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N-Acyl-homoserine lactones and autoinducer-2-mediated quorum sensing during wastewater treatment

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Abstract

Bacteria can coordinate and synchronize activities through a cell density-dependent regulatory mechanism called quorum sensing (QS). Bacteria can measure their population by the synthesis, secretion, and perception of QS signal molecules to regulate specific gene expression when the population reaches a critical threshold. QS participates in various microbial processes such as marine organism bioluminescence, bacterial biofilm formation, and virulence factor expression. The use of QS systems mediated by N-acyl-homoserine lactones and autoinducer-2 has been recently recognized as a promising regulatory approach in environmental science and technology that can intrinsically promote the profound comprehension of wastewater treatment from a microbiology perspective. This article reviewed the study of QS in several environmental systems in wastewater treatment, including systems of aerobic granular sludge, biological nitrogen removal, and bioaugmentation, while several future prospects and suggestions are proposed on the basis of current studies.

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References

  • Ahn YH (2006) Sustainable nitrogen elimination biotechnologies: a review. Process Biochem 41:1709–1721

    Article  CAS  Google Scholar 

  • Arp DJ, Chain PSG, Klotz MG (2007) The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Annu Rev Microbiol 61:503–528

    Article  CAS  PubMed  Google Scholar 

  • Batchelor SE, Cooper M, Chhabra SR, Glover LA, Stewart GS, Williams P, Prosser JI (1997) Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria. Appl Environ Microbiol 63:2281–2286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burton EO, Read HW, Pellitteri MC, Hickey WJ (2005) Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl Environ Microbiol 71:4906–4909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549

    Article  CAS  PubMed  Google Scholar 

  • Chen YY, Ju SP, Lee DJ (2016) Aerobic granulation of protein-rich granules from nitrogen-lean wastewaters. Bioresour Technol 218:469–475

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Takahashi Y, Fujii N, Yamada Y, Satoh H, Okabe S (2010) Nitrogen removal performance and microbial community analysis of an anaerobic up-flow granular bed anammox reactor. Chemosphere 78:1129–1135

    Article  CAS  PubMed  Google Scholar 

  • Coma M, Verawaty M, Pijuan M, Yuan Z, Bond PL (2012) Enhancing aerobic granulation for biological nutrient removal from domestic wastewater. Bioresour Technol 103:101–108

    Article  CAS  PubMed  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daims H, Lucker S, Wagner M (2016) A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol 24:699–712

    Article  CAS  PubMed  Google Scholar 

  • Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298

    Article  CAS  PubMed  Google Scholar 

  • De Clippeleir H, Defoirdt T, Vanhaecke L, Vlaeminck S, Carballa M, Verstraete W, Boon N (2011) Long-chain acylhomoserine lactones increase the anoxic ammonium oxidation rate in an OLAND biofilm. Appl Microbiol Biotechnol 90:1511–1519

    Article  CAS  PubMed  Google Scholar 

  • Decho AW, Frey RL, Ferry JL (2011) Chemical challenges to bacterial AHL signaling in the environment. Chem Rev 111:86–99

    Article  CAS  PubMed  Google Scholar 

  • Deng Y, Wu J, Eberl L, Zhang LH (2010) Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl Environ Microbiol 76:4675–4683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devlin TR, di Biase A, Kowalski M, Oleszkiewicz JA (2017) Granulation of activated sludge under low hydrodynamic shear and different wastewater characteristics. Bioresour Technol 224:229–235

    Article  CAS  PubMed  Google Scholar 

  • Dickschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369

    Article  CAS  PubMed  Google Scholar 

  • Ding S, Zheng P, Lu H, Chen J, Mahmood Q, Abbas G (2013) Ecological characteristics of anaerobic ammonia oxidizing bacteria. Appl Microbiol Biotechnol 97:1841–1849

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Feng H, Huang W, Shen D, Wang M (2015a) A sustainable method for effective regulation of anaerobic granular sludge: artificially increasing the concentration of signal molecules by cultivating a secreting strain. Bioresour Technol 196:273–278

    Article  CAS  PubMed  Google Scholar 

  • Ding Z, Bourven I, Guibaud G, van Hullebusch ED, Panico A, Pirozzi F, Esposito G (2015b) Role of extracellular polymeric substances (EPS) production in bioaggregation: application to wastewater treatment. Appl Microbiol Biotechnol 99:9883–9905

    Article  CAS  PubMed  Google Scholar 

  • Dong J, Zhang Z, Yu Z, Dai X, Xu X, Alvarez PJJ, 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

    Article  CAS  Google Scholar 

  • Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449

    Article  CAS  PubMed  Google Scholar 

  • 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 50:1–9

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Nava Y, Maranon E, Soons J, Castrillon L (2010) Denitrification of high nitrate concentration wastewater using alternative carbon sources. J Hazard Mater 173:682–688

    Article  CAS  PubMed  Google Scholar 

  • Fernández I, Vázquez-Padín JR, Mosquera-Corral A, Campos JL, Méndez R (2008) Biofilm and granular systems to improve Anammox biomass retention. Biochem Eng J 42:308–313

    Article  CAS  Google Scholar 

  • Fuqua C, Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695

    Article  CAS  PubMed  Google Scholar 

  • Fuqua WC, Winans SC (1994) A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol 176:2796–2806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galloway WR, Hodgkinson JT, Bowden SD, Welch M, Spring DR (2011) Quorum sensing in gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 111:28–67

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Zhang H, Yang F, Li H, Zhang R (2014a) The effects of zero-valent iron (ZVI) and ferroferric oxide (Fe3O4) on anammox activity and granulation in anaerobic continuously stirred tank reactors (CSTR). Process Biochem 49:1970–1978

    Article  CAS  Google Scholar 

  • Gao J, Ma A, Zhuang X, Zhuang G (2014b) An N-acyl homoserine lactone synthase in the ammonia-oxidizing bacterium Nitrosospira multiformis. Appl Environ Microbiol 80:951–958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garg N, Manchanda G, Kumar A (2014) Bacterial quorum sensing: circuits and applications. Antonie Van Leeuwenhoek 105:289–305

    Article  PubMed  Google Scholar 

  • Geets J, Boon N, Verstraete W (2006) Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen fluctuations. FEMS Microbiol Ecol 58:1–13

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Martinez A, Munoz-Palazon B, Rodriguez-Sanchez A, Maza-Marquez P, Mikola A, Gonzalez-Lopez J, Vahala R (2017) Start-up and operation of an aerobic granular sludge system under low working temperature inoculated with cold-adapted activated sludge from Finland. Bioresour Technol 239:180–189

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Martinez A, Rodriguez-Sanchez A, van Loosdrecht MCM, Gonzalez-Lopez J, Vahala R (2016) Detection of comammox bacteria in full-scale wastewater treatment bioreactors using tag-454-pyrosequencing. Environ Sci Pollut Res 23:25501–25511

    Article  CAS  Google Scholar 

  • Guo Y, Liu S, Tang X, Yang F (2017) Role of c-di-GMP in anammox aggregation and systematic analysis of its turnover protein in Candidatus Jettenia caeni. Water Res 113:181–190

    Article  CAS  PubMed  Google Scholar 

  • Hamlin HJ, Michaels JT, Beaulaton CM, Graham WF, Dutt W, Steinbach P, Losordo TM, Schrader KK, Main KL (2008) Comparing denitrification rates and carbon sources in commercial scale upflow denitrification biological filters in aquaculture. Aquac Eng 38:79–92

    Article  Google Scholar 

  • Herrero M, Stuckey DC (2015) Bioaugmentation and its application in wastewater treatment: a review. Chemosphere 140:119–128

    Article  CAS  PubMed  Google Scholar 

  • Hou X, Liu S, Zhang Z (2015) Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge. Water Res 75:51–62

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Shi Y, Zeng G, Gu Y, Chen G, Shi L, Hu Y, Tang B, Zhou J (2016) Acyl-homoserine lactone-based quorum sensing and quorum quenching hold promise to determine the performance of biological wastewater treatments: an overview. Chemosphere 157:137–151

    Article  CAS  PubMed  Google Scholar 

  • Jiang B, Liu Y (2012) Roles of ATP-dependent N-acylhomoserine lactones (AHLs) and extracellular polymeric substances (EPSs) in aerobic granulation. Chemosphere 88:1058–1064

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Tay J, Maszenan AM, Tay ST-L (2006) Enhanced phenol biodegradation and aerobic granulation by two coaggregating bacterial strains. Environ Sci Technol 40:6137–6142

    Article  CAS  PubMed  Google Scholar 

  • Kariminik A, Baseri-Salehi M, Kheirkhah B (2017) Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol Lett 190:1–6

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Lee S, Hong S, Oh Y, Seoul M, Kweon J, Kim T (2009) Biofouling of reverse osmosis membranes: microbial quorum sensing and fouling propensity. Desalination 247:303–315

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kunacheva C, Stuckey DC (2014) Analytical methods for soluble microbial products (SMP) and extracellular polymers (ECP) in wastewater treatment systems: a review. Water Res 61:1–18

    Article  CAS  PubMed  Google Scholar 

  • Le Berre R, Nguyen S, Nowak E, Kipnis E, Pierre M, Ader F, Courcol R, Guery BP, Faure K (2008) Quorum-sensing activity and related virulence factor expression in clinically pathogenic isolates of Pseudomonas aeruginosa. Clin Microbiol Infect 14:337–343

    Article  PubMed  Google Scholar 

  • Lee DJ, Chen YY, Show KY, Whiteley CG, Tay JH (2010) Advances in aerobic granule formation and granule stability in the course of storage and reactor operation. Biotechnol Adv 28:919–934

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Lee S, Lee K, Nahm CH, Kwon H, Oh HS, Won YJ, Choo KH, Lee CH, Park PK (2016) More efficient media design for enhanced biofouling control in a membrane bioreactor: quorum quenching bacteria entrapping hollow cylinder. Environ Sci Technol 50:8596–8604

    Article  CAS  PubMed  Google Scholar 

  • Li AJ, Hou BL, Li MX (2015) Cell adhesion, ammonia removal and granulation of autotrophic nitrifying sludge facilitated by N-acyl-homoserine lactones. Bioresour Technol 196:550–558

  • Li AJ, Li XY (2009) Selective sludge discharge as the determining factor in SBR aerobic granulation: numerical modelling and experimental verification. Water Res 43:3387–3396

    Article  CAS  PubMed  Google Scholar 

  • Li AJ, Li XY, Yu HQ (2011) Effect of the food-to-microorganism (F/M) ratio on the formation and size of aerobic sludge granules. Process Biochem 46:2269–2276

    Article  CAS  Google Scholar 

  • Li Y, Zhu J (2014) Role of N-acyl homoserine lactone (AHL)-based quorum sensing (QS) in aerobic sludge granulation. Appl Microbiol Biotechnol 98:7623–7632

  • Li J, Ding LB, Cai A, Huang GX, Horn H (2014a) Aerobic sludge granulation in a full-scale sequencing batch reactor. Biomed Res Int 2014:1–12

    Google Scholar 

  • Li Y, Hao W, Lv J, Wang Y, Zhong C, Zhu J (2014b) The role of N-acyl homoserine lactones in maintaining the stability of aerobic granules. Bioresour Technol 159:305–310

  • Li Y, Lv J, Zhong C, Hao W, Wang Y, Zhu J (2014c) Performance and role of N-acyl-homoserine lactone (AHL)-based quorum sensing (QS) in aerobic granules. J Environ Sci 26:1615–1621

  • Li Y, Cao J, Li B, Li W, Fang F, Tong Z, Yu H (2016) Outcompeting presence of acyl-homoserine-lactone (AHL)-quenching bacteria over AHL-producing bacteria in aerobic granules. Environ Sci Tech Lett 3:36–40

    Article  CAS  Google Scholar 

  • Li YS, Pan XR, Cao JS, Song XN, Fang F, Tong ZH, Li WW, Yu HQ (2017) Augmentation of acyl homoserine lactones-producing and -quenching bacterium into activated sludge for its granulation. Water Res 125:309–317

    Article  CAS  PubMed  Google Scholar 

  • Liang XY, Gao BY, Ni SQ (2017) Effects of magnetic nanoparticles on aerobic granulation process. Bioresour Technol 227:44–49

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Nguyen D, Paice M (2010) Aerobic granule formation in a sequencing batch reactor treating newsprint effluent under low phosphate conditions. Water Sci Technol 62:2571–2578

    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. Wat Res 36:1653-1665

  • Liu X, Sun S, Ma B, Zhang C, Wan C, Lee DJ (2016) Understanding of aerobic granulation enhanced by starvation in the perspective of quorum sensing. Appl Microbiol Biotechnol 100:3747

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Tay JH (2004) State of the art of biogranulation technology for wastewater treatment. Biotechnol Adv 22:533–563

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Wang ZW, Qin L, Liu YQ, Tay JH (2005) Selection pressure-driven aerobic granulation in a sequencing batch reactor. Appl Microbiol Biotechnol 67:26–32

    Article  CAS  PubMed  Google Scholar 

  • Liu YQ, Tay JH (2008) Influence of starvation time on formation and stability of aerobic granules in sequencing batch reactors. Bioresour Technol 99:980–985

    Article  CAS  PubMed  Google Scholar 

  • Lu HF, Ji QX, Ding S, Zheng P (2013) The morphological and settling properties of ANAMMOX granular sludge in high-rate reactors. Bioresour Technol 143:592–597

    Article  CAS  PubMed  Google Scholar 

  • Lu HF, Zheng P, Ji QX, Zhang HT, Ji JY, Wang L, Ding S, Chen TT, Zhang JQ, Tang CJ, Chen JW (2012) The structure, density and settlability of anammox granular sludge in high-rate reactors. Bioresour Technol 123:312–317

    Article  CAS  PubMed  Google Scholar 

  • Luo JG, Wei L, Hao TW, Xue WQ, Mackey H, Chen GH (2015) Effect of L-tyrosine on aerobic sludge granulation and its stability. RSC Adv 5:86513–86521

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014b) The microbial attachment potential and quorum sensing measurement of aerobic granular activated sludge and flocculent activated sludge. Bioresour Technol 151:291–296

    Article  CAS  PubMed  Google Scholar 

  • Mangwani N, Kumari S, Das S (2015) Involvement of quorum sensing genes in biofilm development and degradation of polycyclic aromatic hydrocarbons by a marine bacterium Pseudomonas aeruginosa N6P6. Appl Microbiol Biotechnol 99:10283–10297

    Article  CAS  PubMed  Google Scholar 

  • McLean RJC, Whiteley M, Stickler DJ, Fuqua WC (1997) Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett 154:259–263

    Article  CAS  PubMed  Google Scholar 

  • McSwain BS, Irvine RL, Hausner M, Wilderer PA (2005) Composition and distribution of extracellular polymeric substances in aerobic flocs and granular sludge. Appl Environ Microbiol 71:1051–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McSwain BS, Irvine RL, Wilderer PA (2004) The influence of settling time on the formation of aerobic granules. Water Sci Technol 50:195–202

    CAS  PubMed  Google Scholar 

  • Mellbye BL, Bottomley PJ, Sayavedra-Soto LA (2015) Nitrite-oxidizing bacterium Nitrobacter winogradskyi produces N-acyl-homoserine lactone autoinducers. Appl Environ Microbiol 81:5917–5926

  • Mellbye BL, Davis EW, Spieck E, Chang JH, Bottomley PJ, Sayavedra-Soto LA (2017a) Draft genome sequence of Nitrobacter vulgaris strain Ab1, a nitrite-oxidizing bacterium. Genome A 5:1–2

    Google Scholar 

  • Mellbye BL, Giguere AT, Bottomley PJ, Sayavedra-Soto LA (2016) Quorum quenching of Nitrobacter winogradskyi suggests that quorum sensing regulates fluxes of nitrogen oxide(s) during nitrification. MBio 7:1–9

    Article  Google Scholar 

  • Mellbye BL, Spieck E, Bottomley PJ, Sayavedra-Soto LA (2017b) A survey of putative quorum sensing genes in nitrifying bacteria reveals acyl-homoserine lactone production in ammonia- and nitrite-oxidizing bacteria from the genera Nitrosospira, Nitrobacter, and Nitrospira. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01540-17

  • Moy BYP, Tay JH, Toh SK, Liu Y, Tay STL (2002) High organic loading influences the physical characteristics of aerobic sludge granules. Lett Appl Microbiol 34:407–412

  • Mulder A, van de Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–183

    Article  CAS  Google Scholar 

  • Mußmann M, Ribot M, von Schiller D, Merbt SN, Augspurger C, Karwautz C, Winkel M, Battin TJ, Martí E, Daims H (2013) Colonization of freshwater biofilms by nitrifying bacteria from activated sludge. FEMS Microbiol Ecol 85:104–115

    Article  PubMed  Google Scholar 

  • Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Norton JM, Klotz MG, Stein LY, Arp DJ, Bottomley PJ, Chain PSG, Hauser LJ, Land ML, Larimer FW, Shin MW, Starkenburg SR (2008) Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol 74:3559–3572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes-Alves C (2015) Do it yourself nitrification. Nat Rev Microbiol 14:61

    Article  PubMed  CAS  Google Scholar 

  • Okabe S, Kindaichi T, Ito T, Satoh H (2004) Analysis of size distribution and areal cell density of ammonia-oxidizing bacterial microcolonies in relation to substrate microprofiles in biofilms. Biotechnol Bioeng 85:86–95

    Article  CAS  PubMed  Google Scholar 

  • Oshiki M, Satoh H, Okabe S (2016) Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol 18:2784–2796

    Article  CAS  PubMed  Google Scholar 

  • Paliwal V, Puranik S, Purohit HJ (2012) Integrated perspective for effective bioremediation. Appl Biochem Biotechnol 166:903–924

    Article  CAS  PubMed  Google Scholar 

  • Papenfort K, Bassler BL (2016) Quorum sensing signal–response systems in gram-negative bacteria. Nat Rev Microbiol 14:576–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez J, Buchanan A, Mellbye B, Ferrell R, Chang JH, Chaplen F, Bottomley PJ, Arp DJ, Sayavedra-Soto LA (2015) Interactions of Nitrosomonas europaea and Nitrobacter winogradskyi grown in co-culture. Arch Microbiol 197:79–89

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ren T, Li X, Yu H (2013) Effect of N-acy-l-homoserine lactones-like molecules from aerobic granules on biofilm formation by Escherichia coli K12. Bioresour Technol 129:655–658

    Article  CAS  PubMed  Google Scholar 

  • Ren T, Yu H, Li X (2010) The quorum-sensing effect of aerobic granules on bacterial adhesion, biofilm formation, and sludge granulation. Appl Microbiol Biotechnol 88:789–797

    Article  CAS  PubMed  Google Scholar 

  • Ruan A, Min H, Peng X, Huang Z (2005) Isolation and characterization of Pseudomonas sp. strain HF-1, capable of degrading nicotine. Res Microbiol 156:700–706

    Article  CAS  PubMed  Google Scholar 

  • Santoro AE (2016) The do-it-all nitrifier. Science 351:342–343

    Article  CAS  PubMed  Google Scholar 

  • Sayavedra-Soto L, Ferrell R, Dobie M, Mellbye B, Chaplen F, Buchanan A, Chang J, Bottomley P, Arp D (2015) Nitrobacter winogradskyi transcriptomic response to low and high ammonium concentrations. FEMS Microbiol Lett 362:1–7

    Article  PubMed  Google Scholar 

  • Schuster M, Sexton DJ, Diggle SP, Greenberg EP (2013) Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 67:43–63

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Gao J, Liu J, Liu S, Liu Z, Wang Y, Guo B, Zhuang X, Zhuang G (2016) A new acyl-homoserine lactone molecule generated by Nitrobacter winogradskyi. Sci Rep 6:1–11

    Article  CAS  Google Scholar 

  • Sheng GP, Li AJ, Li XY, Yu HQ (2010) Effects of seed sludge properties and selective biomass discharge on aerobic sludge granulation. Chem Eng J 160:108–114

    Article  CAS  Google Scholar 

  • Shi YH, Huang JH, Zeng GM, Gu YL, Chen YN, Hu Y, Tang B, Zhou JX, Yang Y, Shi LX (2017) Exploiting extracellular polymeric substances (EPS) controlling strategies for performance enhancement of biological wastewater treatments: an overview. Chemosphere 180:396–411

    Article  CAS  PubMed  Google Scholar 

  • Shrout JD, Nerenberg R (2012) Monitoring bacterial twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ Sci Technol 46:1995–2005

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui MF, Sakinah M, Singh L, Zularisam AW (2012) Targeting N-acyl-homoserine-lactones to mitigate membrane biofouling based on quorum sensing using a biofouling reducer. J Biotechnol 161:190–197

  • Solano C, Echeverz M, Lasa I (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18:96–104

    Article  CAS  PubMed  Google Scholar 

  • Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101

    Article  CAS  PubMed  Google Scholar 

  • Starkenburg SR, Chain PSG, Sayavedra-Soto LA, Hauser L, Land ML, Larimer FW, Malfatti SA, Klotz MG, Bottomley PJ, Arp DJ, Hickey WJ (2006) Genome sequence of the chemolithoautotrophic nitrite-oxidizing bacterium Nitrobacter winogradskyi Nb-255. Appl Environ Microbiol 72:2050–2063

  • Straight PD, Kolter R (2009) Interspecies chemical communication in bacterial development. Annu Rev Microbiol 63:99–118

    Article  CAS  PubMed  Google Scholar 

  • Strous M, Fuerst JA, Kramer EH, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MS (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449

    Article  CAS  PubMed  Google Scholar 

  • Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50:589–596

    Article  CAS  Google Scholar 

  • Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes H-W, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794

    Article  PubMed  Google Scholar 

  • Sun S, Liu X, Ma B, Wan C, Lee DJ (2016) The role of autoinducer-2 in aerobic granulation using alternating feed loadings strategy. Bioresour Technol 201:58–64

    Article  CAS  PubMed  Google Scholar 

  • Tan CH, Koh KS, Xie C, Tay M, Zhou Y, Williams R, Ng WJ, Rice SA, Kjelleberg S (2014) The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules. ISME J 8:1186–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan TW, Ng HY (2008) Influence of mixed liquor recycle ratio and dissolved oxygen on performance of pre-denitrification submerged membrane bioreactors. Wat Res 42:1122–1132

    Article  CAS  Google Scholar 

  • Tang CJ, Duan CS, Yu C, Song YX, Chai LY, Xiao R, Wei Z, Min XB (2017) Removal of nitrogen from wastewaters by anaerobic ammonium oxidation (ANAMMOX) using granules in upflow reactors. Environ Chem Lett 15:311–328

    Article  CAS  Google Scholar 

  • Tang X, Liu S, Zhang Z, Zhuang G (2015) Identification of the release and effects of AHLs in anammox culture for bacteria communication. Chem Eng J 273:184–191

    Article  CAS  Google Scholar 

  • Teng Y, Luo Y, Sun M, Liu Z, Li Z, Christie P (2010) Effect of bioaugmentation by Paracoccus sp. strain HPD-2 on the soil microbial community and removal of polycyclic aromatic hydrocarbons from an aged contaminated soil. Bioresour Technol 101:3437–3443

    Article  CAS  PubMed  Google Scholar 

  • Tomaszewski M, Cema G, Ziembinska-Buczynska A (2017) Influence of temperature and pH on the anammox process: a review and meta-analysis. Chemosphere 182:203–214

    Article  CAS  PubMed  Google Scholar 

  • 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 189:4969–4972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valle A, Bailey MJ, Whiteley AS, Manefield M (2004) N-acyl-l-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol 6:424–433

  • van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1997) Metabolic pathway of anaerobic ammonium oxidation on the basis of 15N studies in a fluidized bed reactor. Microbiology 143:2415–2421

    Article  Google Scholar 

  • van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lücker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wagner J, Weissbrodt DG, Manguin V, da Costa RH, Morgenroth E, Derlon N (2015) Effect of particulate organic substrate on aerobic granulation and operating conditions of sequencing batch reactors. Water Res 85:158–166

    Article  CAS  PubMed  Google Scholar 

  • Wan C, Yang X, Lee DJ, Wang XY, Yang Q, Pan X (2014) Aerobic granulation of aggregating consortium X9 isolated from aerobic granules and role of cyclic di-GMP. Bioresour Technol 152:557–561

    Article  CAS  PubMed  Google Scholar 

  • Wan C, Zhang P, Lee D-J, Yang X, Liu X, Sun S, Pan X (2013) Disintegration of aerobic granules: role of second messenger cyclic di-GMP. Bioresour Technol 146:330–335

    Article  CAS  PubMed  Google Scholar 

  • Wang JH, He HZ, Wang MZ, Wang S, Zhang J, Wei W, Xu HX, Lv ZM, Shen DS (2013) Bioaugmentation of activated sludge with Acinetobacter sp. TW enhances nicotine degradation in a synthetic tobacco wastewater treatment system. Bioresour Technol 142:445–453

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Zheng X, Zhang K, Ding Y, He Z, Shen D, Feng H (2014a) A new method for rapid construction of a Pseudomonas sp. HF-1 bioaugmented system: accelerating acylated homoserine lactones secretion by pH regulation. Bioresour Technol 169:229–235

    Article  CAS  PubMed  Google Scholar 

  • Wang M, He H, Zheng X, Feng H, Lv Z, Shen D (2014b) Effect of Pseudomonas sp. HF-1 inoculum on construction of a bioaugmented system for tobacco wastewater treatment: analysis from quorum sensing. Environ Sci Pollut Res 21:7945–7955

    Article  CAS  Google Scholar 

  • Wang M, Yang G, Min H, Lv Z (2009a) A novel nicotine catabolic plasmid pMH1 in Pseudomonas sp. strain HF-1. Can J Microbiol 55:228–233

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Yang G, Min H, Lv Z, Jia X (2009b) Bioaugmentation with the nicotine-degrading bacterium Pseudomonas sp. HF-1 in a sequencing batch reactor treating tobacco wastewater: degradation study and analysis of its mechanisms. Water Res 43:4187–4196

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Zheng X, He H, Shen D, Feng H (2012) Ecological roles and release patterns of acylated homoserine lactones in Pseudomonas sp. HF-1 and their implications in bacterial bioaugmentation. Bioresour Technol 125:119–126

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Shi W, Tang T, Wang Y, Zhi L, Lv J, Li J (2017a) Function of quorum sensing and cell signaling in the formation of aerobic granular sludge. Rev Environ Sci Biotechnol 16:1–13

    Article  CAS  Google Scholar 

  • Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017b) Comammox in drinking water systems. Water Res 116:332–341

    Article  CAS  PubMed  Google Scholar 

  • Waters CM, Lu W, Rabinowitz JD, Bassler BL (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190:2527–2536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551:313–320

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Li A, Yang J, Ma F, Chen H, Pi S, Wei W (2015) N-3-Oxo-octanoyl-homoserine lactone as a promotor to improve the microbial flocculant production by an exopolysaccharide bioflocculant-producing bacterium Agrobacterium tumefaciens F2. RSC Adv 5:89531–89538

  • Wu L, Li A, Hou L, Li M (2017) Exogenous addition of cellular extract N-acyl-homoserine-lactones accelerated the granulation of autotrophic nitrifying sludge. Int Biodeterior Biodegrad 118:119–125

  • Xia S, Zhou L, Zhang Z, Li J (2012) Influence and mechanism of N-(3-oxooxtanoyl)-L-homoserine lactone (C8-oxo-HSL) on biofilm behaviors at early stage. J Environ Sci 24:2035–2040

  • Xiong Y, Liu Y (2010) Involvement of ATP and autoinducer-2 in aerobic granulation. Biotechnol Bioeng 105:51–58

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Liu Y (2012) Essential roles of eDNA and AI-2 in aerobic granulation in sequencing batch reactors operated at different settling times. Appl Microbiol Biotechnol 93:2645–2651

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Liu Y (2013) Importance of extracellular proteins in maintaining structural integrity of aerobic granules. Colloids Surf B 112:435–440

    Article  CAS  Google Scholar 

  • Yang J, Wu D, Li A, Guo H, Chen H, Pi S, Wei W, Ma F (2016) The addition of N-hexanoyl-homoserine lactone to improve the microbial flocculant production of Agrobacterium tumefaciens strain F2, an exopolysaccharide bioflocculant-producing bacterium. Appl Biochem Biotechnol 179:728–739

  • Yuan S, Gao M, Zhu F, Afzal M, Wang Y, Xu H, Wang M, Wang S, Wang X (2017) Disintegration of aerobic granules during prolonged operation. Environ Sci Water Res Technol 3:757–766

    Article  CAS  Google Scholar 

  • Zhang K, Zheng X, Shen DS, Wang MZ, Feng HJ, He HZ, Wang S, Wang JH (2015a) Evidence for existence of quorum sensing in a bioaugmented system by acylated homoserine lactone-dependent quorum quenching. Environ Sci Pollut Res 22:6050–6056

    Article  CAS  Google Scholar 

  • Zhang L, Liu M, Zhang S, Yang Y, Peng Y (2015b) Integrated fixed-biofilm activated sludge reactor as a powerful tool to enrich anammox biofilm and granular sludge. Chemosphere 140:114–118

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Yu X, Guo F, Wu Z (2011) Effect of interspecies quorum sensing on the formation of aerobic granular sludge. Water Sci Technol 64:1284–1290

    Article  CAS  PubMed  Google Scholar 

  • Zhang SH, Zhang XH, Lv L, Wang Q, Jiang QP (2013) Formation of aerobic granular sludge under adverse conditions: low DO and high ammonia. J Environ Biol 34:409–419

    CAS  PubMed  Google Scholar 

  • Zhang W, Li C (2015) Exploiting quorum sensing interfering strategies in gram-negative bacteria for the enhancement of environmental applications. Front Microbiol 6:1–15

    Google Scholar 

  • Zhao R, Zhang H, Zhang F, Yang F (2017) Fast start-up anammox process using acyl-homoserine lactones (AHLs) containing supernatant. J Environ Sci. https://doi.org/10.1016/j.jes.2017.03.025

  • Zhao R, Zhang H, Zou X, Yang F (2016) Effects of inhibiting acylated homoserine lactones (AHLs) on Anammox activity and stability of granules. Curr Microbiol 73:108–114

  • Zhu L, Zhou J, Lv M, Yu H, Zhao H, Xu X (2015) Specific component comparison of extracellular polymeric substances (EPS) in flocs and granular sludge using EEM and SDS-PAGE. Chemosphere 121:26–32

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Shen J, Ruan Y, Guo X, Ye Z, Deng Y, Shi M (2016) The effects of different seeding ratios on nitrification performance and biofilm formation in marine recirculating aquaculture system biofilter. Environ Sci Pollut Res 23:14540–14548

    Article  CAS  Google Scholar 

  • Zou J, Tao Y, Li J, Wu S, Ni Y (2017) Cultivating aerobic granular sludge in a developed continuous-flow reactor with two-zone sedimentation tank treating real and low-strength wastewater. Bioresour Technol 247:776–783

    Article  CAS  Google Scholar 

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Funding

This study was funded by National Natural Science Foundation of China (Nos. 51608154 and 51578179), Open Project of State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (No. HC201526-01), and Postdoctoral Scientific Research Development Fund of Heilongjiang Province in 2014 (No. LBH-Q14076).

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Correspondence to Ang Li.

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Chen, H., Li, A., Cui, D. et al. N-Acyl-homoserine lactones and autoinducer-2-mediated quorum sensing during wastewater treatment. Appl Microbiol Biotechnol 102, 1119–1130 (2018). https://doi.org/10.1007/s00253-017-8697-3

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  • DOI: https://doi.org/10.1007/s00253-017-8697-3

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