Applied Microbiology and Biotechnology

, Volume 103, Issue 21–22, pp 9181–9189 | Cite as

Impacts of environmental factors on AHL-producing and AHL-quenching activities of aerobic granules

  • Yu-Sheng Li
  • Jia-Shun Cao
  • Han-Qing YuEmail author
Environmental biotechnology


Aerobic granule is widely recognized as a promising biological wastewater treatment technique. Acyl-homoserine lactone (AHL)–mediated quorum sensing and quenching are reported to be involved in the formation of aerobic granules. However, little is known about how environmental factors affect the AHL-producing and AHL-quenching communities and their activities in aerobic granules. Therefore, in this work, the bacterial community of aerobic granules was explored and the impacts of substrate, electron acceptor, sludge concentration, pH, and temperature on the AHL-related communities and activities of aerobic granules were examined. These factors were found to affect the AHL-related activities, and thereby change the AHL level. The AHL-producing activities were observed to be more sensitive to the variation of these factors than the AHL-quenching activities. These findings help to establish the links between environmental factors and AHL-related activities and thus provide useful guides for the operation of aerobic granule systems.


Acyl-homoserine lactone (AHL) Aerobic granules Environmental factors Quorum sensing 


Funding information

This work was partially supported by the National Key R&D Program of China (2018YFC0406303), the National Natural Science Foundation of China (51808522, 51578210, 51538011 and 51821006), and the the Program for Changjiang Scholars and Innovative Research Team in University of the Ministry of Education of China.

Compliance with ethical standards

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

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2019_10080_MOESM1_ESM.pdf (516 kb)
ESM 1 (PDF 516 kb)


  1. Adav SS, Lee DJ, Lai JY (2010) Potential cause of aerobic granular sludge breakdown at high organic loading rates. Appl Microbiol Biotechnol 85:1601–1610CrossRefGoogle Scholar
  2. Burton E, Read H, Pellitteri M, Hickey W (2005) Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl Environ Microbiol 71:4906–4909CrossRefGoogle Scholar
  3. Chan KG, Atkinson S, Mathee K, Sam CK, Chhabra SR, Cámara M, Koh CL, Williams P (2011) Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol 11:51CrossRefGoogle Scholar
  4. Chen H, Li A, Cui D, Wang Q, Wu D, Cui C, Ma F (2018) N-Acyl-homoserine lactones and autoinducer-2-mediated quorum sensing during wastewater treatment. Appl Microbiol Biotechnol 102:1119–1130CrossRefGoogle Scholar
  5. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen A, McGarrell DM, Marsh T, Garrity GM (2008) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145CrossRefGoogle Scholar
  6. De Kreuk M, Heijnen J, Van Loosdrecht M (2005) Simultaneous COD, nitrogen, and phosphate removal by aerobic granular sludge. Biotechnol Bioeng 90:761–769CrossRefGoogle Scholar
  7. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  8. Feng H, Ding Y, Wang M, Zhou G, Zheng X, He H, Zhang X, Shen D, Shentu J (2014) Where are signal molecules likely to be located in anaerobic granular sludge? Water Res 50:1–9CrossRefGoogle Scholar
  9. Gao J, Ma A, Zhuang X, Zhuang G (2014) An N-acyl homoserine lactone synthase in the ammonia-oxidizing bacterium Nitrosospira multiformis. Appl Environ Microbiol 80:951–958CrossRefGoogle Scholar
  10. Huang JJ, Han JI, Zhang LH, Leadbetter JR (2003) Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69:5941–5949CrossRefGoogle Scholar
  11. Huang Y, Zeng Y, Yu Z, Zhang J (2013a) Distribution and diversity of acyl homoserine lactone producing bacteria from four different soils. Curr Microbiol 66:10–15CrossRefGoogle Scholar
  12. Huang Y, Zeng Y, Yu Z, Zhang J, Feng H, Lin X (2013b) In silico and experimental methods revealed highly diverse bacteria with quorum sensing and aromatics biodegradation systems-a potential broad application on bioremediation. Bioresour Technol 148:311–316CrossRefGoogle Scholar
  13. Kang YS, Park W (2010) Contribution of quorum sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J Appl Microbiol 109:1650–1659PubMedGoogle Scholar
  14. Li YC, Zhu JR (2014) Role of N-acyl homoserine lactone (AHL)-based quorum sensing (QS) in aerobic sludge granulation. Appl Microbiol Biotechnol 98:7623–7632CrossRefGoogle Scholar
  15. Li Y, Lv J, Zhong C, Hao W, Wang Y, Zhu J (2014) Performance and role of N-acyl-homoserine lactone (AHL)-based quorum sensing (QS) in aerobic granules. J Environ Sci 26:1615–1621CrossRefGoogle Scholar
  16. Li YS, Cao JS, Li BB, Li WW, Fang F, Tong ZH, Yu HQ (2016) Outcompeting presence of acyl-homoserine-lactone (AHL)-quenching bacteria over AHL-producing bacteria in aerobic granules. Environ Sci Technol Lett 3:36–40CrossRefGoogle Scholar
  17. Liu XW, Sheng GP, Yu HQ (2009) Physicochemical characteristics of microbial granules. Biotechnol Adv 27:1061–1070CrossRefGoogle Scholar
  18. Lynch MJ, Swift S, Kirke DF, Keevil CW, Dodd CE, Williams P (2002) The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ Microbiol 4:18–28CrossRefGoogle Scholar
  19. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  20. Rashid R, Morohoshi T, Someya N, Ikeda T (2011) Degradation of N-acylhomoserine lactone quorum sensing signaling molecules by potato root surface-associated Chryseobacterium strains. Microbes Environ 26:144–148CrossRefGoogle Scholar
  21. Ravn L, Christensen AB, Molin S, Givskov M, Gram L (2001) Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44:239–251CrossRefGoogle Scholar
  22. 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 75:7537–7541CrossRefGoogle Scholar
  23. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864CrossRefGoogle Scholar
  24. Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Cámara M, Williams P, Quax WJ (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74:1673–1682CrossRefGoogle Scholar
  25. Song ZW, Ren NQ, Zhang K, Tong LY (2009) Influence of temperature on the characteristics of aerobic granulation in sequencing batch airlift reactors. J Environ Sci 21:273–278CrossRefGoogle Scholar
  26. Sturm B, Irvine R (2008) Dissolved oxygen as a key parameter to aerobic granule formation. Water Sci Technol 58:781–787CrossRefGoogle Scholar
  27. Sun Y, Guan Y, Wang D, Liang K, Wu G (2018) Potential roles of acyl homoserine lactone based quorum sensing in sequencing batch nitrifying biofilm reactors with or without the addition of organic carbon. Bioresour Technol 259:136–145CrossRefGoogle Scholar
  28. Tan CH, Koh KS, Xie C, Zhang J, Tan XH, Lee GP, Zhou Y, Ng WJ, Rice SA, Kjelleberg S (2015) Community quorum sensing signalling and quenching: microbial granular biofilm assembly. NPJ Biofilms Microbi 1:15006CrossRefGoogle Scholar
  29. Tang KH, Zhang YH, Yu M, Shi XC, Coenye T, Bossier P, Zhang XH (2013) Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Sci Rep 3:2935CrossRefGoogle Scholar
  30. Tay JH, Liu QS, Liu Y (2001) The role of cellular polysaccharides in the formation and stability of aerobic granules. Lett Appl Microbiol 33:222–226CrossRefGoogle Scholar
  31. Toyofuku M, Nomura N, Fujii T, Takaya N, Maseda H, Sawada I, Nakajima T, Uchiyama H (2007) Quorum sensing regulates denitrification in Pseudomonas aeruginosa PAO1. J Bacteriol 189:4969–4972CrossRefGoogle Scholar
  32. Uroz S, Oger P, Chhabra SR, Cámara M, Williams P, Dessaux Y (2007) N-acyl homoserine lactones are degraded via an amidolytic activity in Comamonas sp. strain D1. Arch Microbiol 187:249–256CrossRefGoogle Scholar
  33. von Bodman SB, Farrand SK (1995) Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J Bacteriol 177:5000–5008CrossRefGoogle Scholar
  34. Wang F, Yang FL, Zhang XW, Liu YH, Zhang HM, Zhou J (2005) Effects of cycle time on properties of aerobic granules in sequencing batch airlift reactors. World J Microbiol Biotechnol 21:1379–1384CrossRefGoogle Scholar
  35. Wang WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T (2010) AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microbiol 76:2524–2530CrossRefGoogle Scholar
  36. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346CrossRefGoogle Scholar
  37. Wilén BM, Liébana R, Persson F, Modin O, Hermansson M (2018) The mechanisms of granulation of activated sludge in wastewater treatment, its optimization, and impact on effluent quality. Appl Microbiol Biotechnol 102:5005–5020CrossRefGoogle Scholar
  38. Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Cámara M, Smith H (2002) N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70:5635–5646CrossRefGoogle Scholar
  39. Zhu J, Chai Y, Zhong Z, Li S, Winans SC (2003) Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl Environ Microbiol 69:6949–6953CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Urban Pollutant Conversion, Department of Applied ChemistryUniversity of Science & Technology of ChinaHefeiChina
  2. 2.Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes, Ministry of EducationHohai UniversityNanjingChina

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