Abstract
Increased application of titanium dioxide and zinc oxide nanoparticles (nano-TiO2 and nano-ZnO) raises concerns related to their environmental impacts. The effects that such nanoparticles have on environmental processes and the bacteria that carry them out are largely unknown. In this study, ammonia-oxidizing bacteria (AOB) enrichment cultures, grown from surface sediments taken from an estuary wetland in Fujian Province, China, were spiked with nano-TiO2 and nano-ZnO (with an average size of 32 and 43 nm, respectively) at predicted environmentally relevant concentrations (≤2 mg L−1) to determine their impacts on ammonia oxidation and the mechanisms involved. Results showed that higher nano-TiO2 concentrations significantly inhibited ammonia oxidation in enrichment cultures. It is noteworthy that the average ammonia oxidation rate was significantly correlated to the Shannon index, the Simpson’s index, and AOB abundance. This suggested that ammonia oxidation inhibition primarily resulted from a reduction of AOB biodiversity and abundance. However, AOB biodiversity and abundance as well as the average ammonia oxidation rate were not inhibited by nano-ZnO at predicted environmentally relevant concentrations. Accordingly, an insignificant correlation was established between biodiversity and abundance of the AOB amoA gene and the average ammonia oxidation rate under nano-ZnO treatments. AOB present in samples belonged to the β-Proteobacteria class with an affinity close to Nitrosospira and Nitrosomonas genera. This suggested that identified impacts of nano-TiO2 and nano-ZnO on ammonia oxidation processes can be extrapolated to some extent to natural aquatic environments. Complex impacts on AOB may result from different nanomaterials present in aquatic environments at various ambient conditions. Further investigation on how and to what extent different nanomaterials influence AOB diversity and abundance and their subsequent ammonia oxidation processes is therefore required.
Similar content being viewed by others
References
Adams LK, Lyon DY, Alvarez PJ (2006) Comparative ecotoxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40(19):3527–3532
Barnes RJ, Molina R, Xu JB, Dobson PJ, Thompson IP (2013) Comparison of TiO2 and ZnO nanoparticles for photocatalytic degradation of methylene blue and the correlated inactivation of gram-positive and gram-negative bacteria. J Nanoparticle Res 15(2):1432–1440
Belser LW, Mays EL (1980)Specific-inhibition of nitrite oxidation by chlorate and its use in assessing nitrification in soils and sediments. Appl Environ Microbiol 39(3):505–510
Bollmann A, French E, Laanbroek HJ (2011) Isolation, cultivation, and characterization of ammonia-oxidizing bacteria and archaea adapted to low ammonium concentrations. In: Klotz MG (ed) Methods in enzymology. Academic, Burlington, pp 55–88
Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fievet F (2006) Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 6(4):866–870
Bulla L (1994) An index of evenness and its associated diversity measure. Oikos 70(1):167–171
Chao A, Shen TJ (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ Ecol Stat 10(4):429–443
Choi OK, Hu ZQ (2009) Nitrification inhibition by silver nanoparticles. Water Sci Technol 59(9):1699–1702
Du WC, Sun YY, Ji R, Zhu JG, Wu JC, Guo HY (2011) TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. J Environ Monitor 13:822–828
Ge Y, Schimel JP, Holden PA (2011) Evidence for negative effects of TiO2 and ZnO nanoparticles on soil bacterial communities. Environ Sci Technol 45(4):1659–1664
Gorelick R (2006) Combining richness and abundance into a single diversity index using matrix analogues of Shannon’s and Simpson’s indices. Ecography 29(4):525–530
Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43(24):9216–9222
Heinlaan M, Ivask A, Blinova I, Dubourguier H-C, Kahru A (2008) Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71(7):1308–1316
Hofmann T, von der Kammer F (2009) Estimating the relevance of engineered carbonaceous nanoparticle facilitated transport of hydrophobic organic contaminants in porous media. Environ Pollut 157(4):1117–1126
Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625
Jones N, Ray B, Ranjit KT, Manna AC (2008) Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS Microbiol Lett 279:71–76
Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400(1–3):396–414
Li YJ, Huang FY, Luo ZX, Xu B, Wang XX, Li FM, Wang F, Huang LX, Li SX, Li YC (2012) A new hydrogen peroxide biosensor based on synergy of Au@Au2S2O3core-shell nanomaterials and multi-walledcarbon nanotubes towards hemoglobin. Electrochim Acta 74:280–286
Luo Z, Wang Z, Wei Q, Yan C, Liu F (2011a) Effects of engineered nano-titanium dioxide on pore surface properties and phosphorus adsorption of sediment: its environmental implications. J Hazard Mater 192(3):1364–1369
Luo Z, Wang Z, Li Q, Pan Q, Yan C, Liu F (2011b) Spatial distribution, electron microscopy analysis of titanium and its correlation to heavy metals: occurrence and sources of titanium nanomaterials in surface sediments from Xiamen Bay, China. J Environ Monit 13(4):1046–1052
Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K, Oberdorster G, Philbert MA, Ryan J, Seaton A, Stone V, Tinkle SS, Tran L, Walker NJ, Warheit DB (2006) Safe handling of nanotechnology. Nature 444(7117):267–269
Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl Environ Microbiol 75(23):7461–7468
Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16s ribosomal-RNA. Appl Environ Microbiol 59(3):695–700
Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150(1):5–22
Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66(12):5368–5382
Roco MC, Brainbridge W (2001) Societal implications of nanoscience and nanotechnology. Kluwer Academic, Boston
Tayel AA, El-Tras WF, Moussa S, El-Baz AF, Mahrous H, Salem MF, Brimer L (2011) Antibacterial action of zinc oxide nanoparticles against foodborne pathogens. J Food Saf 31:211–218
Tsuang YH, Sun JS, Huang YC, Lu CH, Chang WH, Wang CC (2008) Studies of photokilling of bacteria using titanium dioxide nanoparticles. Artif Organs 32:167–174
Yu S, Zhang QF, Peng JJ, Chen Q, Li XF, Xu CY, Yin HB (2011) Impacts of Spartina alterniflora invasion on abundance and composition of ammonia oxidizers in estuarine sediment. J Soils Sediments 11(6):1020–1031
Zhang L, Jiang Y, Ding Y, Ding Y, Povey M, Povey M, York D (2007) Investigation into the antibacterial behaviour of suspensions of ZnO nanoparticles (ZnO nanofluids). J Nanopart Res 9(3):479–489, 20
Zheng X, Chen YG, Wu R (2011a)Long-term effects of titanium dioxide nanoparticles on nitrogen and phosphorus removal from wastewater and bacterial community shift in activated sludge. Environ Sci Technol 45(17):7284–7290
Zheng XO, Wu R, Chen YG (2011b) Effects of ZnO nanoparticles on wastewater biological nitrogen and phosphorus removal. Environ Sci Technol 45(7):2826–2832
Acknowledgments
The authors of this study would like to thank the anonymous reviewers for their helpful comments. We thank Brian Doonan (McGill University, Canada) in providing language help in writing this paper and provide useful suggestions. They also gratefully acknowledge the joint research funding from the National Nature Science Foundation of China (41001327 and 41271484), the Nature Science Foundation of Fujian Province (2013J01166), the Fujian Provincial Education Department Foundation (JA11168), and the Institute of Urban Environment, Chinese Academy of Sciences for Young Scientists in Frontier Research (IUEQN-2012-04).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible editor: Robert Duran
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 122 kb)
Rights and permissions
About this article
Cite this article
Luo, Z., Qiu, Z., Chen, Z. et al. Impact of TiO2 and ZnO nanoparticles at predicted environmentally relevant concentrations on ammonia-oxidizing bacteria cultures under ammonia oxidation. Environ Sci Pollut Res 22, 2891–2899 (2015). https://doi.org/10.1007/s11356-014-3545-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-014-3545-9