Skip to main content
SpringerLink
Log in

Effects of Quorum Quenching on Biofilm Metacommunity in a Membrane Bioreactor

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Quorum quenching (QQ) has received attention for the control of biofilms, e.g., biofilms that cause biofouling in membrane bioreactors (MBRs). Despite the efficacy of QQ on biofouling, it is elusive how QQ influences biofilm formation on membranes. A pilot-scale QQ-MBR and non-QQ-MBR were identically operated for 4 days and 8 days to destructively sample the membranes. QQ prolonged the membrane filterability by 43% with no harmful influence on MBR performance. qPCR showed no effect of QQ on microbial density during either of these time periods. Community comparisons revealed that QQ influenced the bacterial and fungal community structures, and the fungal structure corresponded with the bacterial structure. Metacommunity and spatial analyses showed that QQ induced structural variation rather than compositional variation of bacteria and fungi. Moreover, QQ considerably enhanced the bacterial dispersal across membrane during the early development. As the dispersal enhancement by QQ counteracted the ecological drift, it eliminated the distance–decay relationship, reflecting a neutral theory archetype of metacommunity. Network analyses showed that QQ substantially reduced the amount and magnitude of interactions, e.g., competition and cooperation, for bacteria and fungi, and weakened their network structures, irrespective of time. Additionally, QQ suppressed the growth of specific microbial species (e.g., Acinetobacter), abundant and widespread at the early stage. These findings suggest that QQ influenced the community dynamics at the regional and local levels, correspondingly the ecological selection and dispersal processes, during the biofilm development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Drews A (2010) Membrane fouling in membrane bioreactors—characterisation, contradictions, cause and cures. J Membr Sci 363:1–28. https://doi.org/10.1016/j.memsci.2010.06.046

    Article  CAS  Google Scholar 

  2. Visvanathan C, Aim RB, Parameshwaran K (2000) Membrane separation bioreactors for wastewater treatment. Crit Rev Environ Sci Technol 30:1–48. https://doi.org/10.1080/10643380091184165

    Article  CAS  Google Scholar 

  3. Miura Y, Watanabe Y, Okabe S (2007) Membrane biofouling in pilot-scale membrane bioreactors (MBRs) treating municipal wastewater: impact of biofilm formation. Environ Sci Technol 41:632–638. https://doi.org/10.1021/es0615371

    Article  CAS  PubMed  Google Scholar 

  4. Lee S, Park S-K, Kwon H, Lee SH, Lee K, Nahm CH, Jo SJ, Oh H-S, Park P-K, Choo K-H, Lee C-H, Yi T (2016) Crossing the border between laboratory and field: bacterial quorum quenching for anti-biofouling strategy in an MBR. Environ Sci Technol 50:1788–1795. https://doi.org/10.1021/acs.est.5b04795

    Article  CAS  PubMed  Google Scholar 

  5. Jo SJ, Kwon H, Jeong S-Y, Lee C-H, Kim TG (2016) Comparison of microbial communities of activated sludge and membrane biofilm in 10 full-scale membrane bioreactors. Water Res 101:214–225. https://doi.org/10.1016/j.watres.2016.05.042

    Article  CAS  PubMed  Google Scholar 

  6. Malaeb L, Le-Clech P, Vrouwenvelder JS, Ayoub GM, Saikaly PE (2013) Do biological-based strategies hold promise to biofouling control in MBRs? Water Res 47:5447–5463. https://doi.org/10.1016/j.watres.2013.06.033

    Article  CAS  PubMed  Google Scholar 

  7. Yeon K-M, Cheong W-S, Oh H-S, Lee W-N, Hwang B-K, Lee C-H, Beyenal H, Lewandowski Z (2009) Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43:380–385. https://doi.org/10.1021/es8019275

    Article  CAS  PubMed  Google Scholar 

  8. Oh H-S, Yeon K-M, Yang C-S, Kim S-R, Lee C-H, Park SY, Han JY, Lee J-K (2012) Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ Sci Technol 46:4877–4884. https://doi.org/10.1021/es204312u

    Article  CAS  PubMed  Google Scholar 

  9. Jeong S-Y, Yi T, Lee C-H, Kim TG (2016) Spatiotemporal dynamics and correlation networks of bacterial and fungal communities in a membrane bioreactor. Water Res 105:218–230. https://doi.org/10.1016/j.watres.2016.09.001

    Article  CAS  PubMed  Google Scholar 

  10. Luo J, Lv P, Zhang J, Fane AG, McDougald D, Rice SA (2017) Succession of biofilm communities responsible for biofouling of membrane bio-reactors (MBRs). PLoS One 12:e0179855. https://doi.org/10.1371/journal.pone.0179855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206

    Article  Google Scholar 

  12. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x

    Article  Google Scholar 

  13. Leibold MA, Chase JM (2018) Metacommunity ecology. Princeton University Press

  14. Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551:313–320. https://doi.org/10.1038/nature24624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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. https://doi.org/10.1038/ismej.2013.240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR (2018) Bacterial quorum sensing and microbial community interactions. mBio 9:e02331–e02317. https://doi.org/10.1128/mBio.02331-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kim TG, Yi T, Lee E-H, Ryu HW, Cho K-S (2012) Characterization of a methane-oxidizing biofilm using microarray, and confocal microscopy with image and geostatic analyses. Appl Microbiol Biotechnol 95:1051–1059. https://doi.org/10.1007/s00253-011-3728-y

    Article  CAS  PubMed  Google Scholar 

  18. Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:1–11. https://doi.org/10.1890/ES10-00117.1

    Article  Google Scholar 

  19. Jin Y-L, Lee W-N, Lee C-H, Chang I-S, Huang X, Swaminathan T (2006) Effect of DO concentration on biofilm structure and membrane filterability in submerged membrane bioreactor. Water Res 40:2829–2836. https://doi.org/10.1016/j.watres.2006.05.040

    Article  CAS  PubMed  Google Scholar 

  20. Andersson S, Kuttuva Rajarao G, Land CJ, Dalhammar G (2008) Biofilm formation and interactions of bacterial strains found in wastewater treatment systems. FEMS Microbiol Lett 283:83–90. https://doi.org/10.1111/j.1574-6968.2008.01149.x

    Article  CAS  PubMed  Google Scholar 

  21. Clemmer KM, Bonomo RA, Rather PN (2011) Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology 157:2534–2544. https://doi.org/10.1099/mic.0.049791-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky OA, Mieszkin S, Millet LJ, Vajna B, Junier P, Bonfante P, Krom BP, Olsson S, van Elsas JD, Wick LY (2018) Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev 42:335–352. https://doi.org/10.1093/femsre/fuy008

    Article  CAS  PubMed  Google Scholar 

  23. Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221. https://doi.org/10.2307/3544021

    Article  Google Scholar 

  24. Hanski I, Gyllenberg M (1993) Two general metapopulation models and the core-satellite species hypothesis. Am Nat 142:17–41

    Article  Google Scholar 

  25. Freckleton RP, Gill JA, Noble D, Watkinson AR (2005) Large-scale population dynamics, abundance–occupancy relationships and the scaling from local to regional population size. J Anim Ecol 74:353–364. https://doi.org/10.1111/j.1365-2656.2005.00931.x

    Article  Google Scholar 

  26. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. https://doi.org/10.1038/nrmicro2795

    Article  CAS  Google Scholar 

  27. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. https://doi.org/10.1038/nrmicro2832

    Article  CAS  PubMed  Google Scholar 

  28. Fukami T, Morin PJ (2003) Productivity–biodiversity relationships depend on the history of community assembly. Nature 424:423–426. https://doi.org/10.1038/nature01785

    Article  CAS  PubMed  Google Scholar 

  29. Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356. https://doi.org/10.1128/mmbr.00051-12

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kim TG, Jeong S-Y, Cho K-S (2014) Functional rigidity of a methane biofilter during the temporal microbial succession. Appl Microbiol Biotechnol 98:3275–3286. https://doi.org/10.1007/s00253-013-5371-2

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the basic science research program through the National Research Foundation of Korea funded by the Ministry of Education (2018R1D1A1B07048872).

Author information

Authors and Affiliations

  1. Department of Microbiology, Pusan National University, Pusan, 46241, Republic of Korea

    So-Yeon Jeong & Tae Gwan Kim

  2. School of Chemical and Biological Engineering, Seoul National University, Seoul, 08826, Republic of Korea

    Chung-Hak Lee

  3. National Institute of Ecology, Seocheon, Choongnam, 33657, Republic of Korea

    Taewoo Yi

Authors
  1. So-Yeon Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chung-Hak Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taewoo Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tae Gwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Taewoo Yi or Tae Gwan Kim.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 398 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, SY., Lee, CH., Yi, T. et al. Effects of Quorum Quenching on Biofilm Metacommunity in a Membrane Bioreactor. Microb Ecol 79, 84–97 (2020). https://doi.org/10.1007/s00248-019-01397-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01397-5

Keywords

Search

Navigation