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Licensed Unlicensed Requires Authentication Published by De Gruyter May 21, 2019

Effects of heavy metals and metal (oxide) nanoparticles on enhanced biological phosphorus removal

  • Ruyi Wang ORCID logo , Juqing Lou , Jing Fang , Jing Cai , Zhirong Hu and Peide Sun EMAIL logo

Abstract

With the rapid growth of economics and nanotechnology, a significant portion of the anthropogenic emissions of heavy metals and nanoparticles (NPs) enters wastewater streams and discharges to wastewater treatment plants, thereby potentially posing a risk to the bacteria that facilitate the successful operation of the enhanced biological phosphorus (P) removal (EBPR) process. Although some efforts have been made to obtain detailed insights into the effects of heavy metals and metal (oxide) nanoparticles [Me(O)NPs], many unanswered questions remain. One question is whether the toxicity of Me(O)NPs originates from the released metal ions. This review aims to holistically evaluate the effects of heavy metals and Me(O)NPs. The interactions among extracellular polymeric substances, P, and heavy metals [Me(O)NPs] are presented and discussed for the first time. The potential mechanisms of the toxicity of heavy metals [Me(O)NPs] are summarized. Additionally, mathematical models of the toxicity and removal of P, heavy metals, and Me(O)NPs are overviewed. Finally, knowledge gaps and opportunities for further study are discussed to pave the way for fully understanding the inhibition of heavy metals [Me(O)NPs] and for reducing their inhibitory effect to maximize the reliability of the EBPR process.

Award Identifier / Grant number: 21606196

Award Identifier / Grant number: S1701

Award Identifier / Grant number: LY18E080007

Award Identifier / Grant number:

Funding statement: This research was financially supported by the National Natural Science Foundation of China (Grant no. 21606196), the Central Government’s Specially Supported Funding for the Development of Local Colleges and Universities (Grant no. S1701), the Zhejiang Provincial Natural Science Foundation of China (Grant no. LY18E080007), and the Scientific Research Fund of Zhejiang Provincial Education Department (Grant no. Y201635678).

References

Adams LK, Lyon DY, Alvarez PJJ. Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 2006; 40: 3527–3532.10.1016/j.watres.2006.08.004Search in Google Scholar PubMed

Al-Qodah Z. Biosorption of heavy metal ions from aqueous solutions by activated sludge. Desalination 2006; 196: 164–176.10.1016/j.desal.2005.12.012Search in Google Scholar

Angela M, Beatrice B, Mathieu S. Biologically induced phosphorus precipitation in aerobic granular sludge process. Water Res 2011; 45: 3776–3786.10.1016/j.watres.2011.04.031Search in Google Scholar PubMed

Auffan M, Rose J, Wiesner MR, Bottero JY. Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ Pollut 2009; 157: 1127–1133.10.1016/j.envpol.2008.10.002Search in Google Scholar PubMed

Ayangbenro AS, Babalola OO. A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 2017; 14: 94.10.3390/ijerph14010094Search in Google Scholar PubMed PubMed Central

Azam A, Ahmed AS, Oves M, Khan M, Memic A. Size-dependent antimicrobial properties of CuO nanoparticles against Gram-positive and-negative bacterial strains. Int J Nanomedicine 2012; 7: 3527–3535.10.2147/IJN.S29020Search in Google Scholar PubMed PubMed Central

Bansod BK, Kumar T, Thakur R, Rana S, Singh I. A review on various electrochemical techniques for heavy metal ions detection with different sensing platforms. Biosens Bioelectron 2017; 94: 443–455.10.1016/j.bios.2017.03.031Search in Google Scholar PubMed

Barat R, Montoya T, Seco A, Ferrer J. Modelling biological and chemically induced precipitation of calcium phosphate in enhanced biological phosphorus removal systems. Water Res 2011; 45: 3744–3752.10.1016/j.watres.2011.04.028Search in Google Scholar PubMed

Barker PS, Dold PL. General model for biological nutrient removal activated sludge systems: model presentation. Water Environ Res 1997; 69: 969–984.10.2175/106143097X125669Search in Google Scholar

Batstone DJ, Amerlinck Y, Ekama GA, Goel R, Grau P, Johnson B, Kaya I, Steyer J-P, Tait S, Takács I, Vanrolleghem PA, Brouchaert CJ, Volcke E. Towards a generalised physicochemical modelling framework. Water Sci Technol 2012; 66: 1147–1161.10.1007/s11157-009-9147-1Search in Google Scholar

Bourven I, Joussein E, Guibaud G. Characterisation of the mineral fraction in extracellular polymeric substances (EPS) from activated sludges extracted by eight different methods. Bioresour Technol 2011; 102: 7124–7130.10.1016/j.biortech.2011.04.058Search in Google Scholar

Brdjanovic D, Van Loosdrecht MCM, Versteeg P, Hooijmans CM, Alaerts GJ, Heijnen JJ. Modeling COD, N and P removal in a full-scale WWTP Haarlem Waarderpolder. Water Res 2000; 34: 846–858.10.1016/S0043-1354(99)00219-5Search in Google Scholar

Brunner TJ, Wick P, Manser PSpohn P, Grass RN, Limbach LK, Bruinink A, Stark WJ. In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 2006; 40: 4374–4381.10.1021/es052069iSearch in Google Scholar PubMed

Bura R, Cheung M, Liao B, Finlayson J, Lee BC, Droppo IG, Leppard GG, Liss SN. Composition of extracellular polymeric substances in the activated sludge floc matrix. Water Sci Technol 1998; 37: 325–333.10.2166/wst.1998.0657Search in Google Scholar

Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Fredrickson JK, Isern NG, Majors PD, Beyenal H. Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U(VI) immobilization. Environ Sci Technol 2011; 45: 5483–5490.10.1021/es200095jSearch in Google Scholar PubMed

Carletti G, Fatone F, Bolzonella D, Cecchi F. Occurrence and fate of heavy metals in large wastewater treatment plants treating municipal and industrial wastewaters. Water Sci Technol 2008; 57: 1329–1336.10.2166/wst.2008.230Search in Google Scholar PubMed

Cecchini G, Cirello P, Eramo B. Partitioning dynamics and fate of metals in an urban wastewater treatment plant. Environ Eng Manag J 2015; 14: 1511–1520.10.30638/eemj.2015.163Search in Google Scholar

Chen Y, Chen H, Zheng X, Mu H. The impacts of silver nanoparticles and silver ions on wastewater biological phosphorous removal and the mechanisms. J Hazard Mater 2012a; 239–240: 88–94.10.1016/j.jhazmat.2012.07.049Search in Google Scholar PubMed

Chen YG, Su YL, Zheng X, Chen H, Yang H. Alumina nanoparticles-induced effects on wastewater nitrogen and phosphorus removal after short-term and long-term exposure. Water Res 2012b; 46: 4379–4386.10.1016/j.watres.2012.05.042Search in Google Scholar PubMed

Chen Y, Wang D, Zhu X, Zheng X, Feng L. Long-term effects of copper nanoparticles on wastewater biological nutrient removal and N2O generation in the activated sludge process. Environ Sci Technol 2012c; 46: 12452–12458.10.1021/es302646qSearch in Google Scholar PubMed

Chen H, Zheng X, Chen YG, Mu H. Long-term performance of enhanced biological phosphorus removal with increasing concentrations of silver nanoparticles and ions. RSC Adv 2013; 3: 9835–9842.10.1039/c3ra40989aSearch in Google Scholar

Chen H, Wang D, Li X, Yang Q, Lou K, Zeng G, Tang M. Effects of Cd(II) on wastewater biological nitrogen and phosphorus removal. Chemosphere 2014a; 117: 27–32.10.1016/j.chemosphere.2014.05.057Search in Google Scholar PubMed

Chen H, Zheng X, Chen Y, Li M, Liu K, Li X. Influence of copper nanoparticles on the physical-chemical properties of activated sludge. PLoS One 2014b; 9: e92871.10.1371/journal.pone.0092871Search in Google Scholar PubMed PubMed Central

Chen H, Li X, Chen Y, Liu Y, Zhang H, Xue G. Performance of wastewater biological phosphorus removal under long-term exposure to Cu NPs: adapting toxicity via microbial community structure adjustment. RSC Adv 2015; 5: 61094–61102.10.1039/C5RA11579ESearch in Google Scholar

Chen H, Chen Y, Meng D, Xue G, Jiang M, Li X. Joint effect of triclosan and copper nanoparticles on wastewater biological nutrient removal. Environ Technol 2018; 39: 2447–2456.10.1080/09593330.2017.1355937Search in Google Scholar PubMed

Choi HJ, Yu SW, Lee SM, Yu SY. Effect of potassium and magnesium in the enhanced biological phosphorus removal process using a membrane bioreactor. Water Environ Res 2011; 83: 613–621.10.2175/106143010X12851009156808Search in Google Scholar PubMed

Choi S, Johnston MV, Wang GS, Huang CP. Looking for engineered nanoparticles (ENPs) in wastewater treatment systems: qualification and quantification aspects. Sci Total Environ 2017; 590–591: 809–817.10.1016/j.scitotenv.2017.03.061Search in Google Scholar PubMed

Chug R, Gour VS, Mathur S, Kothari SL. Optimization of extracellular polymeric substances production using Azotobacter beijreinckii and Bacillus subtilis and its application in chromium(VI) removal. Bioresour Technol 2016; 214: 604–608.10.1016/j.biortech.2016.05.010Search in Google Scholar PubMed

Chung KY, Han SS, Kim HK, Choi GS, Kim IS, Lee SS, Woo SH, Lee KH, Kim JJ. Inhibitory effect of the selected heavy metals on the growth of the phosphorus accumulating microorganism, Acinetobacter sp. Kor J Environ Agric 2006; 25: 40–46.10.5338/KJEA.2006.25.1.040Search in Google Scholar

Cuypers A, Vangronsveld J, Clijsters H. Peroxidases in roots and primary leaves of Phaseolus vulgaris copper and zinc phototoxicity: a comparison. J Plant Physiol 2002; 189: 869–876.10.1078/0176-1617-00676Search in Google Scholar

D’Abzac P, Bordas F, Joussein E, Van Hullebuch E, Lens PNL, Guibaud G. Characterization of the mineral fraction associated to extracellular polymeric substances (EPS) in anaerobic granular sludges. Environ Sci Technol 2010; 44: 412–418.10.1021/es901912gSearch in Google Scholar PubMed

Dhokpande S, Kaware DJ, Kulkarni S. Activated sludge for heavy metal removal – a review. IJRASET 2014; 2: 254–259.Search in Google Scholar

Dizaj SM, Lotfipour F, Barzegar-Jalali M, Zarrintan MH, Adibkia K. Antimicrobial activity of the metals and metal oxide nanoparticles. Mater Sci Eng C Mater Biol Appl 2014; 44: 278–284.10.1016/j.msec.2014.08.031Search in Google Scholar PubMed

Djuršić AB, Leung YH, Ng AMC, Xu XY, Lee PKH, Degger N, Wu RSS. Toxicity of metal oxide nanoparticles: mechanisms, characterization, and avoiding experimental artefacts. Small 2015; 11: 26–44.10.1002/smll.201303947Search in Google Scholar PubMed

Fang W, Hu JY, Ong SL. Influence of phosphorus on biofilm formation in model drinking water distribution systems. J Appl Microbiol 2009; 106: 1328–1335.10.1111/j.1365-2672.2008.04099.xSearch in Google Scholar PubMed

Fang J, Sun P, Xu S, Luo T, Lou J, Han J, Song Y. Impact of Cr(VI) on P removal performance in enhanced biological phosphorus removal (EBPR) system based on the anaerobic and aerobic metabolism. Bioresour Technol 2012; 121: 379–385.10.1016/j.biortech.2012.07.001Search in Google Scholar PubMed

Fang J, Su B, Sun P, Lou J, Han J. Long-term effect of low concentration Cr(VI) on P removal in granule-based enhanced biological phosphorus removal (EBPR) system. Chemosphere 2015; 121: 76–83.10.1016/j.chemosphere.2014.11.024Search in Google Scholar PubMed

Fashola M, Ngole-Jeme V, Babalola O. Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health 2016; 13: 1047.10.3390/ijerph13111047Search in Google Scholar PubMed PubMed Central

Fomina M, Gadd GM. Biosorption: current perspectives on concept, definition and application. Bioresour Technol 2014; 160: 3–14.10.1016/j.biortech.2013.12.102Search in Google Scholar PubMed

Gallagher KL, Braissant O, Kading TJ, Dupraz C, Visscher PT. Phosphate related artefacts in carbonate mineralisation experiments. J Sediment Res 2013; 83: 39–51.10.2110/jsr.2013.9Search in Google Scholar

Gernaey KV, van Loosdrecht MCM, Henze M, Lind M, Jorgensen SB. Activated sludge wastewater treatment plant modelling and simulation: state of the art. Environ Modell Softw 2004; 19: 763–783.10.1016/j.envsoft.2003.03.005Search in Google Scholar

Gómez-Rivera F, Field JA, Brown D, Sierra-Alvarez R. Fate of cerium dioxide (CeO2) nanoparticles in municipal wastewater during activated sludge treatment. Bioresour Technol 2012; 108: 300–304.10.1016/j.biortech.2011.12.113Search in Google Scholar PubMed

Gulnaz O, Saygideger S, Kusvuran E. Study of Cu(II) biosorption by dried activated sludge: effect of physico-chemical environment and kinetics study. J Hazard Mater 2005; 120: 193–200.10.1016/j.jhazmat.2005.01.003Search in Google Scholar PubMed

Gulyás G, Pitás V, Fazekas B, Kárpáti Á. Heavy metal balance in a communal wastewater treatment plant. Hung J Ind Chem 2015; 43: 1–5.10.1515/hjic-2015-0001Search in Google Scholar

Harish R, Samuel J, Mishra R, Chandrasekaran N, Mukherjee A. Bio-reduction of Cr(VI) by exopolysaccharides (EPS) from indigenous bacterial species of Sukinda chromite mine, India. Biodegradation 2012; 23: 487–496.10.1007/s10532-011-9527-4Search in Google Scholar PubMed

Hauduc H, Rieger L, Oehmen A, van Loosdrecht MCM, Comeau Y, Héduit A, Vanrolleghem PA, Gillot S. Critical review of activated sludge modeling: state of process knowledge, modeling concepts, and limitations. Biotechnol Bioeng 2013; 110: 24–46.10.1002/bit.24624Search in Google Scholar PubMed

Henze M, Gujer W, Mino T, Matsuo T, Wentzel MC, Marais GvR. Activated sludge model no. 2. IAWQ Scientific and Technical Report No. 3. IAWQ, London, UK, 1995.Search in Google Scholar

Henze M, Gujer W, Mino T, Matsuo T, Wentzel M, Marais GvR, van Loosdrecht MCM. Activated sludge model no. 2d. Water Sci Technol 1999; 39: 165–182.10.2166/wst.1999.0036Search in Google Scholar

Hernandez-Martinez GR, Ortiz-Alvarez D, Perez-Roa M, Urbina-Suarez NA, Thalasso F. Multiparameter analysis of activated sludge inhibition by nickel, cadmium, and cobalt. J Hazard Mater 2018; 351: 63–70.10.1016/j.jhazmat.2018.02.032Search in Google Scholar PubMed

Hirota K, Sugimoto M, Kato M, Tsukagoshi K, Tanigawa T, Sugimoto H. Preparation of zinc oxide ceramics with a sustainable antibacterial activity under dark conditions. Ceram Int 2010; 36: 497–506.10.1016/j.ceramint.2009.09.026Search in Google Scholar

Hoa PT, Nair L, Visvanathan C. The effect of nutrients on extracellular polymeric substance production and its influence on sludge properties. Water SA 2003; 29: 437–442.10.4314/wsa.v29i4.5050Search in Google Scholar

Hou J, Miao L, Wang C, Wang P, Ao Y, Qian J, Dai S. Inhibitory effects of ZnO nanoparticles on aerobic wastewater biofilms from oxygen concentration profiles determined by microelectrodes. J Hazard Mater 2014; 276: 164–170.10.1016/j.jhazmat.2014.04.048Search in Google Scholar PubMed

Hu Z, Chandran K, Grasso D, Smets BF. Impact of metal sorption and internalization on nitrification inhibition. Environ Sci Technol 2003a; 37: 728–734.10.1021/es025977dSearch in Google Scholar

Hu ZR, Wentzel MC, Ekama GA. Modelling biological nutrient removal activated sludge systems – a review. Water Res 2003b; 37: 3430–3444.10.1016/S0043-1354(03)00168-4Search in Google Scholar

Hu ZR, Wentzel MC, Ekama GA. A general kinetic model for biological nutrient removal activated sludge systems: model development. Biotechnol Bioeng 2007; 98: 1242–1258.10.1002/bit.21508Search in Google Scholar PubMed

Hu X, Wisniewski K, Czerwionka K, Zhou Q, Xie L, Makinia J. Modeling the effect of external carbon source addition under different electron acceptor conditions in biological nutrient removal activated sludge systems. Environ Sci Technol 2016; 50: 1887–1896.10.1021/acs.est.5b04849Search in Google Scholar PubMed

Hu Z, Lu X, Sun P, Hu Z, Wang R, Lou C, Han J. Understanding the performance of microbial community induced by ZnO nanoparticles in enhanced biological phosphorus removal system and its recoverability. Bioresour Technol 2017; 225: 279–285.10.1016/j.biortech.2016.11.080Search in Google Scholar PubMed

Huang W, Huang W, Li H, Lei Z, Zhang Z, Tay JH, Lee DJ. Species and distribution of inorganic and organic phosphorus in enhanced phosphorus removal aerobic granular sludge. Bioresour Technol 2015; 193: 549–552.10.1016/j.biortech.2015.06.120Search in Google Scholar PubMed

Huang H, Chen Y, Zheng X, Su Y, Wan R, Yang S. Distribution of tetracycline resistance genes in anaerobic treatment of waste sludge: the role of pH in regulating tetracycline resistant bacteria and horizontal gene transfer. Bioresour Technol 2016; 218: 1284–1289.10.1016/j.biortech.2016.07.097Search in Google Scholar PubMed

Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN. Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 2014; 7: 60–72.10.2478/intox-2014-0009Search in Google Scholar PubMed PubMed Central

Jiang Y, Hebly M, Kleerebezem R, Muyzer G, van Loosdrecht MCM. Metabolic modeling of mixed substrate uptake for polyhydroxyalkanoate (PHA) production. Water Res 2011; 45: 1309–1321.10.1016/j.watres.2010.10.009Search in Google Scholar PubMed

Joshi N, Ngwenya BT, French CE. Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances. J Hazard Mater 2012; 241–242: 363–370.10.1016/j.jhazmat.2012.09.057Search in Google Scholar PubMed

Kang F, Alvarez PJ, Zhu D. Microbial extracellular polymeric substances reduce Ag+ to silver nanoparticles and antagonize bactericidal activity. Environ Sci Technol 2014a; 48: 316–322.10.1021/es403796xSearch in Google Scholar

Kang D, Tang H, Xie D, Ke P. Adsorption abilities by heavy metals and inorganic particles and activated sludge in domestic wastewater treatment plant. J Chem Pharm Res 2014b; 6: 2918–2926.Search in Google Scholar

Karvelas M, Katsoyiannis A, Samara C. Occurrence and fate of heavy metals in the wastewater treatment process. Chemosphere 2003; 53: 1201–1210.10.1016/S0045-6535(03)00591-5Search in Google Scholar

Kazadi Mbamba C, Batstone DJ, Flores-Alsina X, Tait S. A generalized chemical precipitation modelling approach in wastewater treatment applied to calcite. Water Res 2015a; 68: 342–353.10.1016/j.watres.2014.10.011Search in Google Scholar PubMed

Kazadi Mbamba C, Tait S, Flores-Alsina X, Batstone DJ. A systematic study of multiple minerals precipitation modelling in wastewater treatment. Water Res 2015b; 85: 359–370.10.1016/j.watres.2015.08.041Search in Google Scholar PubMed

Kim SW, An Y-J. Effect of ZnO and TiO2 nanoparticles preilluminated with UVA and UVB light on Escherichia coli and Bacillus subtilis. Appl Microbiol Biotechnol 2012; 95: 243–253.10.1007/s00253-012-4153-6Search in Google Scholar PubMed

Kiser MA, Westerhoff P, Benn T, Wang Y, Perez-Rivera J, Hristovski K. Titanium nanomaterial removal and release from wastewater treatment plants. Environ Sci Technol 2009; 43: 6757–6763.10.1021/es901102nSearch in Google Scholar PubMed

Kiser MA, Ryu H, Jang H, Hristovski K, Westerhoff P. Biosorption of nanoparticles to heterotrophic wastewater biomass. Water Res 2010; 44: 4105–4114.10.1016/j.watres.2010.05.036Search in Google Scholar PubMed

Kozlowski H, Kolkowska P, Watly J, Krzywoszynska K, Potocki S. General aspects of metal toxicity. Curr Med Chem 2014; 21: 3721–3740.10.2174/0929867321666140716093838Search in Google Scholar PubMed

Kumar AVA, Hashimi SA, Hilal N. Investigation of kinetics and mechanism involved in the biosorption of heavy metals on activated sludge. Int J Green Energy 2008; 5: 313–321.10.1080/15435070802229068Search in Google Scholar

Leonard SS, Bower JJ, Shi X. Metal-induced toxicity, carcinogenesis, mechanisms and cellular responses. Mol Cell Biochem 2004; 255: 3–10.10.1023/B:MCBI.0000007255.72746.a6Search in Google Scholar

Li WW, Yu HQ. Insight into the roles of microbial extracellular polymer substances in metal biosorption. Bioresour Technol 2014; 160: 15–23.10.1016/j.biortech.2013.11.074Search in Google Scholar PubMed

Li N, Ren NQ, Wang XH, Kang H. Effect of temperature on intracellular phosphorus absorption and extra-cellular phosphorus removal in EBPR process. Bioresour Technol 2010; 101: 6265–6268.10.1016/j.biortech.2010.03.008Search in Google Scholar PubMed

Li M, Zhu L, Lin D. Toxicity of ZnO nanoparticles to Escherichia coli: mechanism and the influence of medium components. Environ Sci Technol 2011; 45: 1977–1983.10.1021/es102624tSearch in Google Scholar PubMed

Li L, Hartmann G, Doüblinger M, Schuster M. Quantification of nanoscale silver particles removal and release from municipal wastewater treatment plants in Germany. Environ Sci Technol 2013a; 47: 7317–7323.10.1021/es3041658Search in Google Scholar PubMed

Li M, Lin D, Zhu L. Effects of water chemistry on the dissolution of ZnO nanoparticles and their toxicity to Escherichia coli. Environ Pollut 2013b; 173: 97–102.10.1016/j.envpol.2012.10.026Search in Google Scholar PubMed

Li Y, Zou J, Zhang L, Sun J. Aerobic granular sludge for simultaneous accumulation of mineral phosphorus and removal of nitrogen via nitrite in wastewater. Bioresour Technol 2014; 154: 178–184.10.1016/j.biortech.2013.12.033Search in Google Scholar PubMed

Li G, Puyol D, Carvajal-Arroyo JM, Sierra-Alvarez R, Field JA. Inhibition of anaerobic ammonium oxidation by heavy metals. J Chem Technol Biotechnol 2015a; 90: 830–837.10.1002/jctb.4377Search in Google Scholar

Li WW, Zhang HL, Sheng GP, Yu HQ. Roles of extracellular polymeric substances in enhanced biological phosphorus removal process. Water Res 2015b; 86: 85–95.10.1016/j.watres.2015.06.034Search in Google Scholar PubMed

Liao C, Tsai J, Ling M, Liang H, Chou Y, Yang P. Organ-specific toxicokinetics and dose-response of arsenic in tilapia Oreochromis mossambicus. Arch Environ Contam Toxicol 2004; 47: 502–510.10.1007/s00244-004-3105-2Search in Google Scholar PubMed

Limousin G, Gaudet J-P, Charlet L, Szenknect S, Barthès V, Krimissa M. Sorption isotherms: a review on physical bases, modeling and measurement. Appl Geochem 2007; 22: 249–275.10.1016/j.apgeochem.2006.09.010Search in Google Scholar

Lin D, Story D, Walker SL, Huang Q, Cai P. Influence of extracellular polymeric substances on the aggregation kinetics of TiO2 nanoparticles. Water Res 2016; 10: 381–388.10.1016/j.watres.2016.08.044Search in Google Scholar PubMed

Liu YQ, Lowry GV. Effect of particle age (Fe0 content) and solution pH on NZVI reactivity: H2 evolution and TCE dechlorination. Environ Sci Technol 2006; 40: 6085–6090.10.1021/es060685oSearch in Google Scholar PubMed

Liu J, Pennell KG, Hurt RH. Kinetics and mechanisms of nanosilver oxysulfidation. Environ Sci Technol 2011; 45: 7345–7353.10.1021/es201539sSearch in Google Scholar PubMed PubMed Central

Liu SH, Zeng GM, Niu QY, Liu Y, Zhou L, Jiang LH, Tan XF, Xu P, Zhang C, Cheng M. Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour Technol 2017; 224: 25–33.10.1016/j.biortech.2016.11.095Search in Google Scholar PubMed

Liu Z, Zhou H, Liu J, Huang M, Yin X, Liu Z, Mao Y, Xie W, LiD. Evaluation of performance and microbial community successional patterns in an integrated OCO reactor under ZnO nanoparticle stress. RSC Adv 2018; 8: 26928–26933.10.1039/C8RA05057KSearch in Google Scholar

Lopez-Vazquez CM, Oehmen A, Hooijmans CM, Brdjanovic D, Gijzen HJ, Yuan Z, Van Loosdrecht MCM. Modeling the PAO-GAO competition: effects of carbon source, pH and temperature. Water Res 2009; 43: 450–462.10.1016/j.watres.2008.10.032Search in Google Scholar PubMed

Ma B, Wang S, Li Z, Gao M, Li S, Guo L, She Z, Zhao Y, Zheng D, Jin C, Wang X, Gao F. Magnetic Fe3O4 nanoparticles induced effects on performance and microbial community of activated sludge from a sequencing batch reactor under long-term exposure. Bioresour Technol 2017; 225: 377–385.10.1016/j.biortech.2016.11.130Search in Google Scholar PubMed

Ma B, Yu N, Han Y, Gao M, Wang S, Li S, Guo L, She Z, Zhao Y, Jin C, Gao F. Effect of magnesium oxide nanoparticles on microbial diversity and removal performance of sequencing batch reactor. J Environ Manag 2018; 222: 475–482.10.1016/j.jenvman.2018.05.089Search in Google Scholar PubMed

Magdolenova Z, Collins A, Kumar A, Dhawan A, Stones V, Dusinska M. Mechanisms of genotoxicity. A review of in vitro and in vivo studies with engineered nanoparticles. Nanotoxicology 2014; 8: 233–278.10.3109/17435390.2013.773464Search in Google Scholar PubMed

Masaki S, Nakano Y, Ichiyoshi K, Kawamoto K, Takeda A, Ohnuki T, Hochella MF, Utsunomiya S. Adsorption of extracellular polymeric substances derived from S. cerevisiae to Ceria nanoparticles and the effects on their colloidal stability. Environments 2017; 4: 48.10.3390/environments4030048Search in Google Scholar

Massara TM, Solís B, Guisasola A, Katsou E, Baeza JA. Development of an ASM2d-N2O model to describe nitrous oxide emissions in municipal WWTPs under dynamic conditions. Chem Eng J 2018; 335: 185–196.10.1016/j.cej.2017.10.119Search in Google Scholar

Meijer SCF, van Loosdrecht MCM, Heijnen JJ. Metabolic modelling of full-scale biological nitrogen and phosphorus removing WWTP’s. Water Res 2001; 35: 2711–2723.10.1016/S0043-1354(00)00567-4Search in Google Scholar

Miao L, Wang C, Hou J, Wang P, Ao Y, Li Y, Lv B, Yang Y, You G, Xu Y. Enhanced stability and dissolution of CuO nanoparticles by extracellular polymeric substances in aqueous environment. J Nanopart Res 2015; 17: 404.10.1007/s11051-015-3208-xSearch in Google Scholar

Miao L, Wang C, Hou J, Wang P, Ao Y, Li Y, Yao Y, Lv B, Yang Y, You G, Xu Y, Gu Q. Response of wastewater biofilm to CuO nanoparticle exposure in terms of extracellular polymeric substances and microbial community structure. Sci Total Environ 2017; 579: 588–597.10.1016/j.scitotenv.2016.11.056Search in Google Scholar

More TT, Yadav JSS, Yan S, Tyagi RD, Surampalli RY. Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manag 2014; 144: 1–25.10.1016/j.jenvman.2014.05.010Search in Google Scholar

Moura DJ, Péres VF, Jacques RA, Saffi J. Heavy metal toxicity: oxidative stress parameters and DNA repair. In: Gupta DK, Sandalio LM, editors. Metal toxicity in plants: perception, signaling and remediation. Berlin Heidelberg: Springer-Verlag, 2012: 187–205.10.1007/978-3-642-22081-4_9Search in Google Scholar

Mu H, Zheng X, Chen Y, Chen H, Liu K. Response of anaerobic granular sludge to a shock load of zinc oxide nanoparticles during biological wastewater treatment. Environ Sci Technol 2012; 46: 5997–6003.10.1021/es300616aSearch in Google Scholar

Musvoto E, Wentzel M, Loewenthal R, Ekama G. Integrated chemical-physical processes modelling – I. Development of a kinetic-based model for mixed weak acid/base systems. Water Res 2000a; 34: 1857–1867.10.1016/S0043-1354(99)00334-6Search in Google Scholar

Musvoto E, Wentzel M, Loewenthal R, Ekama G. Integrated chemical-physical processes modelling – II. Simulating aeration treatment of anaerobic digester supernatants. Water Res 2000b; 34: 1868–1880.10.1016/S0043-1354(99)00335-8Search in Google Scholar

Nagata T, Kiyono M, Pan-Hou H. Engineering expression of bacterial polyphosphate kinase in tobacco for mercury remediation. Appl Microbiol Biotechnol 2006; 72: 777–782.10.1007/s00253-006-0336-3Search in Google Scholar PubMed

Natarajan R, Manivasagan R. Biosorptive removal of heavy metal onto raw activated sludge: parametric, equilibrium, and kinetic Studies. J Environ Eng 2016; 142: C4015002.10.1061/(ASCE)EE.1943-7870.0000961Search in Google Scholar

Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science 2006; 311: 622–627.10.1126/science.1114397Search in Google Scholar PubMed

Oehmen A, Lemos PC, Carvalho G, Yuan Z, Keller J, Blackall LL, Reis MAM. Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res 2007; 41: 2271–2300.10.1016/j.watres.2007.02.030Search in Google Scholar PubMed

Oehmen A, Lopez-Vaquez CM, Carvalho G, Reis MAM, van Loosdrecht MCM. Modelling the population dynamics and metabolic diversity of organisms relevant in anaerobic/anoxic/aerobic enhanced biological phosphorus removal processes. Water Res 2010; 44: 4473–4486.10.1016/j.watres.2010.06.017Search in Google Scholar PubMed

Ong S, Toorisaka E, Hirata M, Hano T. Adsorption and toxicity of heavy metals on activated sludge. ScienceAsia 2010; 36: 204–209.10.2306/scienceasia1513-1874.2010.36.204Search in Google Scholar

Pagnanelli F, Mainelli S, Bornoroni L, Dionisi D, Toro L. Mechanisms of heavy-metal removal by activated sludge. Chemosphere 2009; 75: 1028–1034.10.1016/j.chemosphere.2009.01.043Search in Google Scholar PubMed

Pamukoglu MY, Kargi F. Mathematical modeling of copper(II) ion inhibition on COD removal in an activated sludge unit. J Hazard Mater 2007; 146: 372–377.10.1016/j.jhazmat.2006.12.033Search in Google Scholar PubMed

Pardo R, Herguedas M, Barrado E, Vega M. Biosorption of cadmium, copper, lead and zinc by inactive biomass of Pseudomonas putida. Anal Bioanal Chem 2003; 376: 26–32.10.1007/s00216-003-1843-zSearch in Google Scholar PubMed

PAS71 (Publicly Available Specification). Vocabulary-Nanoparticles. British Standards Institution (BSI), 2005.Search in Google Scholar

Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J. The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell Biol 2009; 41: 1665–1677.10.1016/j.biocel.2009.03.005Search in Google Scholar PubMed

Priester JH, Van De Werfhorst LC, Ge Y, Adeleye AS, Tomar S, Tom LM, Piceno YM, Andersen GL, Holden PA. Effects of TiO2 and Ag nanoparticles on polyhydroxybutyrate biosynthesis by activated sludge bacteria. Environ Sci Technol 2014; 48: 14712–14720.10.1021/es504117xSearch in Google Scholar PubMed

Puay N, Qiu G, Ting Y. Effect of Zinc oxide nanoparticles on biological wastewater treatment in a sequencing batch reactor. J Clean Prod 2015; 88: 139–145.10.1016/j.jclepro.2014.03.081Search in Google Scholar

Pulicharla R, Hegde K, Brar SK, Surampalli RY. Tetracyclines metal complexation: significance and fate of mutual existence in the environment. Environ Pollut 2017; 221: 1–14.10.1016/j.envpol.2016.12.017Search in Google Scholar

Rayne S, Carey S, Forest K. Evidence for tin Inhibition of enhanced biological phosphorus removal at a municipal wastewater treatment plant. J Environ Sci Heal Part A 2005; 40: 535–551.10.1081/ESE-200046557Search in Google Scholar

Ren TT, Liu L, Sheng GP, Liu XW, Yu HQ, Zhang MC, Zhu JR. Calcium spatial distribution in aerobic granules and its effects on granule structure, strength and bioactivity. Water Res 2008; 42: 3343–3352.10.1016/j.watres.2008.04.015Search in Google Scholar

Rieger L, Koch G, Kuhni M, Gujer W, Siegrist H. The EAWAG Bio-P module for activated sludge model no. 3. Water Res 2001; 35: 3887–3903.10.1016/S0043-1354(01)00110-5Search in Google Scholar

Roco MC. The long view of nanotechnology development: the National Nanotechnology Initiative at 10 years. J Nanopart Res 2011; 13: 427–445.10.1007/978-94-007-1168-6_1Search in Google Scholar

Schützendübel A, Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 2002; 53: 1351–1365.10.1093/jexbot/53.372.1351Search in Google Scholar

Şengör SS¸ Barua S, Gikas P, Ginn TR, Peyton B, Sani RK, Spycher NF. Influence of heavy metals on microbial growth kinetics including lag time: mathematical modeling and experimental verification. Environ Toxicol Chem 2009; 28: 2020–2029.10.1897/08-273.1Search in Google Scholar PubMed

Sheng GP, Yu HQ, Yue ZB. Production of EPS from Rhodopseudomonas acidophila in the presence of toxic substances. Appl Microbiol Biotechnol 2005; 69: 216–222.10.1007/s00253-005-1990-6Search in Google Scholar PubMed

Sheng GP, Yu HQ, Li XY. Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 2010; 28: 882–894.10.1016/j.biotechadv.2010.08.001Search in Google Scholar PubMed

Sheng GP, Xu J, Li WH, Yu HQ. Quantification of the interactions between Ca2+, Hg2+ and extracellular polymeric substances (EPS) of sludge. Chemosphere 2013; 93: 1436–1441.10.1016/j.chemosphere.2013.07.076Search in Google Scholar PubMed

Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC, Bakhori SKM, Hasan H, Mohamad D. Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro Lett 2015; 7: 219–242.10.1007/s40820-015-0040-xSearch in Google Scholar PubMed PubMed Central

Smeraldi J, Rajagopalan G, Cooper WJ, Hosseini T, Rosso D. Precipitation, adsorption and inhibitory effects of nano copper in activated sludge. Nanotechnology 2010; 3: 616–619.10.2175/193864710798158003Search in Google Scholar

Smolders GJF, Vandermeij J, Vanloosdrecht MCM, Heijnen JJ. Model of the anaerobic metabolism of the biological phosphorus removal process – stoichiometry and pH influence. Biotechnol Bioeng 1994a; 43: 461–470.10.1002/bit.260430605Search in Google Scholar PubMed

Smolders GJF, Vandermeij J, Vanloosdrecht MCM, Heijnen JJ. Stoichiometric model of the aerobic metabolism of the biological phosphorus removal process. Biotechnol Bioeng 1994b; 44: 837–848.10.1002/bit.260440709Search in Google Scholar PubMed

Smolders GJF, Vandermeij J, Vanloosdrecht MCM, Heijnen JJ. A structured metabolic model for anaerobic and aerobic stoichiometry and kinetics of the biological phosphorus removal process. Biotechnol Bioeng 1995; 47: 277–287.10.1002/bit.260470302Search in Google Scholar PubMed

Su Y, Chen Y, Zheng X, Wan R, Huang H, Li M, Wu L. Using sludge fermentation liquid to reduce the inhibitory effect of copper oxide nanoparticles on municipal wastewater biological nutrient removal. Water Res 2016; 99: 216–224.10.1016/j.watres.2016.04.066Search in Google Scholar PubMed

Sun P, Wang R, Fang Z. Fully coupled activated sludge model (FCASM): model development. Bioresour Technol 2009; 100: 4632–4641.10.1016/j.biortech.2009.04.065Search in Google Scholar PubMed

Sun J, Yang Q, Wang D, Wang S, Chen F, Zhong Y, Yi K, Yao F, Jiang C, Li S, Li X, Zeng G. Nickel toxicity to the performance and microbial community of enhanced biological phosphorus removal system. Chem Eng J 2017; 313: 415–423.10.1016/j.cej.2016.12.078Search in Google Scholar

Swinarski M, Makinia J, Stensel HD, Czerwionka K, DrewnowskiJ. Modeling external carbon addition in biological nutrient removal processes with an extension of the International Water Association Activated Sludge Model. Water Environ Res 2012; 84: 646–655.10.2175/106143012X13373550426670Search in Google Scholar

Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metals toxicity and the environment. Exp Suppl 2012; 101: 133–164.10.1007/978-3-7643-8340-4_6Search in Google Scholar

Tian WD, Ma C, Lin Y, Ran ZL. Effect of Mg/Ca molar ratios on characteristics of anaerobic-anoxic denitrifying dephosphatation. Bioresour Technol 2017; 240: 94–97.10.1016/j.biortech.2017.01.063Search in Google Scholar

Tiede K, Boxall ABA, Wang X, Gore D, Tiede D, Baxter M, David H, Tear SP, Lewis J. Application of hydrodynamic chromatography-ICP-MS to investigate the fate of silver nanoparticles in activated sludge. J Anal Atom Spectrom 2010; 25: 1149–1154.10.1039/b926029cSearch in Google Scholar

Tourney J, Ngwenya B. The role of bacterial extracellular polymeric substances in geomicrobiology. Chem Geol 2014; 386: 115–132.10.1016/j.chemgeo.2014.08.011Search in Google Scholar

Tourney J, Ngwenya BT, Mosselmans JWF. Magennis M. Physical and chemical effects of extracellular polymers (EPS) on Zn adsorption to Bacillus licheniformis S-86. J Colloid Interf Sci 2009; 337: 381–389.10.1016/j.jcis.2009.05.067Search in Google Scholar

Tsai YP, Chen HT. Influence of sludge retention time on tolerance of copper toxicity for polyphosphate accumulating organisms linked to poly-hydroxyalkanoates metabolism and phosphate removal. Bioresour Technol 2011; 102: 11043–11047.10.1016/j.biortech.2011.09.050Search in Google Scholar

Tsai YP, Tzeng HF, Lin JW, Lu MS, Lin JY. Verification of enzymes deterioration due to Cu(II) presence in an enhanced biological phosphorus removal system. Chemosphere 2013; 91: 602–607.10.1016/j.chemosphere.2012.11.080Search in Google Scholar

Vaiopoulou E, Gikas P. Effects of chromium on activated sludge and on the performance of wastewater treatment plants: a review. Water Res 2012; 46: 549–570.10.1016/j.watres.2011.11.024Search in Google Scholar

van Kerkhove E, Pennemans V, Swennen Q. Cadmium and transport of ions and substances across cell membranes and epithelia. Biometals 2010; 23: 823–855.10.1007/s10534-010-9357-6Search in Google Scholar

van Veldhuizen HM, van Loosdrecht MCM, Heijnen JJ. Modelling biological phosphorus and nitrogen removal in a full scale activated sludge process. Water Res 1999; 33: 3459–3468.10.1016/S0043-1354(99)00064-0Search in Google Scholar

Vilela P, Liu H, Lee S, Hwangbo S, Nam K, Yoo C. A systematic approach of removal mechanisms, control and optimization of silver nanoparticle in wastewater treatment plants. Sci Total Environ 2018; 633: 989–998.10.1016/j.scitotenv.2018.03.247Search in Google Scholar PubMed

Walden C, Zhang W. Biofilms versus activated sludge: considerations in metal and metal oxide nanoparticle removal from wastewater. Environ Sci Technol 2016; 50: 8417–8431.10.1021/acs.est.6b01282Search in Google Scholar PubMed

Wang D, Chen Y. Critical review of the influences of nanoparticles on biological wastewater treatment and sludge digestion. Crit Rev Biotechnol 2016; 36: 816–828.10.3109/07388551.2015.1049509Search in Google Scholar PubMed

Wang XH, Song RH, Teng SX, Gao MM, Ni JY, Liu FF, Wang SG, Gao BY. Characteristics and mechanisms of Cu(II) biosorption by disintegrated aerobic granules. J Hazard Mater 2010; 179: 431–437.10.1016/j.jhazmat.2010.03.022Search in Google Scholar PubMed

Wang Y, Ren Z, Jiang F, Geng J, He W, Yang J. Effect of copper ion on the anaerobic and aerobic metabolism of phosphorus-accumulating organisms linked to intracellular storage compounds. J Hazard Mater 2011; 186: 313–319.10.1016/j.jhazmat.2010.11.007Search in Google Scholar PubMed

Wang J, Li Q, Li MM, Chen TH, Zhou YF, Yue ZB. Competitive adsorption of heavy metal by extracellular polymeric substances (EPS) extracted from sulfate reducing bacteria. Bioresour Technol 2014a; 163: 374–376.10.1016/j.biortech.2014.04.073Search in Google Scholar PubMed

Wang R, Peng Y, Cheng Z, Ren N. Understanding the role of extracellular polymeric substances in an enhanced biological phosphorus removal granular sludge system. Bioresour Technol 2014b; 169: 307–312.10.1016/j.biortech.2014.06.040Search in Google Scholar PubMed

Wang S, Gao M, Li Z, She Z, Wu J, Zheng D, Guo L, Zhao Y, Gao F, Wang X. Performance evaluation, microbial enzymatic activity and microbial community of a sequencing batch reactor under long-term exposure to cerium dioxide nanoparticles. Water Res 2016a; 99: 216–224.10.1016/j.biortech.2016.08.086Search in Google Scholar PubMed

Wang S, Gao M, She Z, Zheng D, Jin C, Guo L, Zhao Y, Li Z, Wang X. Long-term effects of ZnO nanoparticles on nitrogen and phosphorus removal, microbial activity and microbial community of a sequencing batch reactor. Bioresour Technol 2016b; 216: 428–436.10.1016/j.biortech.2016.05.099Search in Google Scholar PubMed

Wang S, Li Z, Gao M, She Z, Guo L, Zheng D, Zhao Y, Ma B, Gao F, Wang X. Long-term effects of nickel oxide nanoparticles on performance, microbial enzymatic activity, and microbial community of a sequencing batch reactor. Chemosphere 2017a; 169: 387–395.10.1016/j.chemosphere.2016.10.139Search in Google Scholar PubMed

Wang S, Li Z, Gao M, She Z, Ma B, Guo L, Zheng D, Zhao Y, Jin C, Wang X, Gao F. Long-term effects of cupric oxide nanoparticles (CuO NPs) on the performance, microbial community and enzymatic activity of activated sludge in a sequencing batch reactor. J Environ Manag 2017b; 187: 330–339.10.1016/j.jenvman.2016.11.071Search in Google Scholar PubMed

Wang P, You G, Hou J, Wang C, Xu Y, Miao L, Feng T, Zhang F. Responses of wastewater biofilms to chronic CeO2 nanoparticles exposure: structural, physicochemical and microbial properties and potential mechanism. Water Res 2018a; 133: 208–217.10.1016/j.watres.2018.01.031Search in Google Scholar PubMed

Wang X, Zhu M, Li N, Du S, Yang J, Li Y. Effects of CeO2 nanoparticles on bacterial community and molecular ecological network in activated sludge system. Environ Pollut 2018b; 238: 516–523.10.1016/j.envpol.2018.03.034Search in Google Scholar PubMed

Wei L, Li Y, Noguera DR, Zhao N, Song Y, Ding J, Zhao Q, Cui F. Adsorption of Cu2+ and Zn2+ by extracellular polymeric substances (EPS) in different sludges: effect of EPS fractional polarity on binding mechanism. J Hazard Mater 2017; 321: 473–483.10.1016/j.jhazmat.2016.05.016Search in Google Scholar PubMed

Wentzel MC, Ekama GA, Marais GVR. Process and modelling of nitrification denitrification biological excess phosphorus removal systems – a review. Water Sci Technol 1992; 25: 59–82.10.2166/wst.1992.0114Search in Google Scholar

Westerhoff P, Song G, Hristovski K, Kiser MA. Occurrence and removal of titanium at full scale wastewater treatment plants: implications for TiO2 nanomaterials. J Environ Monit 2011; 13: 1195–1203.10.1039/c1em10017cSearch in Google Scholar PubMed

Wu G, Rodgers M. Inhibitory effect of copper on enhanced biological phosphorus removal. Water Sci Technol 2010; 62: 1464–1470.10.2166/wst.2010.431Search in Google Scholar PubMed

Wu D, Shen Y, Ding A, Mahmood Q, Liu S, Tu Q. Effects of nanoscale zero-valent iron particles on biological nitrogen and phosphorus removal and microorganisms in activated sludge. J Hazard Mater 2013; 262: 649–655.10.1016/j.jhazmat.2013.09.038Search in Google Scholar PubMed

Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L. A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res 2016; 23: 8244–8259.10.1007/s11356-016-6333-xSearch in Google Scholar PubMed

Xu Y, Wang C, Hou J, Wang P, You G, Miao L, Lv B, Yang Y. Influence of CeO2 NPs on biological phosphorus removal and bacterial community shifts in a sequencing batch biofilm reactor with the differential effects of molecular oxygen. Environ Res 2016; 151: 21–29.10.1016/j.envres.2016.07.008Search in Google Scholar PubMed

Xu Y, Wang C, Hou J, Wang P, You G, Miao L, Lv B, Yang Y. Effects of cerium oxide nanoparticles on the species and distribution of phosphorus in enhanced phosphorus removal sequencing batch biofilm reactor. Bioresour Technol 2017; 227: 393–397.10.1016/j.biortech.2016.12.041Search in Google Scholar PubMed

Xu Y, Wang C, Hou J, Wang P, Miao L, You G. Strategies and relative mechanisms to attenuate the bioaccumulation and biotoxicity of ceria nanoparticles in wastewater biofilms. Bioresour Technol 2018; 265: 102–109.10.1016/j.biortech.2018.05.107Search in Google Scholar PubMed

Yan P, Xia JS, Chen YP, Liu ZP, Guo JS, Shen Y, Zhang CC, Wang J. Thermodynamics of binding interactions between extracellular polymeric substances and heavy metals by isothermal titration microcalorimetry. Bioresour Technol 2017; 232: 354–363.10.1016/j.biortech.2017.02.067Search in Google Scholar PubMed

Yanamala N, Kagan VE, Shvedova AA. Molecular modeling in structural nano-toxicology: interactions of nano-particles with nano-machinery of cells. Adv Drug Deliv Rev 2013; 65: 2070–2077.10.1016/j.addr.2013.05.005Search in Google Scholar PubMed PubMed Central

Yang Y, Chen Q, Wall J, Hu Z. Potential nanosilver impact on anaerobic digestion at moderate silver concentrations. Water Res 2011; 46: 1176–1184.10.1016/j.watres.2011.12.024Search in Google Scholar PubMed

Yang M, Sun P, Wang R, Han J, Wang J, Song Y, Cai J, Tang X. Simulation and optimization of ammonia removal at low temperature for a double channel oxidation ditch based on fully coupled activated sludge model (FCASM): a full-scale study. Bioresour Technol 2013a; 143: 538–548.10.1016/j.biortech.2013.06.029Search in Google Scholar PubMed

Yang Y, Zhang C, Hu Z. Impact of metallic and metal oxide nanoparticles on wastewater treatment and anaerobic digestion. Environ Sci Proc Impacts 2013b; 15: 39–48.10.1039/C2EM30655GSearch in Google Scholar PubMed

Yang SS, Pang JW, Guo WQ, Yang XY, Wu ZY, Ren NQ, Zhao ZQ. Biological phosphorus removal in an extended ASM2 model: Roles of extracellular polymeric substances and kinetic modeling. Bioresour Technol 2017a; 232: 412–416.10.1016/j.biortech.2017.01.048Search in Google Scholar PubMed

Yang Q, Sun J, Wang D, Wang S, Chen F, Yao F, An H, Zhong Y, Xie T, Wang Y, Li X, Zeng G. Effect of nickel on the flocculability, settleability, and dewaterability of activated sludge. Bioresour Technol 2017b; 224: 188–196.10.1016/j.biortech.2016.11.018Search in Google Scholar PubMed

Yilmazer P, Saracoglu N. Bioaccumulation and biosorption of copper(II) and chromium(III) from aqueous solutions by Pichia stipitis yeast. J Chemical Technol Biotechnol 2009; 84: 604–610.10.1002/jctb.2088Search in Google Scholar

Ying J, Zhang T, Tang M. Metal oxide nanomaterial QNAR models: available structural descriptors and understanding of toxicity mechanisms. Nanomaterials 2015; 5: 1620–1637.10.3390/nano5041620Search in Google Scholar PubMed PubMed Central

You SL, Tsai YP, Huang RY. Effects of heavy metals on the specific ammonia and nitrate uptake rates in activated sludge. Environ Eng Sci 2009; 26: 1207–1214.10.1089/ees.2008.0186Search in Google Scholar

You SJ, Tsai YP, Cho BC, Chou YH. Metabolic influence of lead on polyhydroxyalkanoates (PHA) production and phosphate uptake in activated sludge fed with glucose or acetic acid as carbon source. Bioresour Technol 2011; 102: 8165–8170.10.1016/j.biortech.2011.06.022Search in Google Scholar PubMed

You G, Hou J, Xu Y, Wang C, Wang P, Miao L, Ao Y, Li Y, Lv B. Effects of CeO2 nanoparticles on production and physicochemical characteristics of extracellular polymeric substances in biofilms in sequencing batch biofilm reactor. Bioresour Technol 2015; 194: 91–98.10.1016/j.biortech.2015.07.006Search in Google Scholar PubMed

Yu R, Fang X, Somasundaran P, Chandran K. Short-term effects of TiO2, CeO2, and ZnO nanoparticles on metabolic activities and gene expression of Nitrosomonas europaea. Chemosphere 2015; 128: 207–215.10.1016/j.chemosphere.2015.02.002Search in Google Scholar PubMed

Yuncu B, Sanin FD, Yetis U. An investigation of heavy metal biosorption in relation to C/N ratio of activated sludge. J Hazard Mater 2006; 137: 990–997.10.1016/j.jhazmat.2006.03.020Search in Google Scholar PubMed

Zhang HL, Fang W, Wan YP, Sheng GP, Zeng RJ, Li WW, Yu HQ. Phosphorus removal in an enhanced biological phosphorus removal process: roles of extracellular polymeric substances. Environ Sci Technol 2013a; 47: 11482–11489.10.1021/es403227pSearch in Google Scholar PubMed

Zhang HL, Fang W, Wang YP, Sheng GP, Xia CW, Zeng RJ, Yu HQ. Species of phosphorus in the extracellular polymeric substances of EBPR sludge. Bioresour Technol 2013b; 142: 714–718.10.1016/j.biortech.2013.05.068Search in Google Scholar PubMed

Zhang HL, Sheng GP, Fang W, Wang YP, Fang CY, Shao LM, Yu HQ. Calcium effect on the metabolic pathway of phosphorus accumulating organisms in enhanced biological phosphorus removal systems. Water Res 2015a; 84: 171–180.10.1016/j.watres.2015.07.042Search in Google Scholar PubMed

Zhang QQ, Zhang ZZ, Guo Q, Wang JJ, Wang HZ, Jin RC. Analyzing the revolution of anaerobic ammonium oxidation (anammox) performance and sludge characteristics under zinc inhibition. Appl Microbiol Biotechnol 2015b; 99: 3221–3232.10.1007/s00253-014-6205-6Search in Google Scholar PubMed

Zhang D, Trzcinski AP, Oh H, Chew E, Liu Y, Tan SK, Ng WJ. Comparison of the effects and distribution of zinc oxide nanoparticles and zinc ions in activated sludge reactors. J Environ Sci Heal A 2017; 52: 1073–1081.10.1080/10934529.2017.1338896Search in Google Scholar PubMed

Zheng X, Chen Y, Wu R. Long-term effects of titanium dioxide nanoparticles on nitrogen and phosphorus removal from wastewater and bacterial community shift in activated sludge. Environ Sci Technol 2011a; 45: 7284–7290.10.1021/es2008598Search in Google Scholar PubMed

Zheng X, Wu R, Chen Y. Effects of ZnO nanoparticles on wastewater biological nitrogen and phosphorus removal. Environ Sci Technol 2011b; 45: 2826–2832.10.1021/es2000744Search in Google Scholar PubMed

Zheng X, Su Y, Chen Y. Acute and chronic responses of activated sludge viability and performance to silica nanoparticles. Environ Sci Technol 2012; 46: 7182–7188.10.1021/es300777bSearch in Google Scholar PubMed

Zheng X, Sun P, Han J, Song Y, Hu Z, Fan H, Lv S. Inhibitory factors affecting the process of enhanced biological phosphorus removal (EBPR) – a mini-review. Process Biochem 2014; 49: 2207–2213.10.1016/j.procbio.2014.10.008Search in Google Scholar

Zheng X, Wang J, Chen Y, Wei Y. Comprehensive analysis of transcriptional and proteomic profiling reveals silver nanoparticles-induced toxicity to bacterial denitrification. J Hazard Mater 2018a; 344: 291–298.10.1016/j.jhazmat.2017.10.028Search in Google Scholar PubMed

Zheng X, Zhou W, Wan R, Luo J, Su Y, Huang H, Chen Y. Increasing municipal wastewater BNR by using the preferred carbon source derived from kitchen wastewater to enhance phosphorus uptake and short-cut nitrification-denitrification. Chem Eng J 2018b; 344: 556–564.10.1016/j.cej.2018.03.124Search in Google Scholar

Zhou Y, Zhang Z, Zhang J, Xia S. Understanding key constituents and feature of the biopolymer in activated sludge responsible for binding heavy metals. Chem Eng J 2016; 304: 527–532.10.1016/j.cej.2016.06.115Search in Google Scholar

Ziolko D, Martin OV, Scrimshaw MD, Lester JN. An evaluation of metal removal during wastewater treatment: the potential to achieve more stringent final effluent standards. Crit Rev Environ Sci Tec 2011; 41: 733–769.10.1080/10643380903140299Search in Google Scholar

Received: 2018-10-19
Accepted: 2019-02-05
Published Online: 2019-05-21
Published in Print: 2020-11-25

©2019 Walter de Gruyter GmbH, Berlin/Boston

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