Abstract
Periodic chemical cleaning with sodium hypochlorite (NaClO) is essential to restore the membrane permeability in a membrane bioreactor (MBR). However, the chlorination of membrane foulants results in the formation of disinfection by-products (DBPs), which will cause the deterioration of the MBR effluent and increase the antibiotic resistance in bacteria in the MBR tank. In this study, the formation of 14 DBPs during chemical cleaning offouled MBR membrane modules was investigated. Together with the effects of biofilm extracellular polymeric substances (EPS), influences of reaction time, NaClO dosage, initial pH, and cleaning temperature on the DBP formation were investigated. Haloacetic acids (HAAs) and trichloromethane (TCM), composed over 90% of the DBPs, were increasingly accumulated as the NaClO cleaning time extended. By increasing the chlorine dosage, temperature, and pH, the yield of TCM and dichloroacetic acid (DCAA) was increased by up to a factor of 1–14, whereas the yields of haloacetonitriles (HANs) and haloketones (HKs) were decreased. Either decreasing in the chlorine dosage and cleaning temperature or adjusting the pH of cleaning reagents toward acidic or alkaline could effectively reduce the toxic risks caused by DBPs. After the EPS extraction pretreatment, the formation of DBPs was accelerated in the first 12 h due to the damage of biofilm structure. Confocal laser scanning microscopy (CLSM) images showed that EPS, particularly polysaccharides, were highly resistant to chlorine and might be able to protect the cells exposed to chlorination.

Electronic Supplementary Material
Supplementary material is available in the online version of this article at 10.1007/s11783-021-1389-3 and is accessible for authorized users.
Keywords: MBR, Biofouling, EPS, Chemical cleaning, DBPs, CLSM
Electronic Supplementary Material
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 51808316) and the Natural Science Foundation of Shandong Province (Grant No. ZR2019BEE015). In addition, we thank Xiaomin Zhao, Haiyan Yu, and Sen Wang from the State Key Laboratory of Microbial Technology for assistance with confocal imaging.
Footnotes
Highlights
• HAAs was dominant among the DBPs of interest.
• Rising time, dose, temperature and pH raised TCM and HAAs but reduced HANs and HKs.
• Low time, dose and temperature and non-neutrality pH reduced toxic risks of DBPs.
• The presence of EPS decelerated the production of DBPs.
• EPS, particularly polysaccharides were highly resistant to chlorine.
References
- Alasonati E, Slaveykova VI. Effects of extraction methods on the composition and molar mass distributions of exopolymeric substances of the bacterium Sinorhizobium meliloti. Bioresource Technology. 2012;114:603–609. doi: 10.1016/j.biortech.2012.03.071. [DOI] [PubMed] [Google Scholar]
- Berry D, Holder D, Xi C, Raskin L. Comparative transcriptomics of the response of Escherichia coli to the disinfectant monochloramine and to growth conditions inducing monochloramine resistance. Water Research. 2010;44(17):4924–4931. doi: 10.1016/j.watres.2010.07.026. [DOI] [PubMed] [Google Scholar]
- Cai W, Han J, Zhang X, Liu Y. Formation mechanisms of emerging organic contaminants during on-line membrane cleaning with NaOCl in MBR. Journal of Hazardous Materials. 2020;386:121966. doi: 10.1016/j.jhazmat.2019.121966. [DOI] [PubMed] [Google Scholar]
- Cai W, Liu J, Zhu X, Zhang X, Liu Y. Fate of dissolved organic matter and byproducts generated from on-line chemical cleaning with sodium hypochlorite in MBR. Chemical Engineering Journal. 2017;323:233–242. doi: 10.1016/j.cej.2017.04.099. [DOI] [Google Scholar]
- Chen B. Hydrolytic stabilities of halogenated disinfection byproducts: Review and rate constant quantitative structure-property relationship analysis. Environmental Engineering Science. 2011;28(6):385–394. doi: 10.1089/ees.2010.0196. [DOI] [Google Scholar]
- Chowdhury S, Champagne P, James Mclellan P. Investigating effects of bromide ions on trihalomethanes and developing model for predicting bromodichloromethane in drinking water. Water Research. 2010;44(7):2349–2359. doi: 10.1016/j.watres.2009.12.042. [DOI] [PubMed] [Google Scholar]
- Chu W, Gao N, Krasner S W, Templeton M R, Yin D. Formation of halogenated C-, N-DBPs from chlor(am)ination and UV irradiation of tyrosine in drinking water. Environmental Pollution. 2012;161:8–14. doi: 10.1016/j.envpol.2011.09.037. [DOI] [PubMed] [Google Scholar]
- Chu W, Li X, Bond T, Gao N, Bin X, Wang Q, Ding S. Copper increases reductive dehalogenation of haloacetamides by zero-valent iron in drinking water: Reduction efficiency and integrated toxicity risk. Water Research. 2016;107:141–150. doi: 10.1016/j.watres.2016.10.047. [DOI] [PubMed] [Google Scholar]
- Chu W H, Gao N Y, Deng Y, Dong B Z. Formation of chloroform during chlorination of alanine in drinking water. Chemosphere. 2009;77(10):1346–1351. doi: 10.1016/j.chemosphere.2009.09.030. [DOI] [PubMed] [Google Scholar]
- Ding A, Zhao Y, Ngo H H, Bai L, Li G, Liang H, Ren N, Nan J. Metabolic uncoupler, 3,3’,4’,5-tetrachlorosalicylanilide addition for sludge reduction and fouling control in a gravity-driven membrane bioreactor. Frontiers of Environmental Science & Engineering. 2020;14(6):96. doi: 10.1007/s11783-020-1275-4. [DOI] [Google Scholar]
- Ding A, Zhao Y, Yan Z, Bai L, Yang H, Liang H, Li G, Ren N. Co-application of energy uncoupling and ultrafiltration in sludge treatment: Evaluations of sludge reduction, supernatant recovery and membrane fouling control. Frontiers of Environmental Science & Engineering. 2020;14(4):59. doi: 10.1007/s11783-020-1238-9. [DOI] [Google Scholar]
- Fang J, Ma J, Yang X, Shang C. Formation of carbonaceous and nitrogenous disinfection by-products from the chlorination of Microcystis aeruginosa. Water Research. 2010;44(6):1934–1940. doi: 10.1016/j.watres.2009.11.046. [DOI] [PubMed] [Google Scholar]
- Garrido-Baserba M, Asvapathanagul P, Mccarthy G W, Gocke T E, Olson B H, Park H D, Al-Omari A, Murthy S, Bott C B, Wett B, Smeraldi J D, Shaw A R, Rosso D. Linking biofilm growth to fouling and aeration performance of fine-pore diffuser in activated sludge. Water Research. 2016;90:317–328. doi: 10.1016/j.watres.2015.12.011. [DOI] [PubMed] [Google Scholar]
- Gordon C A, Hodges N A, Marriott C. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. Journal of Antimicrobial Chemotherapy. 1988;22(5):667–674. doi: 10.1093/jac/22.5.667. [DOI] [PubMed] [Google Scholar]
- Guo X, Li C, Li C, Wei T, Tong L, Shao H, Zhou Q, Wang L, Liao Y. G-CNTs/PVDF mixed matrix membranes with improved antifouling properties and filtration performance. Frontiers of Environmental Science & Engineering. 2019;13(6):81. doi: 10.1007/s11783-019-1165-9. [DOI] [Google Scholar]
- Joo S H, Mitch W A. Nitrile, aldehyde, and halonitroalkane formation during chlorination/chloramination of primary amines. Environmental Science & Technology. 2007;41(4):1288–1296. doi: 10.1021/es0612697. [DOI] [PubMed] [Google Scholar]
- Luong T V, Peters C J, Perry R. Influence of bromide and ammonia upon the formation of trihalomethanes under water-treatment conditions. Environmental Science & Technology. 1982;16(8):473–479. doi: 10.1021/es00102a009. [DOI] [Google Scholar]
- Lv L, Jiang T, Zhang S, Yu X. Exposure to mutagenic disinfection byproducts leads to increase of antibiotic resistance in Pseudomonas aeruginosa. Environmental Science & Technology. 2014;48(14):8188–8195. doi: 10.1021/es501646n. [DOI] [PubMed] [Google Scholar]
- Ma D, Gao B, Wang Y, Yue Q, Li Q. Factors affecting trihalomethane formation and speciation during chlorination of reclaimed water. Water Science and Technology. 2015;72(4):616–622. doi: 10.2166/wst.2015.260. [DOI] [PubMed] [Google Scholar]
- Nikolaou A D, Golfinopoulos S K, Kostopoulou M N, Lekkas T D. Decomposition of dihaloacetonitriles in water solutions and fortified drinking water samples. Chemosphere. 2000;41(8):1149–1154. doi: 10.1016/S0045-6535(00)00025-4. [DOI] [PubMed] [Google Scholar]
- Pellicer-Nàcher C, Domingo-Félez C, Mutlu A G, Smets B F. Critical assessment of extracellular polymeric substances extraction methods from mixed culture biomass. Water Research. 2013;47(15):5564–5574. doi: 10.1016/j.watres.2013.06.026. [DOI] [PubMed] [Google Scholar]
- Plewa, M J, Wagner E D. Charting a new path to resolve the adverse health effects of DBPs (2015). In: Karanfil T, Mitch B, Westerhoff B, Xie Y F. Recent advances in disinfection by-products. Washington, DC: American Chemical Society, 1190: 3–23
- Sirivedhin T, Gray K A. 2. Comparison of the disinfection by-product formation potentials between a wastewater effluent and surface waters. Water Research. 2005;39(6):1025–1036. doi: 10.1016/j.watres.2004.11.031. [DOI] [PubMed] [Google Scholar]
- Sun H, Liu H, Han J, Zhang X, Cheng F, Liu Y. Chemical cleaning-associated generation of dissolved organic matter and halogenated byproducts in ceramic MBR: Ozone versus hypochlorite. Water Research. 2018;140:243–250. doi: 10.1016/j.watres.2018.04.050. [DOI] [PubMed] [Google Scholar]
- Wang H, Shi W, Ma D, Shang Y, Wang Y, Gao B. Formation of DBPs during chlorination of antibiotics and control with permanganate/bisulfite pretreatment. Chemical Engineering Journal. 2020;392:123701. doi: 10.1016/j.cej.2019.123701. [DOI] [Google Scholar]
- Wang S, Chew J W, Liu Y. An environmentally sustainable approach for online chemical cleaning of MBR with activated peroxymonosulfate. Journal of Membrane Science. 2020;600:117872. doi: 10.1016/j.memsci.2020.117872. [DOI] [Google Scholar]
- Wang Z, Ding J, Xie P, Chen Y, Wan Y, Wang S. Formation of halogenated by-products during chemical cleaning of humic acid-fouled UF membrane by sodium hypochlorite solution. Chemical Engineering Journal. 2018;332:76–84. doi: 10.1016/j.cej.2017.09.053. [DOI] [Google Scholar]
- Wang Z, Ma J, Tang C Y, Kimura K, Wang Q, Han X. Membrane cleaning in membrane bioreactors: A review. Journal of Membrane Science. 2014;468:276–307. doi: 10.1016/j.memsci.2014.05.060. [DOI] [Google Scholar]
- Wu Q, Yan Y, Lu Y, Du Y, Liang Z, Hu H. Identification of important precursors and theoretical toxicity evaluation of byproducts driving cytotoxicity and genotoxicity in chlorination. Frontiers of Environmental Science & Engineering. 2020;14(2):25. doi: 10.1007/s11783-019-1204-6. [DOI] [Google Scholar]
- Xiao K, Xu Y, Liang S, Lei T, Sun J, Wen X, Zhang H, Chen C, Huang X. Engineering application of membrane bioreactor for wastewater treatment in China: Current state and future prospect. Frontiers of Environmental Science & Engineering. 2014;8(6):805–819. doi: 10.1007/s11783-014-0756-8. [DOI] [Google Scholar]
- Xie P, De Lannoy C F, Ma J, Wiesner M R. Chlorination of polyvinyl pyrrolidone-polysulfone membranes: Organic compound release, byproduct formation, and changes in membrane properties. Journal of Membrane Science. 2015;489:28–35. doi: 10.1016/j.memsci.2015.03.058. [DOI] [Google Scholar]
- Xue Z, Sendamangalam V R, Gruden C L, Seo Y. Multiple roles of extracellular polymeric substances on resistance of biofilm and detached clusters. Environmental Science & Technology. 2012;46(24):13212–13219. doi: 10.1021/es3031165. [DOI] [PubMed] [Google Scholar]
- Yang X, Shang C, Westerhoff P. Factors affecting formation of haloacetonitriles, haloketones, chloropicrin and cyanogen halides during chloramination. Water Research. 2007;41(6):1193–1200. doi: 10.1016/j.watres.2006.12.004. [DOI] [PubMed] [Google Scholar]
- Yu Y, Reckhow D A. Kinetic analysis of haloacetonitrile stability in drinking waters. Environmental Science & Technology. 2015;49(18):11028–11036. doi: 10.1021/acs.est.5b02772. [DOI] [PubMed] [Google Scholar]
- Yuan B, Wang X, Tang C, Li X, Yu G. In situ observation of the growth of biofouling layer in osmotic membrane bioreactors by multiple fluorescence labeling and confocal laser scanning microscopy. Water Research. 2015;75:188–200. doi: 10.1016/j.watres.2015.02.048. [DOI] [PubMed] [Google Scholar]
- Zhang X, Liu Y. Potential toxicity and implication of halogenated byproducts generated in MBR online — cleaning with hypochlorite. Journal of Chemical Technology and Biotechnology (Oxford, Oxfordshire) 2020;95(1):20–26. doi: 10.1002/jctb.6199. [DOI] [Google Scholar]
- Zhu X, Zhang X. Modeling the formation of TOCl, TOBr and TOI during chlor(am)ination of drinking water. Water Research. 2016;96:166–176. doi: 10.1016/j.watres.2016.03.051. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
