Bacterial perspectives on the dissemination of antibiotic resistance genes in domestic wastewater bio-treatment systems: beneficiary to victim

Mini-Review

Abstract

Domestic wastes, ranging from sewage and sludge to municipal solid waste, are usually treated in bioprocessing systems. These systems are regarded as main conduits for the elevated levels of antibiotic resistance genes (ARGs) observed in the environment. This paper mainly reviews recent studies on the occurrence and dynamics of ARGs in wastewater bio-treatment systems and discusses the ins and outs of ARG dissemination from the perspective of the microbial community. Our analysis shows that concentration of antibiotics through adsorption to microbial aggregates triggers the bacteria to acquire ARGs, which can be facilitated by the presence of mobile genetic elements. Notably, the acquisition and flow of ARGs during the rapid dissemination process is directed towards and for the best interests of the microbial community as a whole, and is influenced by surrounding nutrient levels, toxicant types, and sensitivities of the species in the prevailing antibiotic-stressed conditions. Furthermore, our review argues that predation of ARG-carrying bacteria by bacteriophages does periodically enhance the accessibility of ARGs to bacteria, which indirectly facilitates the recruitment of ARGs into environmental microbial communities.

Keywords

Domestic wastes Antibiotic resistance genes Waste bio-treatment Antibiotic resistance dissemination 

Notes

Acknowledgments

This work was supported by the Natural Science Foundation of China (21577038,31370510) and East China Normal University: Outstanding doctoral dissertation cultivation plan of action (PY2015034). J.D. acknowledges an international exchange grant from the Royal Society (Grant IE131283) for work on the treatment of landfill leachate. D.W. acknowledges the support from Distinguished Young PhD student Fellowship granted by Shanghai Tongji Gao-Tingyao Environmental Science & Technology Development Foundation (STGEF2017).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

There is no ethical or legal conflict involved in this article.

Consent for publication

The manuscript has not been published elsewhere and all authors have seen the manuscript and approved to submit to your journal with mutual consent.

References

  1. Abegglen C, Joss A, McArdell CS, Fink G, Schlusener MP, Ternes TA, Siegrist H (2009) The fate of selected micropollutants in a single-house MBR. Water Res 43(7):2036–2046. 10.1016/j.watres.2009.02.005 CrossRefPubMedGoogle Scholar
  2. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8(4):251–259. 10.1038/nrmicro2312 CrossRefPubMedGoogle Scholar
  3. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14(4):176–182. 10.1016/j.tim.2006.02.006 CrossRefPubMedGoogle Scholar
  4. Baltrus DA (2013) Exploring the costs of horizontal gene transfer. Trends Ecol Evol 28(8):489–495 doi:10.1016/j.tree.2013.04.002
  5. Bjorkman J, Andersson DI (2000) The cost of antibiotic resistance from a bacterial perspective. Drug Resis Updat 3(4):237–245. 10.1054/drup.2000.0147 CrossRefGoogle Scholar
  6. Bound JP, Voulvoulis N (2005) Household disposal of pharmaceuticals as a pathway for aquatic contamination in the United Kingdom. Environ Health Perspect 113(12):1705–1711. 10.1289/ehp.8315 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brown-Jaque M, Calero-Caceres W, Muniesa M (2015) Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid 79:1–7. 10.1016/j.plasmid.2015.01.001 CrossRefPubMedGoogle Scholar
  8. Calero-Caceres W, Muniesa M (2016) Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater. Water Res 95:11–18. 10.1016/j.watres.2016.03.006 CrossRefPubMedGoogle Scholar
  9. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann M-L, Brüssow H (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6(4):417–424. 10.1016/s1369-5274(03)00086-9 CrossRefPubMedGoogle Scholar
  10. Chen B, Yang Y, Liang X, Yu K, Zhang T, Li X (2013) Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environ Sci Technol 47(22):12753–12760. 10.1021/es403818e CrossRefPubMedGoogle Scholar
  11. Chen B, Yuan K, Chen X, Yang Y, Zhang T, Wang Y, Luan T, Zou S, Li X (2016) Metagenomic analysis revealing antibiotic resistance genes (ARGs) and their genetic compartments in the Tibetan environment. Environ Sci Technol 50(13):6670–6679. 10.1021/acs.est.6b00619 CrossRefPubMedGoogle Scholar
  12. Christgen B, Yang Y, Ahammad SZ, Li B, Rodriquez DC, Zhang T, Graham DW (2015) Metagenomics shows that low-energy anaerobic-aerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environ Sci Technol 49(4):2577–2584. 10.1021/es505521w CrossRefPubMedGoogle Scholar
  13. Chua H, Hua FL (1996) Effects of a heavy metal (zinc) on organic adsorption capacity and organic removal in activated sludge. Appl Biochem Biotechnol 57-8:845-849 doi:Doi 10.1007/Bf02941764
  14. Colomer-Lluch M, Calero-Caceres W, Jebri S, Hmaied F, Muniesa M, Jofre J (2014) Antibiotic resistance genes in bacterial and bacteriophage fractions of Tunisian and Spanish wastewaters as markers to compare the antibiotic resistance patterns in each population. Environ Int 73:167–175. 10.1016/j.envint.2014.07.003 CrossRefPubMedGoogle Scholar
  15. Colomer-Lluch M, Imamovic L, Jofre J, Muniesa M (2011) Bacteriophages carrying antibiotic resistance genes in fecal waste from cattle, pigs, and poultry. Antimicrob Agents Ch 55(10):4908–4911. 10.1128/AAC.00535-11 CrossRefGoogle Scholar
  16. Cordero OX, Wildschutte H, Kirkup B, Proehl S, Ngo L, Hussain F, Le Roux F, Mincer T, Polz MF (2012) Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337(6099):1228–1231. 10.1126/science.1219385 CrossRefPubMedGoogle Scholar
  17. Crofts TS, Gasparrini AJ, Dantas G (2017) Next-generation approaches to understand and combat the antibiotic resistome. Nature Rev Microbiol 15(7):422–434. 10.1038/nrmicro.2017.28 CrossRefGoogle Scholar
  18. Czekalski N, Gascon Diez E, Burgmann H (2014) Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME J 8(7):1381–1390. 10.1038/ismej.2014.8 CrossRefPubMedPubMedCentralGoogle Scholar
  19. D'Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477(7365):457–461. 10.1038/nature10388 CrossRefPubMedGoogle Scholar
  20. Dantas G, Sommer MOA, Oluwasegun RD, Church GM (2008) Bacteria subsisting on antibiotics. Science 320(5872):100–103. 10.1126/science.1155157 CrossRefPubMedGoogle Scholar
  21. Di Cesare A, Eckert EM, D'Urso S, Bertoni R, Gillan DC, Wattiez R, Corno G (2016) Co-occurrence of integrase 1, antibiotic and heavy metal resistance genes in municipal wastewater treatment plants. Water Res 94:208–214. 10.1016/j.watres.2016.02.049 CrossRefPubMedGoogle Scholar
  22. Drillia P, Dokianakis SN, Fountoulakis MS, Kornaros M, Stamatelatou K, Lyberatos G (2005) On the occasional biodegradation of pharmaceuticals in the activated sludge process: the example of the antibiotic sulfamethoxazole. J Hazard Mater 122(3):259–265. 10.1016/j.jhazmat.2005.03.009 CrossRefPubMedGoogle Scholar
  23. Environment Agency (2013) Waste management 2013—England. UKGoogle Scholar
  24. Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature 509(7502):612–616. 10.1038/nature13377 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3(9):722–732. 10.1038/nrmicro1235 CrossRefPubMedGoogle Scholar
  26. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall AB, Wellington EM (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5(8):1253–1261. 10.1038/ismej.2011.15 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Graham DW, Knapp CW, Christensen BT, McCluskey S, Dolfing J (2016) Appearance of beta-lactam resistance genes in agricultural soils and clinical isolates over the 20(th) century. Sci Rep 6(1):21550. 10.1038/srep21550 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Guellil A, Thomas F, Block JC, Bersillon JL, Ginestet P (2001) Transfer of organic matter between wastewater and activated sludge flocs. Water Res 35(1):143-150 doi:Doi 10.1016/S0043-1354(00)00240-2
  29. Guo J, Li J, Chen H, Bond PL, Yuan Z (2017) Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements. Water Res 123:468–478. 10.1016/j.watres.2017.07.002 CrossRefPubMedGoogle Scholar
  30. Hardy K, Buckley S, Collins MJ, Estalrrich A, Brothwell D, Copeland L, Garcia-Tabernero A, Garcia-Vargas S, de la Rasilla M, Lalueza-Fox C, Huguet R, Bastir M, Santamaria D, Madella M, Wilson J, Cortes AF, Rosas A (2012) Neanderthal medics? Evidence for food, cooking, and medicinal plants entrapped in dental calculus. Naturwissenschaften 99(8):617–626. 10.1007/s00114-012-0942-0 CrossRefPubMedGoogle Scholar
  31. Hu HW, Wang JT, Li J, Shi XZ, Ma YB, Chen D, He JZ (2017) Long-term nickel contamination increases the occurrence of antibiotic resistance genes in agricultural soils. Environ Sci Technol 51(2):790–800. 10.1021/acs.est.6b03383 CrossRefGoogle Scholar
  32. Jiang L, Hu X, Xu T, Zhang H, Sheng D, Yin D (2013) Prevalence of antibiotic resistance genes and their relationship with antibiotics in the Huangpu River and the drinking water sources, Shanghai, China. Sci Total Environ 458-460:267–272. 10.1016/j.scitotenv.2013.04.038 CrossRefPubMedGoogle Scholar
  33. Kümmerer K (2008) Pharmaceuticals in the Environment: sources, fate, effects and risks, 3rd edn. Springer-Verlag Berlin, Heidelberg. 10.1007/978-3-540-74664-5 CrossRefGoogle Scholar
  34. Kümmerer K, Al-Ahmad A, Mersch-Sundermann V (2000) Biodegradability of some antibiotics, elimination of the genotoxicity and affection of wastewater bacteria in a simple test. Chemosphere 40(7):701–710. 10.1016/S0045-6535(99)00439-7 CrossRefPubMedGoogle Scholar
  35. Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8(1):1–13. 10.1016/j.ecolind.2007.06.002 CrossRefGoogle Scholar
  36. Knapp CW, Dolfing J, Ehlert PA, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44(2):580–587. 10.1021/es901221x CrossRefPubMedGoogle Scholar
  37. Koonin EV, Makarova KS, Aravind L (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55(1):709–742. 10.1146/annurev.micro.55.1.709 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lee KW, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA (2014) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8(4):894–907. 10.1038/ismej.2013.194 CrossRefPubMedGoogle Scholar
  39. Li LG, Xia Y, Zhang T (2017) Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J 11(3):651–662. 10.1038/ismej.2016.155 CrossRefPubMedGoogle Scholar
  40. Li W, Shi Y, Gao L, Liu J, Cai Y (2013) Occurrence, distribution and potential affecting factors of antibiotics in sewage sludge of wastewater treatment plants in China. Sci Total Environ 445-446:306–313. 10.1016/j.scitotenv.2012.12.050 CrossRefPubMedGoogle Scholar
  41. Lindberg RH, Olofsson U, Rendahl P, Johansson MI, Tysklind M, Andersson BAV (2006) Behavior of fluoroquinolones and trimethoprim during mechanical, chemical, and active sludge treatment of sewage water and digestion of sludge. Environ Sci Technol 40(3):1042–1048. 10.1021/es0516211 CrossRefPubMedGoogle Scholar
  42. Luczkiewicz A, Jankowska K, Fudala-Ksiazek S, Olanczuk-Neyman K (2010) Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Res 44(17):5089–5097. 10.1016/j.watres.2010.08.007 CrossRefPubMedGoogle Scholar
  43. Mao D, Luo Y, Mathieu J, Wang Q, Feng L, Mu Q, Feng C, Alvarez PJ (2014) Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environ Sci Technol 48(1):71–78. 10.1021/es404280v CrossRefPubMedGoogle Scholar
  44. Marx C, Gunther N, Schubert S, Oertel R, Ahnert M, Krebs P, Kuehn V (2015) Mass flow of antibiotics in a wastewater treatment plant focusing on removal variations due to operational parameters. Sci Total Environ 538:779–788. 10.1016/j.scitotenv.2015.08.112 CrossRefPubMedGoogle Scholar
  45. Miao XS, Bishay F, Chen M, Metcalfe CD (2004) Occurrence of antimicrobials in the final effluents of wastewater treatment plants in Canada. Environ Sci Technol 38(13):3533–3541. 10.1021/es030653q CrossRefPubMedGoogle Scholar
  46. Miao Y, Liao R, Zhang XX, Wang Y, Wang Z, Shi P, Liu B, Li A (2015) Metagenomic insights into Cr(VI) effect on microbial communities and functional genes of an expanded granular sludge bed reactor treating high-nitrate wastewater. Water Res 76:43–52. 10.1016/j.watres.2015.02.042 CrossRefPubMedGoogle Scholar
  47. Michael I, Rizzo L, McArdell CS, Manaia CM, Merlin C, Schwartz T, Dagot C, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res 47(3):957–995. 10.1016/j.watres.2012.11.027 CrossRefPubMedGoogle Scholar
  48. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334(6058):982–986. 10.1126/science.1211037 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Park C, Zhang J (2012) High expression hampers horizontal gene transfer. Genome biology and evolution 4(4):523–532. 10.1093/gbe/evs030 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pehrsson EC, Tsukayama P, Patel S, Mejia-Bautista M, Sosa-Soto G, Navarrete KM, Calderon M, Cabrera L, Hoyos-Arango W, Bertoli MT, Berg DE, Gilman RH, Dantas G (2016) Interconnected microbiomes and resistomes in low-income human habitats. Nature 533(7602):212–216. 10.1038/nature17672 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ratcliff WC, Denison RF (2011) Microbiology. Alternative actions for antibiotics. Science 332(6029):547–548. 10.1126/science.1205970 CrossRefPubMedGoogle Scholar
  52. Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasic L, Thingstad TF, Rohwer F, Mira A (2009) Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7(11):828–836. 10.1038/nrmicro2235 CrossRefPubMedGoogle Scholar
  53. Rysz M, Mansfield WR, Fortner JD, Alvarez PJ (2013) Tetracycline resistance gene maintenance under varying bacterial growth rate, substrate and oxygen availability, and tetracycline concentration. Environ Sci Technol 47(13):6995–7001. 10.1021/es3035329 CrossRefPubMedGoogle Scholar
  54. Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Frontiers Microbiol 3:399. 10.3389/fmicb.2012.00399 CrossRefGoogle Scholar
  55. Shapiro OH, Kushmaro A (2011) Bacteriophage ecology in environmental biotechnology processes. Curr Opin Biotech 22(3):449–455. 10.1016/j.copbio.2011.01.012 CrossRefPubMedGoogle Scholar
  56. Shapiro OH, Kushmaro A, Brenner A (2010) Bacteriophage predation regulates microbial abundance and diversity in a full-scale bioreactor treating industrial wastewater. ISME J 4(3):327–336. 10.1038/ismej.2009.118 CrossRefPubMedGoogle Scholar
  57. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8(9):1510–1514. 10.1111/j.1462-2920.2006.01091.x CrossRefPubMedGoogle Scholar
  58. Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, HJ X, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49(12):7356–7363. 10.1021/acs.est.5b01012 CrossRefGoogle Scholar
  59. Sun M, Ye M, Schwab AP, Li X, Wan J, Wei Z, Wu J, Friman VP, Liu K, Tian D, Liu M, Li H, Hu F, Jiang X (2016) Human migration activities drive the fluctuation of ARGs: case study of landfills in Nanjing, eastern China. J Hazard Mater 315:93–101. 10.1016/j.jhazmat.2016.04.077 CrossRefPubMedGoogle Scholar
  60. Szczepanowski R, Linke B, Krahn I, Gartemann KH, Gutzkow T, Eichler W, Puhler A, Schluter A (2009) Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 155(Pt 7):2306–2319. 10.1099/mic.0.028233-0 CrossRefPubMedGoogle Scholar
  61. Thingstad TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45(6):1320–1328. 10.4319/lo.2000.45.6.1320 CrossRefGoogle Scholar
  62. Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014) Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14(8):742–750. 10.1016/s1473-3099(14)70780-7 CrossRefPubMedGoogle Scholar
  63. Wellington EMH, Boxall ABA, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013) The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis 13(2):155–165. 10.1016/s1473-3099(12)70317-1 CrossRefPubMedGoogle Scholar
  64. Withey S, Cartmell E, Avery LM, Stephenson T (2005) Bacteriophages—potential for application in wastewater treatment processes. Sci Total Environ 339(1–3):1–18. 10.1016/j.scitotenv.2004.09.021 CrossRefPubMedGoogle Scholar
  65. Wu D, Chen G, Zhang X, Yang K, Xie B (2017) Change in microbial community in landfill refuse contaminated with antibiotics facilitates denitrification more than the increase in ARG over long-term. Sci Rep 7:41230. 10.1038/srep41230 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wu D, Huang Z, Yang K, Graham D, Xie B (2015) Relationships between antibiotics and antibiotic resistance gene levels in municipal solid waste leachates in Shanghai, China. Environ Sci Technol 49(7):4122–4128. 10.1021/es506081z CrossRefPubMedGoogle Scholar
  67. Wu Q, Liu WT (2009) Determination of virus abundance, diversity and distribution in a municipal wastewater treatment plant. Water Res 43(4):1101–1109. 10.1016/j.watres.2008.11.039 CrossRefPubMedGoogle Scholar
  68. Yang Y, Li B, Zou S, Fang HH, Zhang T (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res 62:97–106. 10.1016/j.watres.2014.05.019 CrossRefPubMedGoogle Scholar
  69. Yu P, Mathieu J, GW L, Gabiatti N, Alvarez PJ (2017) Control of antibiotic-resistant bacteria in activated sludge using polyvalent phages in conjunction with a production host. Environ Sci Technol Lett 4(4):137–142. 10.1021/acs.estlett.7b00045 CrossRefGoogle Scholar
  70. Yu Z, He P, Shao L, Zhang H, Lu F (2016) Co-occurrence of mobile genetic elements and antibiotic resistance genes in municipal solid waste landfill leachates: a preliminary insight into the role of landfill age. Water Res 106:583–592. 10.1016/j.watres.2016.10.042 CrossRefPubMedGoogle Scholar
  71. Zhang Y, Geissen SU, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73(8):1151–1161. 10.1016/j.chemosphere.2008.07.086 CrossRefPubMedGoogle Scholar
  72. Zhou LJ, Ying GG, Liu S, Zhao JL, Yang B, Chen ZF, Lai HJ (2013) Occurrence and fate of eleven classes of antibiotics in two typical wastewater treatment plants in South China. Sci Total Environ 452-453:365–376. 10.1016/j.scitotenv.2013.03.010 CrossRefPubMedGoogle Scholar
  73. Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Chen YS, Zhang T, Gillings MR, JQ S (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2:16270. 10.1038/nmicrobiol.2016.270 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, School of Ecological and Environmental ScienceEast China Normal UniversityShanghaiChina
  2. 2.Shanghai Institute of Pollution Control and Ecological SecurityTongji UniversityShanghaiChina
  3. 3.Joint Research Institute for New Energy and the EnvironmentEast China Normal University and Colorado State UniversityShanghaiChina
  4. 4.School of Civil Engineering and GeosciencesNewcastle UniversityNewcastle upon TyneUK

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