticles the observation of an unusual kinetic size effect. Journal of Physical Chemistry B, 110, 3955–3963. doi:10.1021/jp055361l.CrossRefGoogle Scholar
  34. Solecka, J., Ziemska, J., Rajnisz, A., Laskowska, A., & Guśpiel, A. (2013). Actinomycetes—occurrence and production of biologically active compounds. Postępy Mikrobiologii, 52, 83–91.Google Scholar
  35. Stankovic, N., Radulovic, V., Petkovic, M., Vuckovic, I., Jadranin, M., Vasiljevic, B., & Nikodinovic-Runic, J. (2012). Streptomyces sp. JS520 produces exceptionally high quantities of undecylprodigiosin with antibacterial, antioxidative, and UV-protective properties. Applied Microbiology and Biotechnology, 96, 1217–1231. doi:10.1007/s00253-012-4237-3.CrossRefGoogle Scholar
  36. Tung, W. S., & Daoud, W. A. (2009). New approach toward nanosized ferrous ferric oxide and Fe3O4-doped titanium dioxide photocatalysts. ACS Applied Materials & Interfaces, 1, 2453–2461.CrossRefGoogle Scholar
  37. Yamada, H., Urata, C., Aoyama, Y., Osada, S., Yamauchi, Y., & Kuroda, K. (2012). Preparation of colloidal mesoporous silica nanoparticles with different diameters and their unique degradation behavior in static aqueous systems. Chemistry of Materials, 24, 1462–147. doi:10.1021/cm3001688.CrossRefGoogle Scholar
  38. Weir, A., Westerhoff, P., Fabricius, L., & Goetz, N. (2012). Titanium dioxide nanoparticles in food and personal care products. Environmental Science and Technology, 46, 2242–2250. doi:10.1021/es204168d.CrossRefGoogle Scholar
  39. Ziemniak, S. E., Jones, M. E., & Combs, K. E. S. (1993). Solubility behavior of titanium(IV) oxide in alkaline media at elevated temperatures. Journal of Solution Chemistry, 22, 601–623. doi:10.1007/BF00646781.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Adrian Augustyniak
    • 1
  • Krzysztof Cendrowski
    • 2
  • Paweł Nawrotek
    • 1
  • Martyna Barylak
    • 2
  • Ewa Mijowska
    • 2
  1. 1.Department of Immunology, Microbiology and Physiological Chemistry, Faculty of Biotechnology and Animal HusbandryWest Pomeranian University of TechnologySzczecinPoland
  2. 2.Institute of Chemical and Environment EngineeringWest Pomeranian University of TechnologySzczecinPoland

Personalised recommendations