Applied Microbiology and Biotechnology

, Volume 102, Issue 9, pp 3967–3979 | Cite as

Microbial community structure and function in aerobic granular sludge

  • Juntao Xia
  • Lin Ye
  • Hongqiang Ren
  • Xu-Xiang Zhang


Aerobic granular sludge (AGS), a self-immobilized microbial consortium containing different functional microorganisms, is receiving growing attention, since it has shown great technological and economical potentials in the field of wastewater treatment. Microbial community is crucial for the formation, stability, and pollutant removal efficiency of aerobic granules. This mini-review systematically summarizes the recent findings of the microbial community structure and function of AGS and discusses the new research progress in the microbial community dynamics during the granulation process and spatial distribution patterns of the microbiota in AGS. The presented information may be helpful for the in-depth theoretical study and practical application of AGS technology in the future.


Aerobic granular sludge Microbial community Microbial community function Wastewater treatment 



This work was supported by the Natural Science Foundation for Distinguished Young Scholars of Jiangsu Province China (BK20150019) and the Natural Science Foundation of Jiangsu Province (BK20160657).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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


  1. Adav SS, Lee DJ (2008) Single-culture aerobic granules with Acinetobacter calcoaceticus. Appl Microbiol Biotechnol 78(3):551–557. PubMedCrossRefGoogle Scholar
  2. Adav SS, Lee DJ, Lai JY (2007a) Effects of aeration intensity on formation of phenol-fed aerobic granules and extracellular polymeric substances. Appl Microbiol Biotechnol 77(1):175–182. PubMedCrossRefGoogle Scholar
  3. Adav SS, Lee DJ, Ren NQ (2007b) Biodegradation of pyridine using aerobic granules in the presence of phenol. Water Res 41(13):2903–2910. PubMedCrossRefGoogle Scholar
  4. Adav SS, Lee DJ, Show KY, Tay JH (2008a) Aerobic granular sludge: recent advances. Biotechnol Adv 26(5):411–423. PubMedCrossRefGoogle Scholar
  5. Adav SS, Lee DJ, Tay JH (2008b) Extracellular polymeric substances and structural stability of aerobic granule. Water Res 42(6–7):1644–1650. PubMedCrossRefGoogle Scholar
  6. Adav SS, Lee DJ, Lai JY (2009) Aerobic granulation in sequencing batch reactors at different settling times. Bioresour Technol 100(21):5359–5361. PubMedCrossRefGoogle Scholar
  7. Adav SS, Lee DJ, Lai JY (2010) Microbial community of acetate utilizing denitrifiers in aerobic granules. Appl Microbiol Biotechnol 85(3):753–762. PubMedCrossRefGoogle Scholar
  8. Amorim CL, Maia AS, Mesquita RB, Rangel AO, van Loosdrecht MC, Tiritan ME, Castro PM (2014) Performance of aerobic granular sludge in a sequencing batch bioreactor exposed to ofloxacin, norfloxacin and ciprofloxacin. Water Res 50:101–113. PubMedCrossRefGoogle Scholar
  9. Amorim CL, Moreira IS, Ribeiro AR, Santos LHMLM, Delerue-Matos C, Tiritan ME, Castro PML (2016) Treatment of a simulated wastewater amended with a chiral pharmaceuticals mixture by an aerobic granular sludge sequencing batch reactor. Int Biodeterior Biodegrad 115:277–285. CrossRefGoogle Scholar
  10. Amorim CL, Alves M, Castro PM, Henriques I (2017) Bacterial community dynamics within an aerobic granular sludge reactor treating wastewater loaded with pharmaceuticals. Ecotoxicol Environ Saf 147:905–912. PubMedCrossRefGoogle Scholar
  11. Aqeel H, Basuvaraj M, Hall M, Neufeld JD, Liss SN (2016) Microbial dynamics and properties of aerobic granules developed in a laboratory-scale sequencing batch reactor with an intermediate filamentous bulking stage. Appl Microbiol Biotechnol 100(1):447–460. PubMedCrossRefGoogle Scholar
  12. Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Icwsm 8:361–362Google Scholar
  13. Beun JJ, van Loosdrecht MC, Heijnen JJ (2002) Aerobic granulation in a sequencing batch airlift reactor. Water Res 36(3):702–712. PubMedCrossRefGoogle Scholar
  14. Bin Z, Zhe C, Zhigang Q, Min J, Zhiqiang C, Zhaoli C, Junwen L, Xuan W, Jingfeng W (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. PubMedCrossRefGoogle Scholar
  15. Cassidy DP, Belia E (2005) Nitrogen and phosphorus removal from an abattoir wastewater in a SBR with aerobic granular sludge. Water Res 39(19):4817–4823. PubMedCrossRefGoogle Scholar
  16. Chen MY, Lee DJ, Tay JH (2007) Distribution of extracellular polymeric substances in aerobic granules. Appl Microbiol Biotechnol 73(6):1463–1469. PubMedCrossRefGoogle Scholar
  17. Chen YC, Chen D, Peng LC, Fu SY, Zhan HY (2009) The microorganism community of pentachlorophenol (PCP)-degrading coupled granules. Water Sci Technol 59(5):987–994. PubMedCrossRefGoogle Scholar
  18. Chen CQ, Bin LY, Tang B, Huang SS, Fu FL, Chen QY, Wu LY, Wu CM (2017) Cultivating granular sludge directly in a continuous-flow membrane bioreactor with internal circulation. Chem Eng J 309:108–117. CrossRefGoogle Scholar
  19. Crocetti GR, Banfield JF, Keller J, Bond PL, Blackall LL (2002) Glycogen-accumulating organisms in laboratory-scale and full-scale wastewater treatment processesb. Microbiology 148(11):3353–3364. PubMedCrossRefGoogle Scholar
  20. Dai Y, Jiang Y, Su H (2015) Influence of an aniline supplement on the stability of aerobic granular sludge. J Environ Manag 162:115–122. CrossRefGoogle Scholar
  21. de Bruin LM, de Kreuk MK, van der Roest HF, Uijterlinde C, van Loosdrecht MC (2004) Aerobic granular sludge technology: an alternative to activated sludge? Water Sci Technol 49(11–12):1–7PubMedGoogle Scholar
  22. de Kreuk MV, Van Loosdrecht M (2004) Selection of slow growing organisms as a means for improving aerobic granular sludge stability. Water Sci Technol 49(11–12):9–17PubMedGoogle Scholar
  23. De Kreuk MK, van Loosdrecht MC (2006) Formation of aerobic granules with domestic sewage. J Environ Eng 132(6):694–697. CrossRefGoogle Scholar
  24. Di Iaconi C, Ramadori R, Lopez A, Passino R (2005) Hydraulic shear stress calculation in a sequencing batch biofilm reactor with granular biomass. Environ Sci Technol 39(3):889–894. PubMedCrossRefGoogle Scholar
  25. Dong J, Zhang Z, Yu Z, Dai X, Xu X, Alvarez PJ, Zhu L (2017) Evolution and functional analysis of extracellular polymeric substances during the granulation of aerobic sludge used to treat p-chloroaniline wastewater. Chem Eng J 330:596–604. CrossRefGoogle Scholar
  26. Duque AF, Bessa VS, Castro PM (2015) Characterization of the bacterial communities of aerobic granules in a 2-fluorophenol degrading process. Biotechnology Reports 5:98–104. PubMedCrossRefGoogle Scholar
  27. Ebrahimi S, Gabus S, Rohrbach-Brandt E, Hosseini M, Rossi P, Maillard J, Holliger C (2010) Performance and microbial community composition dynamics of aerobic granular sludge from sequencing batch bubble column reactors operated at 20 a degrees C, 30 a degrees C, and 35 a degrees C. Appl Microbiol Biotechnol 87(4):1555–1568. PubMedCrossRefGoogle Scholar
  28. Fang F, Liu XW, Xu J, Yu HQ, Li YM (2009) Formation of aerobic granules and their PHB production at various substrate and ammonium concentrations. Bioresour Technol 100(1):59–63. PubMedCrossRefGoogle Scholar
  29. Figueroa M, Val del Rio A, Campos JL, Mendez R, Mosquera-Corral A (2015) Filamentous bacteria existence in aerobic granular reactors. Bioprocess Biosyst Eng 38(5):841–851. PubMedCrossRefGoogle Scholar
  30. Franca RD, Vieira A, Mata AM, Carvalho GS, Pinheiro HM, Lourenco 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. PubMedCrossRefGoogle Scholar
  31. Fra-Vazquez A, Morales N, Figueroa M, del Rio AV, Regueiro L, Campos JL, Mosquera-Corral A (2016) Bacterial community dynamics in long-term operation of a pilot plant using aerobic granular sludge to treat pig slurry. Biotechnol Prog 32(5):1212–1221. PubMedCrossRefGoogle Scholar
  32. Gao D, Peng Y, Wu W-M (2010) Kinetic model for biological nitrogen removal using shortcut nitrification-denitrification process in sequencing batch reactor. Environ Sci Technol 44(13):5015–5021. PubMedCrossRefGoogle Scholar
  33. Gao D, 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. PubMedCrossRefGoogle Scholar
  34. Garrity G, Brenner DJ, Krieg NR, Staley J, Boone DR (2011) Bergey’s manual of systematic bacteriology: volume two Proteobacteria (part C). SpringerGoogle Scholar
  35. Gómez-Acata S, Vital-Jácome M, Pérez-Sandoval MV, Navarro-Noya YE, Thalasso F, Luna-Guido M, Conde-Barajas E, Dendooven L (2018) Microbial community structure in aerobic and fluffy granules formed in a sequencing batch reactor supplied with 4-chlorophenol at different settling times. J Hazard Mater 342:606–616. PubMedCrossRefGoogle Scholar
  36. Gonzalezgil G, Holliger C (2011) Dynamics of microbial community structure of and enhanced biological phosphorus removal by aerobic granules cultivated on propionate or acetate. Appl Environ Microbiol 77(22):8041–8051. CrossRefGoogle Scholar
  37. He Q, Zhou J, Wang H, Zhang J, Wei L (2016) Microbial population dynamics during sludge granulation in an A/O/A sequencing batch reactor. Bioresour Technol 214:1–8. PubMedCrossRefGoogle Scholar
  38. Henriet O, Meunier C, Henry P, Mahillon J (2016) Improving phosphorus removal in aerobic granular sludge processes through selective microbial management. Bioresour Technol 211:298–306. PubMedCrossRefGoogle Scholar
  39. Irie K, Fujitani H, Tsuneda S (2016) Physical enrichment of uncultured Accumulibacter and Nitrospira from activated sludge by unlabeled cell sorting technique. J Biosci Bioeng 122(4):475–481. PubMedCrossRefGoogle Scholar
  40. Ivanov V, Wang XH, Tay STL, Tay JH (2006) Bioaugmentation and enhanced formation of microbial granules used in aerobic wastewater treatment. Appl Microbiol Biotechnol 70(3):374–381. PubMedCrossRefGoogle Scholar
  41. 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. PubMedCrossRefGoogle Scholar
  42. Jiang H-L, Tay J-H, Maszenan AM, Tay ST-L (2004) Bacterial diversity and function of aerobic granules engineered in a sequencing batch reactor for phenol degradation. Appl Environ Microbiol 70(11):6767–6775. PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jiang Y, Wei L, Yang K, Shi X, Wang H (2017) Rapid formation of aniline-degrading aerobic granular sludge and investigation of its microbial community succession. J Clean Prod 166:1235–1243. CrossRefGoogle Scholar
  44. Kagawa Y, Tahata J, Kishida N, Matsumoto S, Picioreanu C, van Loosdrecht M, Tsuneda S (2015) Modeling the nutrient removal process in aerobic granular sludge system by coupling the reactor-and granule-scale models. Biotechnol Bioeng 112(1):53–64. PubMedCrossRefGoogle Scholar
  45. Kong Q, Wang Z-B, Shu L, Miao M-S (2015) Characterization of the extracellular polymeric substances and microbial community of aerobic granulation sludge exposed to cefalexin. Int Biodeterior Biodegrad 102:375–382. CrossRefGoogle Scholar
  46. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55(1):485–529. PubMedCrossRefGoogle Scholar
  47. Lemaire RLG (2007) Development and fundamental investigations of innovative technologies for biological nutrient removal from abattoir wastewater. University of QueenslandGoogle Scholar
  48. Lemaire R, Webb RI, Yuan ZG (2008a) Micro-scale observations of the structure of aerobic microbial granules used for the treatment of nutrient-rich industrial wastewater. Isme J 2(5):528–541. PubMedCrossRefGoogle Scholar
  49. Lemaire R, Yuan Z, Blackall LL, Crocetti GR (2008b) Microbial distribution of Accumulibacter spp. and Competibacter spp. in aerobic granules from a lab-scale biological nutrient removal system. Environ Microbiol 10(2):354–363. PubMedCrossRefGoogle Scholar
  50. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461(7261):254–257. PubMedCrossRefGoogle Scholar
  51. Li AJ, Yang SF, Li XY, Gu JD (2008) Microbial population dynamics during aerobic sludge granulation at different organic loading rates. Water Res 42(13):3552–3560. PubMedCrossRefGoogle Scholar
  52. Li J, Ding LB, Cai A, Huang GX, Horn H (2014a) Aerobic sludge granulation in a full-scale sequencing batch reactor. Biomed Res Int 2014(5):268789–268712. PubMedPubMedCentralGoogle Scholar
  53. Li Y, Zou J, Zhang L, Sun J (2014b) Aerobic granular sludge for simultaneous accumulation of mineral phosphorus and removal of nitrogen via nitrite in wastewater. Bioresour Technol 154:178–184. PubMedCrossRefGoogle Scholar
  54. Li K, Wei D, Zhang G, Shi L, Wang Y, Wang B, Wang X, Du B, Wei Q (2015) Toxicity of bisphenol A to aerobic granular sludge in sequencing batch reactors. J Mol Liq 209:284–288. CrossRefGoogle Scholar
  55. Linlin H, Jianlong W, Xianghua W, Yi Q (2005) The formation and characteristics of aerobic granules in sequencing batch reactor (SBR) by seeding anaerobic granules. Process Biochem 40(1):5–11. CrossRefGoogle Scholar
  56. Liu Y, Liu QS (2006) Causes and control of filamentous growth in aerobic granular sludge sequencing batch reactors. Biotechnol Adv 24(1):115–127. PubMedCrossRefGoogle Scholar
  57. 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. PubMedCrossRefGoogle Scholar
  58. Liu YQ, Tay JH (2008) Influence of starvation time on formation and stability of aerobic granules in sequencing batch reactors. Bioresour Technol 99(5):980–985. PubMedCrossRefGoogle Scholar
  59. Liu YQ, Liu Y, Tay JH (2004) The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl Microbiol Biotechnol 65(2):143–148. PubMedCrossRefGoogle Scholar
  60. Liu B, Zhang F, Feng X, Liu Y, Yan X, Zhang X, Wang L, Zhao L (2005) Thauera and Azoarcus as functionally important genera in a denitrifying quinoline-removal bioreactor as revealed by microbial community structure comparison. FEMS Microbiol Ecol 55(2):274–286. CrossRefGoogle Scholar
  61. Liu XW, Sheng GP, Yu HQ (2009) Physicochemical characteristics of microbial granules. Biotechnol Adv 27(6):1061–1070. PubMedCrossRefGoogle Scholar
  62. Liu L, You Q, Gibson V, Huang X, Chen S, Ye Z, Liu C (2015a) Treatment of swine wastewater in aerobic granular reactors: comparison of different seed granules as factors. Front Env Sci Eng 9(6):1139–1148. CrossRefGoogle Scholar
  63. Liu X, Chen Y, Zhang X, Jiang X, Wu S, Shen J, Sun X, Li J, Lu L, Wang L (2015b) Aerobic granulation strategy for bioaugmentation of a sequencing batch reactor (SBR) treating high strength pyridine wastewater. J Hazard Mater 295:153–160. PubMedCrossRefGoogle Scholar
  64. Long B, Yang CZ, Pu WH, Yang JK, Liu FB, Zhang L, Zhang J, Cheng K (2015) Tolerance to organic loading rate by aerobic granular sludge in a cyclic aerobic granular reactor. Bioresour Technol 182:314–322. PubMedCrossRefGoogle Scholar
  65. Lotti T, Kleerebezem R, Hu Z, Kartal B, de Kreuk MK, van Erp Taalman Kip C, Kruit J, Hendrickx TL, van Loosdrecht MC (2015) Pilot-scale evaluation of anammox-based mainstream nitrogen removal from municipal wastewater. Environ Technol 36(9–12):1167–1177. PubMedCrossRefGoogle Scholar
  66. Luo J, Hao T, Wei L, Mackey HR, Lin Z, Chen G-H (2014) Impact of influent COD/N ratio on disintegration of aerobic granular sludge. Water Res 62:127–135. PubMedCrossRefGoogle Scholar
  67. Luo JH, Wei L, Hao TW, Xue WQ, Mackey HR, Chena GH (2015) Effect of L-tyrosine on aerobic sludge granulation and its stability. RSC Adv 5(105):86513–86521. CrossRefGoogle Scholar
  68. Luo J, Chen H, Han X, Sun Y, Yuan Z, Guo J (2017) Microbial community structure and biodiversity of size-fractionated granules in a partial nitritation-anammox process. FEMS Microbiol Ecol 93(6):fix021 doi:
  69. Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014a) The effect of quorum sensing and extracellular proteins on the microbial attachment of aerobic granular activated sludge. Bioresour Technol 152:53–58. PubMedCrossRefGoogle Scholar
  70. Lv Y, Wan C, Lee DJ, Liu X, Tay JH (2014b) Microbial communities of aerobic granules: granulation mechanisms. Bioresour Technol 169:344–351. PubMedCrossRefGoogle Scholar
  71. Majone M, Beccari M, Dionisi D, Levantesi C, Ramadori R, Tandoi V (2007) Effect of periodic feeding on substrate uptake and storage rates by a pure culture of Thiothrix (CT3 strain). Water Res 41(1):177–187. PubMedCrossRefGoogle Scholar
  72. Mañas A, Biscans B, Spérandio M (2011) Biologically induced phosphorus precipitation in aerobic granular sludge process. Water Res 45(12):3776–3786. CrossRefGoogle Scholar
  73. Matsuyama H, Katoh H, Ohkushi T, Satoh A, Kawahara K, Yumoto I (2008) Sphingobacterium kitahiroshimense sp. nov., isolated from soil. Int J Syst Evol Microbiol 58(Pt 7):1576–1579. PubMedCrossRefGoogle Scholar
  74. McSwain BS, Irvine RL, Wilderer PA (2004) The influence of settling time on the formation of aerobic granules. Water Sci Technol 50(10):195–202PubMedGoogle Scholar
  75. Metsalu T, Vilo J (2015) ClustVis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res 43(W1):W566–W570. PubMedPubMedCentralCrossRefGoogle Scholar
  76. Morales N, Figueroa M, Fra-Vázquez A, Del Río AV, Campos J, Mosquera-Corral A, Méndez R (2013) Operation of an aerobic granular pilot scale SBR plant to treat swine slurry. Process Biochem 48(8):1216–1221. CrossRefGoogle Scholar
  77. Nancharaiah Y, Reddy GKK (2017) Aerobic granular sludge technology: mechanisms of granulation and biotechnological applications. Bioresour Technol 247:1128–1143. PubMedCrossRefGoogle Scholar
  78. Ni B-J, Xie W-M, Liu S-G, Yu H-Q, Wang Y-Z, 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. PubMedCrossRefGoogle Scholar
  79. Nielsen PH, Mielczarek AT, Kragelund C, Nielsen JL, Saunders AM, Kong Y, Hansen AA, Vollertsen J (2010) A conceptual ecosystem model of microbial communities in enhanced biological phosphorus removal plants. Water Res 44(17):5070–5088. PubMedCrossRefGoogle Scholar
  80. Park HD, Regan JM, Noguera DR (2002) Molecular analysis of ammonia-oxidizing bacterial populations in aerated-anoxic orbal processes. Water Sci Technol 46(1–2):273–280PubMedGoogle Scholar
  81. Picioreanu C, Kreft JU, Van Loosdrecht MC (2004) Particle-based multidimensional multispecies biofilm model. Appl Environ Microbiol 70(5):3024–3040. PubMedPubMedCentralCrossRefGoogle Scholar
  82. Pronk M, de Kreuk MK, de Bruin B, Kamminga P, Kleerebezem R, van Loosdrecht MC (2015) Full scale performance of the aerobic granular sludge process for sewage treatment. Water Res 84:207–217. PubMedCrossRefGoogle Scholar
  83. Ramos C, Suarez-Ojeda ME, Carrera J (2016) Biodegradation of a high-strength wastewater containing a mixture of ammonium, aromatic compounds and salts with simultaneous nitritation in an aerobic granular reactor. Process Biochem 51(3):399–407. CrossRefGoogle Scholar
  84. Reynaert E (2017) Effect of in influent composition on the microbial communities and granulation process in aerobic granular sludge systems. Dissertation, École polytechnique fédérale de LausanneGoogle Scholar
  85. Seviour RJ, McIlroy S (2008) The microbiology of phosphorus removal in activated sludge processes-the current state of play. J Microbiol 46(2):115–124. PubMedCrossRefGoogle Scholar
  86. Seviour T, Pijuan M, Nicholson T, Keller J, Yuan ZG (2009) Gel-forming exopolysaccharides explain basic differences between structures of aerobic sludge granules and floccular sludges. Water Res 43(18):4469–4478. PubMedCrossRefGoogle Scholar
  87. Shi Y, Xing S, Wang X, Wang S (2013) Changes of the reactor performance and the properties of granular sludge under tetracycline (TC) stress. Bioresour Technol 139:170–175. PubMedCrossRefGoogle Scholar
  88. Show KY, Lee DJ, Tay JH (2012) Aerobic granulation: advances and challenges. Appl Biochem Biotechnol 167(6):1622–1640. PubMedCrossRefGoogle Scholar
  89. Song Z, Pan Y, Zhang K, Ren N, Wang A (2010) Effect of seed sludge on characteristics and microbial community of aerobic granular sludge. J Environ Sci (China) 22(9):1312–1318. CrossRefGoogle Scholar
  90. Su KZ, Yu HQ (2005) Formation and characterization of aerobic granules in a sequencing batch reactor treating soybean-processing wastewater. Environ Sci Technol 39(8):2818–2827. PubMedCrossRefGoogle Scholar
  91. Sun H, Yu P, Li Q, Ren H, Liu B, Ye L, Zhang X-X (2017) Transformation of anaerobic granules into aerobic granules and the succession of bacterial community. Appl Microbiol Biotechnol 101(20):7703–7713. PubMedCrossRefGoogle Scholar
  92. Szabo E, Liebana R, Hermansson M, Modin O, Persson F, Wilen BM (2017) Microbial population dynamics and ecosystem functions of anoxic/aerobic granular sludge in sequencing batch reactors operated at different organic loading rates. Front Microbiol 8:1–14. CrossRefGoogle Scholar
  93. Tay JH, Tay STL, Ivanov V, Pan S, Jiang HL, Liu QS (2003) Biomass and porosity profiles in microbial granules used for aerobic wastewater treatment. Lett Appl Microbiol 36(5):297–301. PubMedCrossRefGoogle Scholar
  94. Verawaty M, Pijuan M, Yuan Z, Bond PL (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. PubMedCrossRefGoogle Scholar
  95. Wan C, Chen S, Wen L, Lee DJ, Liu X (2015) Formation of bacterial aerobic granules: role of propionate. Bioresour Technol 197:489–494. PubMedCrossRefGoogle Scholar
  96. Wan C, Shen Y, Chen S, Liu X, Liu G, Lai JY, Lee DJ (2016) Microstructural strength deterioration of aerobic granule sludge under organic loading swap. Bioresour Technol 221:671–676. PubMedCrossRefGoogle Scholar
  97. Wang Q, Du G, Chen J (2004) Aerobic granular sludge cultivated under the selective pressure as a driving force. Process Biochem 39(5):557–563. CrossRefGoogle Scholar
  98. Wang Z, Liu L, Yao J, Cai W (2006) Effects of extracellular polymeric substances on aerobic granulation in sequencing batch reactors. Chemosphere 63(10):1728–1735PubMedCrossRefGoogle Scholar
  99. Wang Z, Gao M, She Z, Wang S, Jin C, Zhao Y, Yang S, Guo L (2015) Effects of salinity on performance, extracellular polymeric substances and microbial community of an aerobic granular sequencing batch reactor. Sep Purif Technol 144:223–231. CrossRefGoogle Scholar
  100. Wang L, Deng S, Wang S, Su H (2017) Analysis of aerobic granules under the toxic effect of ampicillin in sequencing batch reactors: performance and microbial community. J Environ Manag 204(Pt 1):152–159. CrossRefGoogle Scholar
  101. Weber S, Ludwig W, Schleifer K-H, Fried J (2007) Microbial composition and structure of aerobic granular sewage biofilms. Appl Environ Microbiol 73(19):6233–6240. PubMedPubMedCentralCrossRefGoogle Scholar
  102. Weissbrodt DG, Lochmatter S, Ebrahimi S, Rossi P, Maillard J, Holliger C (2012) Bacterial selection during the formation of early-stage aerobic granules in wastewater treatment systems operated under wash-out dynamics. Front Microbiol 3:332. PubMedPubMedCentralCrossRefGoogle Scholar
  103. Weissbrodt DG, Neu T, Lochmatter S, Holliger C (2013a) The biofilm granulation mechanisms depend on the predominant populations involved 71st annual assembly of the SSM. Interlaken, SwitzerlandGoogle Scholar
  104. Weissbrodt DG, Neu TR, Kuhlicke U, Rappaz Y, Holliger C (2013b) Assessment of bacterial and structural dynamics in aerobic granular biofilms. Front Microbiol 4:175. PubMedPubMedCentralCrossRefGoogle Scholar
  105. Weissbrodt DG, Shani N, Holliger C (2014) Linking bacterial population dynamics and nutrient removal in the granular sludge biofilm ecosystem engineered for wastewater treatment. FEMS Microbiol Ecol 88(3):579–595. PubMedCrossRefGoogle Scholar
  106. Wells GF, Park HD, Yeung CH, Eggleston B, Francis CA, Criddle CS (2009) Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ Microbiol 11(9):2310–2328. PubMedCrossRefGoogle Scholar
  107. Winkler MK, Bassin JP, Kleerebezem R, Sorokin DY, van Loosdrecht MC (2012) Unravelling the reasons for disproportion in the ratio of AOB and NOB in aerobic granular sludge. Appl Microbiol Biotechnol 94(6):1657–1666. PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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. PubMedCrossRefGoogle Scholar
  109. Winkler M-K, Le QH, Volcke EI (2015) Influence of partial denitrification and mixotrophic growth of nob on microbial distribution in aerobic granular sludge. Environ Sci Technol 49(18):11003–11010. PubMedCrossRefGoogle Scholar
  110. Xavier JB, De Kreuk MK, Picioreanu C, Van Loosdrecht MC (2007) Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ Sci Technol 41(18):6410–6417. PubMedCrossRefGoogle Scholar
  111. 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. PubMedCrossRefGoogle Scholar
  112. 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. PubMedCrossRefGoogle Scholar
  113. Yang Y-C, Liu X, Wan C, Sun S, Lee D-J (2014) Accelerated aerobic granulation using alternating feed loadings: alginate-like exopolysaccharides. Bioresour Technol 171:360–366. PubMedCrossRefGoogle Scholar
  114. Yilmaz G, Lemaire R, Keller J, Yuan Z (2008) Simultaneous nitrification, denitrification, and phosphorus removal from nutrient-rich industrial wastewater using granular sludge. Biotechnol Bioeng 100(3):529–541. PubMedCrossRefGoogle Scholar
  115. Zhang B, Ji M, Qiu Z, Liu H, Wang J, Li J (2011) Microbial population dynamics during sludge granulation in an anaerobic–aerobic biological phosphorus removal system. Bioresour Technol 102(3):2474–2480. PubMedCrossRefGoogle Scholar
  116. 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. PubMedCrossRefGoogle Scholar
  117. Zhang Q, Hu J, Lee DJ (2016) Aerobic granular processes: current research trends. Bioresour Technol 210:74–80. PubMedCrossRefGoogle Scholar
  118. Zhang D, Li W, Hou C, Shen J, Jiang X, Sun X, Li J, Han W, Wang L, Liu X (2017) Aerobic granulation accelerated by biochar for the treatment of refractory wastewater. Chem Eng J 314:88–97. CrossRefGoogle Scholar
  119. Zhao Y, Huang J, Zhao H, Yang H (2013) Microbial community and N removal of aerobic granular sludge at high COD and N loading rates. Bioresour Technol 143:439–446. PubMedCrossRefGoogle Scholar
  120. Zhao X, Chen Z, Wang X, Li J, Shen J, Xu H (2015) Remediation of pharmaceuticals and personal care products using an aerobic granular sludge sequencing bioreactor and microbial community profiling using Solexa sequencing technology analysis. Bioresour Technol 179:104–112. PubMedCrossRefGoogle Scholar
  121. Zheng X-Y, Lu D, Chen W, Y-j G, Zhou G, Zhang Y, Zhou X, Jin M-Q (2017a) Response of aerobic granular sludge to the long-term presence of CuO NPs in A/O/A SBRs: nitrogen and phosphorus removal, enzymatic activity, and the microbial community. Environ Sci Technol 51(18):10503–10510. PubMedCrossRefGoogle Scholar
  122. Zheng, X-Y, Lu D, Wang M-y, Chen W, Zhou G, Zhang Y (2017b) Effect of chromium (VI) on the multiple nitrogen removal pathways and microbial community of aerobic granular sludge. Environ Technol (just-accepted):1–49.
  123. Zhou D, Niu S, Xiong Y, Yang Y, Dong S (2014) Microbial selection pressure is not a prerequisite for granulation: dynamic granulation and microbial community study in a complete mixing bioreactor. Bioresour Technol 161:102–108. PubMedCrossRefGoogle Scholar
  124. Zhu L, Dai X, Xu X, Lv M, Cao D (2014) Microbial community analysis for aerobic granular sludge reactor treating high-level 4-chloroaniline wastewater. Int J Environ Sci Technol (Tehran) 11(7):1845–1854. CrossRefGoogle Scholar
  125. Zou J, Li Y, Zhang L, Wang R, Sun J (2015) Understanding the impact of influent nitrogen concentration on granule size and microbial community in a granule-based enhanced biological phosphorus removal system. Bioresour Technol 177:209–216. PubMedCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Pollution Control and Resource Reuse, School of the EnvironmentNanjing UniversityNanjingChina

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