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Transformation of anaerobic granules into aerobic granules and the succession of bacterial community

  • Environmental biotechnology
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Abstract

In this study, we demonstrated that anaerobic granular sludge could be successfully transformed into aerobic granular sludge in a continuous up-flow reactor in 45 days. An aerobic microbial community successfully developed in the granules and high organic matter and nitrogen removal performance was achieved. Under an ammonia nitrogen loading rate of 0.8 kg N/(m3 day), ammonia nitrogen and the total nitrogen removal efficiency of the reactor reached up to 100 and 93%, respectively. An obvious bacterial community shift in granular sludge was observed during the transformation process. By comparing with the bacterial community in aerobic granules cultivated from floccular activated sludge, some bacteria (affiliated with Comamonadaceae, Xanthomonadaceae, Rhodocyclaceae, Moraxellaceae, and Nitrosomonadaceae) playing significant roles in maintaining the structures and functions of aerobic granules were identified. After the transformation, the granules could be clearly separated into the inner core and outer shell. 16S rRNA gene sequencing results indicated many bacterial species present in both the inner core and outer shell; however, their abundance differed significantly. Overall, this study confirms the feasibility of transforming anaerobic granules into aerobic granules and provides novel approaches and insights to understand the microbial ecology in granular sludge.

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References

  • Adav SS, Chen MY, Lee DJ, Ren NQ (2007) Degradation of phenol by Acinetobacter strain isolated from aerobic granules. Chemosphere 67(8):1566–1572

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lee DJ (2008) Single-culture aerobic granules with Acinetobacter calcoaceticus. Appl Microbiol Biotechnol 78(3):551–557

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lee D-J, Lai J-Y (2010) Microbial community of acetate utilizing denitrifiers in aerobic granules. Appl Microbiol Biotechnol 85(3):753–762

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lee DJ, Show KY, Tay JH (2008) Aerobic granular sludge: recent advances. Biotechnol Adv 26(5):411–423

    Article  CAS  PubMed  Google Scholar 

  • Apah W (2005) AWWA. Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Arrojo B, Mosquera-Corral A, Garrido JM, Méndez R (2004) Aerobic granulation with industrial wastewater in sequencing batch reactors. Water Res 38(14):3389–3399

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7(5):335–336

    Article  CAS  Google Scholar 

  • Carr EL, Kämpfer P, Patel BK, Gürtler V, Seviour RJ (2003) Seven novel species of Acinetobacter isolated from activated sludge. Int J Syst Evol Microbiol 53(4):953–963

    Article  CAS  PubMed  Google Scholar 

  • Corsino S, Campo R, Di Bella G, Torregrossa M, Viviani G (2016) Study of aerobic granular sludge stability in a continuous-flow membrane bioreactor. Bioresour Technol 200:1055–1059

    Article  CAS  PubMed  Google Scholar 

  • De Kreuk M, Heijnen J, Van Loosdrecht M (2005) Simultaneous COD, nitrogen, and phosphate removal by aerobic granular sludge. Biotechnol Bioeng 90(6):761–769

    Article  PubMed  Google Scholar 

  • de Kreuk MK, Kishida N, van Loosdrecht MCM (2007) Aerobic granular sludge—state of the art. Water Sci Technol 55(8–9):75–81

    Article  PubMed  Google Scholar 

  • Figueroa M, Mosquera-Corral A, Campos J, Méndez R (2008) Treatment of saline wastewater in SBR aerobic granular reactors. Water Sci Technol 58(2):479–485

    Article  CAS  PubMed  Google Scholar 

  • Franca RD, Vieira A, Mata AM, Carvalho GS, Pinheiro HM, Lourenço ND (2015) Effect of an azo dye on the performance of an aerobic granular sludge sequencing batch reactor treating a simulated textile wastewater. Water Res 85:327–336

    Article  CAS  PubMed  Google Scholar 

  • Gao DW, Liu L, Liang H, Wu WM (2011) Aerobic granular sludge: characterization, mechanism of granulation and application to wastewater treatment. Crit Rev Biotechnol 31(2):137–152

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Wang J, Wen X, Qian Y (2005) The formation and characteristics of aerobic granules in sequencing batch reactor (SBR) by seeding anaerobic granules. Process Biochem 40(1):5–11

    Article  CAS  Google Scholar 

  • Jemaat Z, Suárez-Ojeda ME, Pérez J, Carrera J (2014) Partial nitritation and o-cresol removal with aerobic granular biomass in a continuous airlift reactor. Water Res 48:354–362

    Article  CAS  PubMed  Google Scholar 

  • Juang YC, Adav SS, Lee DJ, Tay JH (2010) Stable aerobic granules for continuous-flow reactors: precipitating calcium and iron salts in granular interiors. Bioresour Technol 101(21):8051–8057

    Article  CAS  PubMed  Google Scholar 

  • Li D, Lv Y, Zeng H, Zhang J (2016a) Enhanced biological phosphorus removal using granules in continuous-flow reactor. Chem Eng J 298:107–116

    Article  CAS  Google Scholar 

  • Li D, Lv Y, Zeng H, Zhang J (2016b) Startup and long term operation of enhanced biological phosphorus removal in continuous-flow reactor with granules. Bioresour Technol 212:92–99

    Article  CAS  PubMed  Google Scholar 

  • Liu WT, Chan OC, Fang HH (2002) Microbial community dynamics during start-up of acidogenic anaerobic reactors. Water Res 36(13):3203–3210

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Tay JH (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36(7):1653–1665

    Article  CAS  PubMed  Google Scholar 

  • Lv Y, Wan C, Lee D-J, Liu X, Tay J-H (2014) Microbial communities of aerobic granules: granulation mechanisms. Bioresour Technol 169:344–351

    Article  CAS  PubMed  Google Scholar 

  • Nagendra H (2002) Opposite trends in response for the Shannon and Simpson indices of landscape diversity. Appl Geogr 22(2):175–186

    Article  Google Scholar 

  • Ni BJ, Xie WM, Liu SG, Yu HQ, Wang YZ, Wang G, Dai X-L (2009) Granulation of activated sludge in a pilot-scale sequencing batch reactor for the treatment of low-strength municipal wastewater. Water Res 43(3):751–761

    Article  CAS  PubMed  Google Scholar 

  • Oren A (2014) The family Rhodocyclaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin/Heidelberg, Germany, pp 975–998

    Chapter  Google Scholar 

  • Pronk M, de Kreuk M, de Bruin B, Kamminga P, Kleerebezem R, van Loosdrecht M (2015) Full scale performance of the aerobic granular sludge process for sewage treatment. Water Res 84:207–217

    Article  CAS  PubMed  Google Scholar 

  • Satoh H, Miura Y, Tsushima I, Okabe S (2007) Layered structure of bacterial and archaeal communities and their in situ activities in anaerobic granules. Appl Environ Microbiol 73(22):7300–7307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saunders AM, Albertsen M, Vollertsen J, Nielsen PH (2016) The activated sludge ecosystem contains a core community of abundant organisms. ISME J 10:11–20

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60

    Article  PubMed  PubMed Central  Google Scholar 

  • Song Y, Ishii S, Rathnayake L, Ito T, Satoh H, Okabe S (2013) Development and characterization of the partial nitrification aerobic granules in a sequencing batch airlift reactor. Bioresour Technol 139:285–291

    Article  CAS  PubMed  Google Scholar 

  • Stein LY, Arp DJ, Berube PM, Chain PS, Hauser L, Jetten MS, Klotz MG, Larimer FW, Norton JM, Op den Camp HJ (2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ Microbiol 9(12):2993–3007

    Article  CAS  PubMed  Google Scholar 

  • Teixeira LM, Merquior VLC (2014) The family Moraxellaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Gammaproteobacteria. Springer, Berlin/Heidelberg, Germany, pp 443–476

    Google Scholar 

  • Tsuneda S, Nagano T, Hoshino T, Ejiri Y, Noda N, Hirata A (2003) Characterization of nitrifying granules produced in an aerobic upflow fluidized bed reactor. Water Res 37(20):4965–4973

    Article  CAS  PubMed  Google Scholar 

  • van der Roest H, de Bruin L, Gademan G, Coelho F (2011) Towards sustainable waste water treatment with Dutch Nereda® technology. Water Pract Technol 6(3):wpt2011059

    Google Scholar 

  • Verawaty M, Pijuan M, Yuan Z, Bond P (2012) Determining the mechanisms for aerobic granulation from mixed seed of floccular and crushed granules in activated sludge wastewater treatment. Water Res 46(3):761–771

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Du GC, Chen J (2004) Aerobic granular sludge cultivated under the selective pressure as a driving force. Process Biochem 39(5):557–563

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willems A (2014) The family Comamonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin/Heidelberg, pp 975–998

  • Winkler MH, Kleerebezem R, De Bruin L, Verheijen P, Abbas B, Habermacher J, Van Loosdrecht M (2013) Microbial diversity differences within aerobic granular sludge and activated sludge flocs. Appl Microbiol Biotechnol 97(16):7447–7458

    Article  CAS  PubMed  Google Scholar 

  • Wu J-H, Liu W-T, Tseng I-C, Cheng S-S (2001) Characterization of microbial consortia in a terephthalate-degrading anaerobic granular sludge system. Microbiology 147(2):373–382

    Article  CAS  PubMed  Google Scholar 

  • Xu G, Peng J, Feng C, Fang F, Chen S, Xu Y, Wang X (2015) Evaluation of simultaneous autotrophic and heterotrophic denitrification processes and bacterial community structure analysis. Appl Microbiol Biotechnol 99(15):6527–6536

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Zhang S, Hao G, Zhang X, Ren Y, Wen Y, Guo Y, Zhang Y (2016) Simultaneous nitrification and denitrification by EPSs in aerobic granular sludge enhanced nitrogen removal of ammonium-nitrogen-rich wastewater. Bioresour Technol 202:101–106

    Article  CAS  PubMed  Google Scholar 

  • Ye L, Zhang T (2011) Ammonia-oxidizing bacteria dominates over ammonia-oxidizing archaea in a saline nitrification reactor under low DO and high nitrogen loading. Biotechnol Bioeng 108(11):2544–2552

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Chen Z, Qiu Z, Jin M, Chen Z, Chen Z, Li J, Wang X, Wang J (2011) Dynamic and distribution of ammonia-oxidizing bacteria communities during sludge granulation in an anaerobic–aerobic sequencing batch reactor. Water Res 45(18):6207–6216

    Article  CAS  Google Scholar 

  • Zhang T, Shao MF, Ye L (2012) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6(6):1137–1147

    Article  CAS  PubMed  Google Scholar 

  • Zheng YM, Yu HQ, Liu SJ, Liu XZ (2006) Formation and instability of aerobic granules under high organic loading conditions. Chemosphere 63(10):1791–1800

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Kailong Huang for the assistance in the sequencing and data analysis.

Funding

This work was supported by the Natural Science Foundation of Jiangsu Province (BK20160657), the National Natural Science Foundation of China (51608256, 51378252), Science Foundation for Distinguished Young Scholars of Jiangsu Province of China (SBK2015010297) and National Key Technology Support Program of China (2014BAC08B04).

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Authors and Affiliations

  1. State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, 163 Xianlin Avenue, Nanjing, 210023, China

    Haohao Sun, Qiaoling Li, Hongqiang Ren, Bo Liu, Lin Ye & Xu-Xiang Zhang

  2. Jiangsu Information Institute of Science and Technology, 117 Longpan Road, Nanjing, 210042, China

    Ping Yu

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  1. Haohao Sun
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Correspondence to Lin Ye or Xu-Xiang Zhang.

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Sun, H., Yu, P., Li, Q. et al. Transformation of anaerobic granules into aerobic granules and the succession of bacterial community. Appl Microbiol Biotechnol 101, 7703–7713 (2017). https://doi.org/10.1007/s00253-017-8491-2

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  • DOI: https://doi.org/10.1007/s00253-017-8491-2

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