Skip to main content
Log in

Evidence for existence of quorum sensing in a bioaugmented system by acylated homoserine lactone-dependent quorum quenching

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The introduction of a gene, strain, or microbial consortium into an indigenous bacterial population is known as bioaugmentation. This technique has been proposed as an effective strategy for accelerating and enhancing the removal of recalcitrant and toxic compounds during wastewater treatment. In this study, three types of reactors were used to test whether quorum sensing plays an important role in bioaugmented systems. Reverse transcriptase polymerase chain reaction showed that the inoculated strain, HF-1, successfully colonized in the bioaugmented reactor. Meanwhile, no HF-1 colonization was observed in the quorum-quenching and non-bioaugmented reactors. Removal of nicotine in the bioaugmented reactor was almost 100 %, and removal of total organic carbon (TOC) was higher than 50 %. However, less than 20 % of nicotine and 30 % of TOC was removed in quorum-quenching and non-bioaugmented reactors. Moreover, the release of acylated homoserine lactones reached the threshold for HF-1 biofilm formation in bioaugmented reactors but not in quorum-quenching or non-bioaugmented reactors. The addition of porcine kidney acylase I, a quenching reagent, to the quorum-quenching reactor hampered the colonization of HF-1. Together, these results demonstrate that quorum sensing plays an important role in HF-1 colonization of bioaugmented systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

TOC:

Total organic carbon

QS:

Quorum sensing

AHLs:

Acylated homoserine lactones

ISM:

Inorganic salt medium

Non-BA:

Non-bioaugmented

BA:

Bioaugmented

QQ:

Quorum quenching

RT-PCR:

Reverse transcriptase polymerase chain reaction

RT-qPCR:

Reverse transcriptase quantitative polymerase chain reaction

EPS:

Extracellular polymeric substances

3-oxo-C6-HSL:

N-3-oxo-hexanoyl-homoserine lactone

C6-HSL:

N-hexanoyl-homoserine lactone

3-oxo-C8-HSL:

N-3-oxo-octanoyl-homoserine lactone

C8-HSL:

N-octanoyl-homoserine lactone

References

  • Bouchez T, Patureau D, Dabert P, Juretschko S, Doré J, Delgenès P, Moletta R, Wagner M (2000) Ecological study of a bioaugmentation failure. Environ Microbiol 2(2):179–190. doi:10.1046/j.1462-2920.2000.00091.x

    Article  CAS  Google Scholar 

  • Darch SE, West SA, Winzer K, Diggle SP (2012) Density-dependent fitness benefits in quorum-sensing bacterial populations. PNAS 109(21):8259–8263. doi:10.1073/pnas.1118131109

    Article  CAS  Google Scholar 

  • Geske GD, O’Neill JC, Blackwell HE (2008) Expanding dialogues: from natural autoinducers to non-natural analogues that modulate quorum sensing in Gram-negative bacteria. Chem Soc Rev 37(7):1432–1447

    Article  CAS  Google Scholar 

  • Gupta P, Chhibber S, Harjai K (2014) Efficacy of purified lactonase and ciprofloxacin in preventing systemic spread of Pseudomonas aeruginosa in murine burn wound model. Burns. doi:10.1016/j.burns.2014.06.009

    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(9):1058–1064. doi:10.1016/j.chemosphere.2012.04.059

    Article  CAS  Google Scholar 

  • Kim SR, Oh HS, Jo SJ, Yeon KM, Lee CH, Lim DJ, Lee CH, Lee JK (2013) Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: physical and biological effects. Environ Sci Technol 47(2):836–842. doi:10.1021/es303995s

    Article  CAS  Google Scholar 

  • Martín-Hernández M, Suárez-Ojeda ME, Carrera J (2012) Bioaugmentation for treating transient or continuous p-nitrophenol shock loads in an aerobic sequencing batch reactor. Bioresour Technol 123:150–156. doi:10.1016/j.biortech.2012.07.014

    Article  Google Scholar 

  • Paliwal V, Puranik S, Purohit HJ (2012) Integrated perspective for effective bioremediation. Appl Biochem Biotechnol 166(4):903–924. doi:10.1007/s12010-011-9479-5

    Article  CAS  Google Scholar 

  • Ren TT, Li XY, Yu HQ (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. doi:10.1016/j.biortech.2012.12.043

    Article  CAS  Google Scholar 

  • Song XN, Cheng YY, Li WW, Li BB, Sheng GP, Fang CY, Wang YK, Li XY, Yu HQ (2014) Quorum quenching is responsible for the underestimated quorum sensing effects in biological wastewater treatment reactors. Bioresour Technol 171:472–476. doi:10.1016/j.biortech.2014.08.027

    Article  CAS  Google Scholar 

  • Tang HZ, Wang SN, Ma LY, Meng XZ, Deng ZX, Zhang DK, Ma CQ, Xu P (2008) A novel gene, encoding 6-hydroxy-3-succinoylpyridine hydroxylase, involved in nicotine degradation by Pseudomonas putida strain S16. Appl Environ Microbiol 74(5):1567–1574. doi:10.1128/AEM. 02529-07

    Article  CAS  Google Scholar 

  • Wang MZ, Yang GQ, Min H, Lv ZM (2009a) A novel nicotine catabolic plasmid pMH1 in Pseudomonas sp. strain HF-1. Can J Microbiol 55(3):228–233. doi:10.1139/w08-135

    Article  CAS  Google Scholar 

  • Wang MZ, Yang GQ, Min H, Lv ZM, Jia XY (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(17):4187–4196. doi:10.1016/j.watres.2009.07.012

    Article  CAS  Google Scholar 

  • Wang MZ, Zheng X, He HZ, Shen DS, Feng HJ (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. doi:10.1016/j.biortech.2012.08.116

    Article  CAS  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. doi:10.1016/j.biortech.2013.05.067

    Article  CAS  Google Scholar 

  • Wang MZ, He HZ, Zheng X, Feng HJ, Lv ZM, Shen DS (2014a) 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. doi:10.1007/s11356-014-2760-8

    Article  CAS  Google Scholar 

  • Wang MZ, Zheng X, Zhang K, Ding YC, He HZ, Shen DS, Feng HJ (2014b) 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. doi:10.1016/j.biortech.2014.06.098

    Article  CAS  Google Scholar 

  • Xu F, Byun T, Dussen HJ, Duke KR (2003) Degradation of N-acylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. J Biotechnol 101(1):89–96. doi:10.1016/S0168-1656(02)00305-X

    Article  CAS  Google Scholar 

  • Yao YL, Lv ZM, Zhu FX, Min H, Bian CM (2013) Successful bioaugmentation of an activated sludge reactor with Rhodococcus sp. YYL for efficient tetrahydrofuran degradation. J Hazard Mater 261:550–558. doi:10.1016/j.jhazmat.2013.08.007

    Article  CAS  Google Scholar 

  • Yeon KM, Cheong WS, Oh HS, Lee WN, Hwang BK, Lee CH, Beyenal H, Lewandowski Z (2009) Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43(2):380–385. doi:10.1021/es8019275

    Article  CAS  Google Scholar 

  • Yong YC, Zhong JJ (2013) Regulation of aromatics biodegradation by rhl quorum sensing system through induction of catechol meta-cleavage pathway. Bioresour Technol 136:761–765. doi:10.1016/j.biortech.2013.03.134

    Article  CAS  Google Scholar 

  • Zhang J, Wen DH, Zhao C, Tang XY (2013) Bioaugmentation accelerates the shift of bacterial community structure against shock load: a case study of coking wastewater treatment by zeolite-sequencing batch reactor. Appl Microbiol Biotechnol 98(2):863–873. doi:10.1007/s00253-013-4848-3

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation of China (21107095), the public technology research plan of Zhejiang province (2014C33028), the Special Foundation of Young Scientists of Zhejiang Gongshang University (QZ11-7), and the Natural Science Foundation of Zhejiang Province (Y5110019).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mei-zhen Wang.

Additional information

Responsible editor: Gerald Thouand

Kun Zhang and Xin Zheng contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, K., Zheng, X., Shen, Ds. et al. Evidence for existence of quorum sensing in a bioaugmented system by acylated homoserine lactone-dependent quorum quenching. Environ Sci Pollut Res 22, 6050–6056 (2015). https://doi.org/10.1007/s11356-014-3795-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3795-6

Keywords

Navigation