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Download Author Version (PDF) RSC Advances This is an Accepted Manuscript, which has been through the Royal Society of Chemistry peer review process and has been accepted for publication. Accepted Manuscripts are published online shortly after acceptance, before technical editing, formatting and proof reading. Using this free service, authors can make their results available to the community, in citable form, before we publish the edited article. This Accepted Manuscript will be replaced by the edited, formatted and paginated article as soon as this is available. You can find more information about Accepted Manuscripts in the Information for Authors. Please note that technical editing may introduce minor changes to the text and/or graphics, which may alter content. The journal’s standard Terms & Conditions and the Ethical guidelines still apply. In no event shall the Royal Society of Chemistry be held responsible for any errors or omissions in this Accepted Manuscript or any consequences arising from the use of any information it contains. www.rsc.org/advances Page 1 of 27 RSC Advances The impact of zinc oxide nanoparticles on nitrification and the bacterial community in activated sludge in an SBR S.T. Wang*a, S.P. Li b, W.Q. Wang a and H. You c (a State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China; b Environmental Monitoring Station of Guangzhou Military Region, Guangzhou 510517, P.R. China; c School of Marine Science and Technology, Harbin Institute of Technology at Weihai, Weihai 264209, China) Manuscript *Corresponding author: S.T. Wang S.T. Wang (Shutao Wang): E-Mail: [email protected] Address: School of Municipal and Environmental Engineering, Harbin Institute of Technology, 73, Huanghe Rd., Nangang Dist., Harbin 150090, China Accepted S.P. L (Suping Li): E-Mail: [email protected] Address: Environmental Monitoring Station of Guangzhou Military Region, Guangzhou 510517, P.R. China W.Q. Wang (Weiqing Wang): E-Mail: [email protected] Advances Address: School of Municipal and Environmental Engineering, Harbin Institute of Technology, 73, Huanghe Rd., Nangang Dist., Harbin 150090, China H. You (Hong You): RSC E-Mail: [email protected] Address: School of Marine Science and Technology, Harbin Institute of Technology at Weihai, Weihai 264209, China RSC Advances Page 2 of 27 1 The impact of zinc oxide nanoparticles on nitrification and the bacterial community in activated sludge in 2 an SBR 3 S.T. Wang,*a S.P. Li b , W.Q. Wang a and H. You c 4 Zinc oxide(ZnO) nanoparticles (NPs) have been reported to induce adverse effects on organisms. The 5 impacts of ZnO NPs on nitrification and the nitrobacteria community in activated sludge were investigated 6 in a simulated SBR. It revealed that ZnO NPs at low concentrations (5 and 10 mg/L) slightly inhibited 7 nitrification. At these concentrations the activity of ammonia monooxygenase (AMO) and nitrite 8 oxidoreductase (NOR) as well as the cell membrane integrity of nitrosomonas europaea were almost 9 unaffected. Concentrations of 20 mg/L and 50 mg/L ZnO NPs had significantly adverse effects on the Manuscript + - - - 10 activity of AMO and NOR and on the transformation of NH 4 -N to NO 2 -N and NO 2 -N to NO 3 -N. Analysis by 11 denaturing gradient gel electrophoresis (DGGE) revealed that higher concentrations of ZnO NPs significantly 12 inhibited the growth of the typical ammonia-oxidizing bacteria (AOB) that were mainly responsible for 13 oxidation of ammonia to nitrate. Moderate concentrations of ZnO NPs could accelerate the growth of some Accepted 14 types of denitrifying bacteria and promote the growth of some pathogenic bacteria. Moderate and high 15 concentrations of ZnO NPs could obviously destroy the integrity of the cell membrane of Nitrosomonas 16 europaea . These findings meaningfully assessed the adverse effects of ZnO NPs on activated sludge in 17 wastewater treatment. Advances 18 1. Introduction 19 The development and application of nanotechnology have raised significant concerns about the adverse RSC 20 effects of nanoparticles (NPs) on human health and the environment.1 NPs can be more toxic than larger 21 particles of the same composition because of their large specific surface area and unique size-effect.2,3 22 Many studies were thus conducted to predict their environmental concentrations and investigate the 23 behavior of NPs in the environment.4,5,6 The increasing utilization of products containing NPs, however, was 2 Page 3 of 27 RSC Advances 24 observed to result in the release of NPs into wastewater treatment plants (WWTPs).7,8,9 Large amounts of 25 zinc oxide nanoparticles (ZnO NPs) have been used in semiconductors, plastic additives, pigments and 26 cosmetics.10 A recent study confirmed that ZnO NPs were present in sewage sludge and effluents. 27 According to the report issued by the USEPA in 2009, an examination of 84 WWTPs showed that the zinc 28 content in WWTP biosolids was 8.55 g/kg-SS.11 The investigations in China in 2011 (139 WWTPs in total) 29 and in 2009 (107 WWTPs in total) showed that the average concentration of Zn in biosolids was 1.03 30 g/kg-SS and that the maximum concentration was 9.14 g/kg-SS.12,13,14 Concerns can therefore be raised 31 about whether the NPs in WWTPs have negative impacts on the microbial community in activated sludge, 32 which may eventually hamper the function of WWTPs in removing pollutants from wastewater, such as Manuscript 33 chemical oxygen demand (COD), nitrogen and phosphorous. 34 Recently, studies have started to address this issue. Zheng et al. 15 reported that the presence of 10 and 50 35 mg/L of ZnO NPs decreased the total nitrogen removal efficiencies from 81.5% to 75.6% and 70.8%, 36 respectively, compared with the absence of ZnO NPs. Additionally, several other publications indicated that Accepted 37 different NPs and exposure times showed different effects on biological nitrogen removal. For instance, 15 38 Zheng et al. reported that 1 mg/L of SiO 2 NPs caused no adverse acute and chronic effects on sludge 39 viability and wastewater nitrogen removal, while chronic exposure to 50 mg/L SiO 2 NPs depressed the total 40 nitrogen (TN) removal efficiency from 79.6% to 51.6% after a 70-day exposure. Chen et al. 16 found that Advances 41 short-term exposure to 1 and 50 mg/L Al 2O3 NPs induced only marginal influences on wastewater 42 nitrification and denitrification. Nevertheless, prolonged exposure to 50 mg/L Al 2O3 NPs was observed to RSC 43 decrease the TN removal efficiency from 80.4% to 62.5%. Ni et al. 17 found that the short-term presence of 44 50-200 mg/L of NPs decreased the TN removal efficiency resulting from the acute toxicity of a shock load of 45 magnetic NPs, while long-term exposure to 50 mg/L magnetic NPs was observed to significantly improve 7 46 the TN removal efficiency. Zheng et al. found that concentrations of 1 and 50 mg/L TiO 2 NPs had no acute 3 RSC Advances Page 4 of 27 47 effects on nitrogen removal from wastewater after a short-term exposure (1 day), while 50 mg/L TiO 2 NPs 48 (higher than its environmentally relevant concentration) was observed to significantly decrease the TN 49 removal efficiency from 80.3% to 24.4% after long-term exposure (70 days). Li et al. 18 found that 2-50 mg/L 50 of TiO 2 NPs did not adversely affect nitrogen removal, but when the activated sludge was exposed to 51 100-200 mg/L of TiO 2 NPs, the effluent TN removal efficiencies were 36.5% and 20.3%, respectively, which 52 were markedly lower than the values observed in the control test (80%). Most of the above studies 53 demonstrated that NPs hampered the function of the WWTP in removing nitrogen from wastewater. 54 However,it is still not well known how ZnO NPs affect nitrification in activated sludge and which step of 55 nitrification is more sensitive to ZnO NPs. Manuscript 56 As is well known, the biological removal of nitrogen in wastewater is achieved by complex microbial 57 populations that are responsible for nitrification and denitrification.7,19,20 Therefore, the diversity of the 58 microbial populations and a stable bacterial community structure both play important roles in achieving a 59 high efficiency of biological nitrogen removal. Previous publications noted that silver NPs could cause a 50% Accepted 60 inhibition of the respiration of nitrifying bacteria at a concentration of 0.14 mg/L, 21 whereas Cu NPs 22 61 showed no inhibitory effect on the respiration of ammonia-oxidizing bacteria at the level of 10 mg/L . 16 62 Chen et al. indicated that, compared with the control, 50 mg/L Al 2O3 NPs decreased the abundance of 63 denitrifying bacteria in activated sludge according to quantitative polymerase chain reaction (PCR) assays. Advances 64 Ni et al. 17 reported that a short-term exposure to 50 mg/L magnetic NPs led to the abatement of nitrifying 65 bacteria according to fluorescence in situ hybridization (FISH) assays. According to Zheng et al. 7, denaturing RSC 66 gradient gel electrophoresis (DGGE) profiles showed that 50 mg/L TiO 2 NPs clearly reduced the diversity of 67 the microbial community in activated sludge, and FISH analysis indicated that the abundance of nitrifying 68 bacteria, especially ammonia-oxidizing bacteria, was significantly decreased after long-term exposure to 50 18 69 mg/L TiO 2 NPs. Similarly, according to Li et al., the DGGE profiles showed that 200 mg/L of TiO 2 NPs 4 Page 5 of 27 RSC Advances 70 significantly reduced the microbial diversity in the activated sludge.
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