Applied Microbiology and Biotechnology

, Volume 103, Issue 21–22, pp 9155–9168 | Cite as

Deterministic and stochastic processes driving the shift in the prokaryotic community composition in wastewater treatment plants of a coastal Chinese city

  • Liyuan Hou
  • Sikandar I. Mulla
  • Juan Pablo Niño-Garcia
  • Daliang Ning
  • Azhar Rashid
  • Anyi HuEmail author
  • Chang-Ping Yu
Environmental biotechnology


Wastewater treatment plants (WWTPs) rely mainly on the microbial assemblages to contribute significantly for the removal of organic pollutants and nutrients. However, limited information is available on the ecological driving forces underlying the turnover of prokaryotic communities across wastewater treatment processes (i.e., from influents (IFs) and effluents (EFs)) within WWTPs. Here, we used a combination of the 16S rRNA gene amplicon sequencing and a quantitative ecological null model analysis to explore the ecological processes governing the turnover of the prokaryotic communities and the dominant taxonomic taxa across wastewater treatment processes of five full-scale WWTPs in China. Our results indicated that a significant variation in the composition of prokaryotic communities and the dominant taxa between IFs and EFs. The analysis of the environmental sources of indicator OTUs showed that a relatively lower abundance of the sludge/sewage and human guts associated OTUs in EFs than in IFs. Ecological null models revealed that among the ecological processes, deterministic processes were dominant in controlling the turnover of the overall communities from IFs to EFs, whereas the relative importance of deterministic processes varied among the dominant taxa (i.e., Bacteroidetes > Proteobacteria > Gammaproteobacteria > Firmicutes > Betaproteobacteria). However, the assembly of IF and EF communities was influenced mainly by the deterministic and stochastic processes, respectively. In addition, our results indicated that EF communities have a higher phylogenetic diversity than those of the IF communities, but the abundance of prokaryotic 16S rRNA genes was lower in EFs than in IFs. Overall, our study provides a novel insight of the assembly mechanisms underlying the turnover of prokaryotic communities during wastewater treatment processes.


Prokaryotic community Turnover Ecological processes Wastewater treatment plant 16S rRNA gene amplicon sequencing 



We thank Mr. Hongjie Wang for assistance during field sampling and Dr. Konstantinos T. Konstantinidis for providing the custom SILVA 119 database.


This work was supported by the National Natural Science Foundation of China (31870475 and U1805244) and the Foreign Cooperation Project of the Fujian Province, China (2019I0030). Dr. Juan Pablo Niño-Garcia was supported by the Talented Young Scientist Program (TYSP) of Ministry of Science and Technology of China, and Dr. Azhar Rashid was supported by PIFI CAS (2017VEB0008).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2019_10177_MOESM1_ESM.pdf (185 kb)
ESM 1 (PDF 743 kb)


  1. Aanderud ZT, Vert JC, Lennon JT, Magnusson TW, Breakwell DP, Harker AR (2016) Bacterial dormancy is more prevalent in freshwater than hypersaline lakes. Front Microbiol 7:853. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahmed W, Staley C, Sidhu J, Sadowsky M, Toze S (2017) Amplicon-based profiling of bacteria in raw and secondary treated wastewater from treatment plants across Australia. Appl Microbiol Biotechnol 101(3):1253–1266. CrossRefPubMedGoogle Scholar
  3. An XL, Su JQ, Li B, Ouyang WY, Zhao Y, Chen QL, Cui L, Chen H, Gillings MR, Zhang T, Zhu YG (2018) Tracking antibiotic resistome during wastewater treatment using high throughput quantitative PCR. Environ Int 117:146–153. CrossRefPubMedGoogle Scholar
  4. Ayarza JM, Erijman L (2011) Balance of neutral and deterministic components in the dynamics of activated sludge floc assembly. Microb Ecol 61(3):486–495. CrossRefPubMedGoogle Scholar
  5. Bissett A, Richardson A, Baker G, Wakelin S, Thrall P (2010) Life history determines biogeographical patterns of soil bacterial communities over multiple spatial scales. Mol Ecol 19(19):4315–4327. CrossRefPubMedGoogle Scholar
  6. Cai L, Ju F, Zhang T (2014) Tracking human sewage microbiome in a municipal wastewater treatment plant. Appl Microbiol Biotechnol 98(7):3317–3326. CrossRefPubMedGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Catano CP, Dickson TL, Myers JA (2017) Dispersal and neutral sampling mediate contingent effects of disturbance on plant beta-diversity: a meta-analysis. Ecol Lett 20(3):347–356. CrossRefPubMedGoogle Scholar
  9. Cui Q, Huang Y, Wang H, Fang T (2019) Diversity and abundance of bacterial pathogens in urban rivers impacted by domestic sewage. Environ Pollut 249:24–35. CrossRefPubMedGoogle Scholar
  10. Curtis TP, Sloan WT (2006) Towards the design of diversity: stochastic models for community assembly in wastewater treatment plants. Water Sci Technol 54(1):227–236. CrossRefPubMedGoogle Scholar
  11. Drury B, Rosi-Marshall E, Kelly JJ (2013) Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Ecotoxicol Environ Safe 79(6):1897–1905. CrossRefGoogle Scholar
  12. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. CrossRefGoogle Scholar
  13. Evans S, Martiny JBH, Allison SD (2017) Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J 11(1):176–185. CrossRefPubMedGoogle Scholar
  14. Foladori P, Bruni L, Tamburini S, Ziglio G (2010) Direct quantification of bacterial biomass in influent, effluent and activated sludge of wastewater treatment plants by using flow cytometry. Water Res 44(13):3807–3818. CrossRefPubMedGoogle Scholar
  15. Grady CL Jr, Daigger GT, Love NG, Filipe CD (2011) Biological wastewater treatment. CRC pressGoogle Scholar
  16. Graham EB, Crump AR, Resch CT, Fansler S, Arntzen E, Kennedy DW, Fredrickson JK, Stegen JC (2016) Coupling spatiotemporal community assembly processes to changes in microbial metabolism. Front Microbiol 7:1949. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gu ZG, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32(18):2847–2849. CrossRefGoogle Scholar
  18. Günther S, Faust K, Schumann J, Harms H, Raes J, Müller S (2016) Species-sorting and mass-transfer paradigms control managed natural metacommunities. Environ Microbiol 18(12):4862–4877. CrossRefPubMedGoogle Scholar
  19. Hashimoto K, Matsuda M, Inoue D, Ike M (2014) Bacterial community dynamics in a full-scale municipal wastewater treatment plant employing conventional activated sludge process. J Biosci Bioeng 118(1):64–71. CrossRefPubMedGoogle Scholar
  20. Hildebrand F, Tadeo R, Voigt AY, Bork P, Raes J (2014) LotuS: an efficient and user-friendly OTU processing pipeline. Microbiome 2(1):30. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hou L, Hu A, Chen S, Zhang K, Orlić S, Rashid A, Yu C-P (2019) Decipher the assembly processes of the key ecological assemblages of microbial communities in thirteen full-scale wastewater treatment plants. Microbes Environ. CrossRefGoogle Scholar
  22. Hu A, Yang X, Chen N, Hou L, Ma Y, Yu C-P (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756. CrossRefPubMedGoogle Scholar
  23. Huang KL, Mao YP, Zhao FZ, Zhang XX, Ju F, Ye L, Wang YL, Li B, Ren HQ, Zhang T (2018) Free-living bacteria and potential bacterial pathogens in sewage treatment plants. Appl Microbiol Biotechnol 102(5):2455–2464. CrossRefPubMedGoogle Scholar
  24. Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH, Chinwalla AT, Creasy HH, Earl AM, FitzGerald MG, Fulton RS, Giglio MG, Hallsworth-Pepin K, Lobos EA, Madupu R, Magrini V, Martin JC, Mitreva M, Muzny DM, Sodergren EJ, Versalovic J, Wollam AM, Worley KC, Wortman JR, Young SK, Zeng QD, Aagaard KM, Abolude OO, Allen-Vercoe E, Alm EJ, Alvarado L, Andersen GL, Anderson S, Appelbaum E, Arachchi HM, Armitage G, Arze CA, Ayvaz T, Baker CC, Begg L, Belachew T, Bhonagiri V, Bihan M, Blaser MJ, Bloom T, Bonazzi V, Brooks JP, Buck GA, Buhay CJ, Busam DA, Campbell JL, Canon SR, Cantarel BL, Chain PSG, Chen IMA, Chen L, Chhibba S, Chu K, Ciulla DM, Clemente JC, Clifton SW, Conlan S, Crabtree J, Cutting MA, Davidovics NJ, Davis CC, DeSantis TZ, Deal C, Delehaunty KD, Dewhirst FE, Deych E, Ding Y, Dooling DJ, Dugan SP, Dunne WM, Durkin AS, Edgar RC, Erlich RL, Farmer CN, Farrell RM, Faust K, Feldgarden M, Felix VM, Fisher S, Fodor AA, Forney LJ, Foster L, Di Francesco V, Friedman J, Friedrich DC, Fronick CC, Fulton LL, Gao HY, Garcia N, Giannoukos G, Giblin C, Giovanni MY, Goldberg JM, Goll J, Gonzalez A, Griggs A, Gujja S, Haake SK, Haas BJ, Hamilton HA, Harris EL, Hepburn TA, Herter B, Hoffmann DE, Holder ME, Howarth C, Huang KH, Huse SM, Izard J, Jansson JK, Jiang HY, Jordan C, Joshi V, Katancik JA, Keitel WA, Kelley ST, Kells C, King NB, Knights D, Kong HDH, Koren O, Koren S, Kota KC, Kovar CL, Kyrpides NC, La Rosa PS, Lee SL, Lemon KP, Lennon N, Lewis CM, Lewis L, Ley RE, Li K, Liolios K, Liu B, Liu Y, Lo CC, Lozupone CA, Lunsford RD, Madden T, Mahurkar AA, Mannon PJ, Mardis ER, Markowitz VM, Mavromatis K, McCorrison JM, McDonald D, McEwen J, McGuire AL, McInnes P, Mehta T, Mihindukulasuriya KA, Miller JR, Minx PJ, Newsham I, Nusbaum C, O'Laughlin M, Orvis J, Pagani I, Palaniappan K, Patel SM, Pearson M, Peterson J, Podar M, Pohl C, Pollard KS, Pop M, Priest ME, Proctor LM, Qin X, Raes J, Ravel J, Reid JG, Rho M, Rhodes R, Riehle KP, Rivera MC, Rodriguez-Mueller B, Rogers YH, Ross MC, Russ C, Sanka RK, Sankar P, Sathirapongsasuti JF, Schloss JA, Schloss PD, Schmidt TM, Scholz M, Schriml L, Schubert AM, Segata N, Segre JA, Shannon WD, Sharp RR, Sharpton TJ, Shenoy N, Sheth NU, Simone GA, Singh I, Smillie CS, Sobel JD, Sommer DD, Spicer P, Sutton GG, Sykes SM, Tabbaa DG, Thiagarajan M, Tomlinson CM, Torralba M, Treangen TJ, Truty RM, Vishnivetskaya TA, Walker J, Wang L, Wang ZY, Ward DV, Warren W, Watson MA, Wellington C, Wetterstrand KA, White JR, Wilczek-Boney K, Wu YQ, Wylie KM, Wylie T, Yandava C, Ye L, Ye YZ, Yooseph S, Youmans BP, Zhang L, Zhou YJ, Zhu YM, Zoloth L, Zucker JD, Birren BW, Gibbs RA, Highlander SK, Methe BA, Nelson KE, Petrosino JF, Weinstock GM, Wilson RK, White O, Consortiu HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214. CrossRefGoogle Scholar
  25. Ibekwe AM, Grieve CM, Lyon SR (2003) Characterization of microbial communities and composition in constructed dairy wetland wastewater effluent. Appl Environ Microbiol 69(9):5060–5069. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Isazadeh S, Jauffur S, Frigon D (2016) Bacterial community assembly in activated sludge: mapping beta diversity across environmental variables. Microbiologyopen 5(6):1050–1060. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci U S A 107(13):5881–5886. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ju F, Zhang T (2015) Bacterial assembly and temporal dynamics in activated sludge of a full-scale municipal wastewater treatment plant. ISME J 9(3):683–695. CrossRefPubMedGoogle Scholar
  29. Ju F, Xia Y, Guo F, Wang ZP, Zhang T (2014) Taxonomic relatedness shapes bacterial assembly in activated sludge of globally distributed wastewater treatment plants. Environ Microbiol 16(8):2421–2432. CrossRefPubMedGoogle Scholar
  30. Karkman A, Johnson TA, Lyra C, Stedtfeld RD, Tamminen M, Tiedje JM, Virta M (2016) High-throughput quantification of antibiotic resistance genes from an urban wastewater treatment plant. FEMS Microbiol Ecol 92(3). CrossRefGoogle Scholar
  31. Karkman A, Do T, Walsh F, Virta M (2018) Antibiotic-resistance genes in waste water. Trends Microbiol 26(3):220–228. CrossRefPubMedGoogle Scholar
  32. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464. CrossRefPubMedGoogle Scholar
  33. Kirkegaard RH, McIlroy SJ, Kristensen JM, Nierychlo M, Karst SM, Dueholm MS, Albertsen M and Nielsen PH (2017). The impact of immigration on microbial community composition in full-scale anaerobic digesters. Sci Rep 7(1):9343.
  34. Lee SH, Kang HJ, Park HD (2015) Influence of influent wastewater communities on temporal variation of activated sludge communities. Water Res 73:132–144. CrossRefPubMedGoogle Scholar
  35. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7(7):601–613. CrossRefGoogle Scholar
  36. Li LG, Yin XL, Zhang T (2018) Tracking antibiotic resistance gene pollution from different sources using machine-learning classification. Microbiome 6Google Scholar
  37. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Matar GK, Bagchi S, Zhang K, Oerther DB, Saikaly PE (2017) Membrane biofilm communities in full-scale membrane bioreactors are not randomly assembled and consist of a core microbiome. Water Res 123:124–133. CrossRefPubMedGoogle Scholar
  39. McLellan SL, Huse SM, Mueller-Spitz SR, Andreishcheva EN, Sogin ML (2010) Diversity and population structure of sewage-derived microorganisms in wastewater treatment plant influent. Environ Microbiol 12(2):378–392. CrossRefPubMedGoogle Scholar
  40. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Meziti A, Tsementzi D, Ar. Kormas K, Karayanni H, Konstantinidis KT (2016) Anthropogenic effects on bacterial diversity and function along a river-to-estuary gradient in Northwest Greece revealed by metagenomics. Environ Microbiol. CrossRefGoogle Scholar
  42. Monard C, Gantner S, Bertilsson S, Hallin S, Stenlid J (2016) Habitat generalists and specialists in microbial communities across a terrestrial-freshwater gradient. Sci Rep-Uk 6:37719. CrossRefGoogle Scholar
  43. Narciso-da-Rocha C, Rocha J, Vaz-Moreira I, Lira F, Tamames J, Henriques I, Martinez JL, Manaia CM (2018) Bacterial lineages putatively associated with the dissemination of antibiotic resistance genes in a full-scale urban wastewater treatment plant. Environ Int 118:179–188. CrossRefPubMedGoogle Scholar
  44. Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77(3):342–356. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Ofiteru ID, Lunn M, Curtis TP, Wells GF, Criddle CS, Francis CA, Sloan WT (2010) Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci U S A 107(35):15345–15350. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Oksanen J, Kindt R, Legendre P, O'Hara B, Simpson G, Solymos P, Stevens M, Wagner H (2009) vegan: community ecology package. R package version 115-2Google Scholar
  47. Qin Y, Hou J, Deng M, Liu QS, Wu CW, Ji YJ, He XG (2016) Bacterial abundance and diversity in pond water supplied with different feeds. Sci Rep 6.
  48. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12(1):38. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Roberts D (2007) labdsv: Ordination and multivariate analysis for ecology. R package version 1(1)Google Scholar
  50. Shanks OC, Newton RJ, Kelty CA, Huse SM, Sogin ML, McLellan SL (2013) Comparison of the microbial community structures of untreated wastewaters from different geographic locales. Appl Environ Microbiol 79(9):2906–2913. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shchegolkova NM, Krasnov GS, Belova AA, Dmitriev AA, Kharitonov SL, Klimina KM, Melnikova NV, Kudryavtseva AV (2016) Microbial community structure of activated sludge in treatment plants with different wastewater compositions. Front Microbiol 7:90. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3(8):992–1000. CrossRefPubMedGoogle Scholar
  53. Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7(11):2069–2079. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Stegen JC, Lin X, Fredrickson JK, Konopka AE (2015) Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol 6:370. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Stegen JC, Fredrickson JK, Wilkins MJ, Konopka AE, Nelson WC, Arntzen EV, Chrisler WB, Chu RK, Danczak RE, Fansler SJ (2016) Groundwater–surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover. Nat Commun 7:11237. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sun Q, Wang Y, Li Y, Ashfaq M, Dai L, Xie X, Yu CP (2017) Fate and mass balance of bisphenol analogues in wastewater treatment plants in Xiamen City, China. Environ Pollut 225:542–549. CrossRefPubMedGoogle Scholar
  57. Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl Environ Microbiol 66(11):4605–4614. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Valentin-Vargas A, Toro-Labrador G, Massol-Deya AA (2012) Bacterial community dynamics in full-scale activated sludge bioreactors: operational and ecological factors driving community assembly and performance. PLoS One 7(8):e42524. CrossRefPubMedPubMedCentralGoogle Scholar
  59. van der Gast CJ, Jefferson B, Reid E, Robinson T, Bailey MJ, Judd SJ, Thompson IP (2006) Bacterial diversity is determined by volume in membrane bioreactors. Environ Microbiol 8(6):1048–1055. CrossRefPubMedGoogle Scholar
  60. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85(2):183–206. CrossRefPubMedGoogle Scholar
  61. Vignola M, Werner D, Wade MJ, Meynet P, Davenport RJ (2018) Medium shapes the microbial community of water filters with implications for effluent quality. Water Res 129:499–508. CrossRefPubMedGoogle Scholar
  62. Wakelin SA, Colloff MJ, Kookana RS (2008) Effect of wastewater treatment plant effluent on microbial function and community structure in the sediment of a freshwater stream with variable seasonal flow. Appl Environ Microbiol 74(9):2659–2668. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang XH, Hu M, Xia Y, Wen XH, Ding K (2012a) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl Environ Microbiol 78(19):7042–7047. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wang XH, Wen XH, Xia Y, Hu M, Zhao F, Ding K (2012b) Ammonia oxidizing bacteria community dynamics in a pilot-scale wastewater treatment plant. PLoS One 7(4). CrossRefGoogle Scholar
  65. Wang JJ, Shen J, Wu YC, Tu C, Soininen J, Stegen JC, He JZ, Liu XQ, Zhang L, Zhang EL (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7(7):1310–1321. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wang Y, Li Y, Hu A, Rashid A, Ashfaq M, Wang Y, Wang H, Luo H, Yu C-P, Sun Q (2018) Monitoring, mass balance and fate of pharmaceuticals and personal care products in seven wastewater treatment plants in Xiamen City, China. J Hazard Mater 354:81–90. CrossRefPubMedGoogle Scholar
  67. Wells GF, Wu CH, Piceno YM, Eggleston B, Brodie EL, DeSantis TZ, Andersen GL, Hazen TC, Francis CA, Criddle CS (2014) Microbial biogeography across a full-scale wastewater treatment plant transect: evidence for immigration between coupled processes. Appl Microbiol Biotechnol 98(10):4723–4736. CrossRefPubMedGoogle Scholar
  68. Wickham H (2016) ggplot2: elegant graphics for data analysis. SpringerGoogle Scholar
  69. Wu W, Lu HP, Sastri A, Yeh Y, Gong G, Chou W, Hsieh C (2017) Contrasting the relative importance of species sorting and dispersal limitation in shaping marine bacterial versus protist communities. ISME J 12:485–494. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yang Y, Yu K, Xia Y, Lau FTK, Tang DTW, Fung WC, Fang HHP, Zhang T (2014) Metagenomic analysis of sludge from full-scale anaerobic digesters operated in municipal wastewater treatment plants. Appl Microbiol Biotechnol 98(12):5709–5718. CrossRefPubMedGoogle Scholar
  71. Ye L, Zhang T (2013) Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing. Appl Microbiol Biotechnol 97(6):2681–2690. CrossRefPubMedGoogle Scholar
  72. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glockner FO (2014) The SILVA and All-species Living Tree Project (LTP) taxonomic frameworks. Nucleic Acids Res 42(D1):D643–D648. CrossRefPubMedGoogle Scholar
  73. Zhang K, Farahbakhsh K (2007) Removal of native coliphages and coliform bacteria from municipal wastewater by various wastewater treatment processes: Implications to water reuse. Water Res 41(12):2816–2824. CrossRefPubMedGoogle Scholar
  74. Zhang T, Shao M-F, Ye L (2012) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6(6):1137–1147. CrossRefPubMedGoogle Scholar
  75. Zhang Y, Li AL, Dai TJ, Li FF, Xie H, Chen LJ, Wen DH (2018) Cell-free DNA: A Neglected Source for antibiotic resistance genes spreading from WWTPs. Environ Sci Technol 52(1):248–257. CrossRefPubMedGoogle Scholar
  76. Zhou JZ, Ning DL (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev 81(4):e00002–e00017. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zhou JZ, Liu WZ, Deng Y, Jiang YH, Xue K, He ZL, Van Nostrand JD, Wu LY, Yang YF, Wang AJ (2013) Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. Mbio 4(2):e00584–e00512. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

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Authors and Affiliations

  1. 1.CAS Key Laboratory of Urban Pollutant ConversionInstitute of Urban Environment, Chinese Academy of SciencesXiamenChina
  2. 2.Department of Civil and Environmental EngineeringUniversity of MissouriColumbiaUSA
  3. 3.Department of Biochemistry, School of Applied SciencesREVA UniversityBangaloreIndia
  4. 4.Escuela de MicrobiologíaUniversidad de AntioquiaMedellínColombia
  5. 5.Institute for Environmental Genomics, Department of Microbiology and Plant Biology, and School of Civil Engineering and Environmental SciencesUniversity of OklahomaNormanUSA
  6. 6.Nuclear Institute for Food and AgriculturePeshawarPakistan
  7. 7.Graduate Institute of Environmental EngineeringNational Taiwan UniversityTaipeiTaiwan

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