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Application of acyl-homoserine lactones for regulating biofilm characteristics on PAO1 and multi-strains in membrane bioreactor

  • Wonjung, Song (The Academy of Applied Science and Technology, Konkuk University) ;
  • Chehyeun, Kim (Department of Environmental Engineering, Konkuk University) ;
  • Jiwon, Han (Department of Environmental Engineering, Konkuk University) ;
  • Jihoon, Lee (Department of Environmental Engineering, Konkuk University) ;
  • Zikang, Jiang (Department of Environmental Engineering, Konkuk University) ;
  • Jihyang, Kweon (Department of Environmental Engineering, Konkuk University)
  • Received : 2022.11.07
  • Accepted : 2023.02.02
  • Published : 2023.01.25

Abstract

Biofilms significantly affect the performance of wastewater treatment processes in which biodegradability of numerous microorganisms are actively involved, and various technologies have been applied to secure microbial biofilms. Understanding changes in biofilm characteristics by regulating expression of signaling molecules is important to control and regulate biofilms in membrane bioreactor, i.e., biofouling. This study investigated effects of addition of acyl-homoserine lactones (AHL) as a controllable factor for the microbial signaling system on biofilm formation of Pseudomonas aeruginosa PAO1 and multiple strains in membrane bioreactor. The addition of three AHL, i.e., C4-, C6-, and C8-HSL, at a concentration of 200 ㎍/L, enhanced the formation of the PAO1 biofilm and the degree of increases in the biofilm formation of PAO1 were 70.2%, 76.6%, and 72.9%, respectively. The improvement of biofilm formation of individual strains by C4-HSL was an average of 68%, and the microbial consortia increased by approximately 52.1% in the presence of 200 ㎍/L C4-HSL. CLSM images showed that more bacterial cells were present on the membrane surface after the AHL application. In the COMSTAT results, biomass and thickness were increased up to 2.2 times (PAO1) and 1.6 times (multi-strains) by C4-HSL. This study clearly showed that biofilm formation was increased by the application of AHL to individual strain groups, including PAO1 and microbial consortia, and significant increases were observed when 50 or 100 ㎍/L AHL was administered. This suggests that AHL application can improve the biofilm formation of microorganisms, which could yield an enhancement in efficiency of biofilm control, such as in various biofilm reactors including membrane bioreactor and bioflocculent systems in water/wastewater treatment processes.

Keywords

Acknowledgement

This work was supported by a National Research Foundation of Korea(NRF) grant funded by the Korean Government (MICT). (No. NRF-2021R1A2C2014255)

References

  1. Al-Halbouni, D., Traber, J., Lyko, S., Wintgens, T., Melin, T., Tacke, D., Janot, A., Dott, W. and Hollender, J. (2008), "Correlation of EPS content in activated sludge at different sludge retention times with membrane fouling phenomena", Water Res., 42(6-7), 1475-1488. https://doi.org/10.1016/j.watres.2007.10.026
  2. An, D. and Parsek, M.R. (2007), "The promise and peril of transcriptional profiling in biofilm communities", Curr. Opinion Microbiol., 10(3), 292-296. https://doi.org/10.1016/j.mib.2007.05.011
  3. Bengtsson, S., de Blois, M., Wilen, B.M. and Gustavsson, D. (2019). A comparison of aerobic granular sludge with conventional and compact biological treatment technologies. Environ. Technol., 40(21), 2769-2778. https://doi.org/10.1080/09593330.2018.1452985
  4. Burmolle, M., Webb, J.S., Rao, D., Hansen, L.H., Sorensen, S.J. and Kjelleberg, S. (2006), "Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms", Appl. Environ. Microbiol., 72(6), 3916-3923. https://doi.org/10.1128/AEM.03022-05
  5. Chattopadhyay, I., Usman, T.M. and Varjani, S. (2022), "Exploring the role of microbial biofilm for industrial effluents treatment", Bioengineered, 13(3), 6420-6440. https://doi.org/10.1080/21655979.2022.2044250
  6. Costa, O.Y., Raaijmakers, J.M. and Kuramae, E.E. (2018), "Microbial extracellular polymeric substances: ecological function and impact on soil aggregation", Front. Microbiol., 9, 1636. https://doi.org/10.3389/fmicb.2018.01636
  7. Dobretsov, S., Teplitski, M. and Paul, V. (2009), "Mini-review: quorum sensing in the marine environment and its relationship to biofouling", Biofouling, 25(5), 413-427. https://doi.org/10.1080/08927010902853516
  8. Frolund, B., Palmgren, R., Keiding, K. and Nielsen, P.H. (1996), "Extraction of extracellular polymers from activated sludge using a cation exchange resin", Water Res., 30(8), 1749-1758. https://doi.org/10.1016/0043-1354(95)00323-1
  9. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersboll, B.K. and Molin, S. (2000), "Quantification of biofilm structures by the novel computer program COMSTAT", Microbiology, 146(10), 2395-2407. https://doi.org/10.1099/00221287-146-10-2395
  10. Iorhemen, O.T., Hamza, R.A. and Tay, J.H. (2017). Membrane fouling control in membrane bioreactors (MBRs) using granular materials. Bioresour. Technol., 240, 9-24. https://doi.org/10.1016/j.biortech.2017.03.005
  11. Karygianni, L., Ren, Z., Koo, H. and Thurnheer, T. (2020), "Biofilm matrixome: extracellular components in structured microbial communities", Trends Microbiol., 28(8), 668-681. https://doi.org/10.1016/j.tim.2020.03.016
  12. Kim, S.R., Oh, H.S., Jo, S.J., Yeon, K.M., Lee, C.H., Lim, D.J., Lee, C.H. and Lee, J.K. (2013), "Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: Physical and biological effects", Environ. Sci. Technol., 47(2), 836-842. https://doi.org/10.1021/es303995s
  13. Lade, H., Paul, D. and Kweon, J.H. (2014), "Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge", Int. J. Mol. Sci., 15(2), 2255-2273. https://doi.org/10.3390/ijms15022255
  14. Lade, H., Paul, D. and Kweon, J.H. (2014), "Quorum quenching mediated approaches for control of membrane biofouling", Int. J. Biol. Sci., 10(5), 550. https://doi.org/10.7150/ijbs.9028.
  15. Lade, H., Song, W.J., Yu, Y.J., Ryu, J.H., Arthanareeswaran, G. and Kweon, J.H. (2017), "Exploring the potential of curcumin  for control of N-acyl homoserine lactone-mediated biofouling in membrane bioreactors for wastewater treatment", RSC Adv., 7(27), 16392-16400. https://doi.org/10.1039/C6RA28032C
  16. Laspidou, C.S. and Rittmann, B.E. (2002), "A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass", Water Res., 36(11), 2711-2720. https://doi.org/10.1016/S0043-1354(01)00413-4
  17. Li, Y.Y., Huang, X.W. and Li, X.Y. (2021), "Use of a packed-bed biofilm reactor to achieve rapid formation of anammox biofilms for high-rate nitrogen removal", J. Clean. Prod., 321, 128999. https://doi.org/10.1016/j.jclepro.2021.128999
  18. Lynch, M.J., Swift, S., Kirke, D.F., Keevil, C.W., Dodd, C.E. and Williams, P. (2002), "The regulation of biofilm development by quorum sensing in Aeromonas hydrophila", Environ. Microbiol., 4(1), 18-28. https://doi.org/10.1046/j.1462-2920.2002.00264.x
  19. Mangwani, N., Kumari, S. and Das, S. (2016), "Effect of synthetic N-acylhomoserine lactones on cell-cell interactions in marine Pseudomonas and biofilm mediated degradation of polycyclic aromatic hydrocarbons", Chem. Eng. J., 302, 172-186. https://doi.org/10.1016/j.cej.2016.05.042
  20. Morohoshi, T., Shiono, T., Takidouchi, K., Kato, M., Kato, N., Kato, J. and Ikeda, T. (2007), "Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone", Appl. Environ. Microbiol., 73(20), 6339-6344. https://doi.org/10.1128/AEM.00593-07
  21. Muhammad, M. H., Idris, A.L., Fan, X., Guo, Y., Yu, Y., Jin, X., Qiu, J., Guan, X. and Huang, T. (2020), "Beyond risk: bacterial biofilms and their regulating approaches", Front. Microbiol., 11, 928. https://doi.org/10.3389/fmicb.2020.00928
  22. Muras, A., Mayer, C., Otero-Casal, P., Exterkate, R.A., Brandt, B.W., Crielaard, W., Otero, A. and Krom, B.P. (2020), "Short-Chain N-acylhomoserine lactone quorum-sensing molecules promote periodontal pathogens in in vitro oral biofilms", Appl. Environ. Microbiol., 86(3), e01941-19. https://doi.org/10.1128/AEM.01941-19
  23. Murga, R., Stewart, P.S. and Daly, D. (1995), "Quantitative analysis of biofilm thickness variability", Biotechnol. Bioeng., 45(6), 503-510. https://doi.org/10.1002/bit.260450607
  24. O'Toole, G.A. (2011), "Microtiter dish biofilm formation assay", JoVE J. Visual. Experim., 47, e2437. https://doi.org/10.3791/2437
  25. Papenfort, K and Bassler, B.L. (2016), "Quorum sensing signal-response systems in Gram-negative bacteria", Nature Rev. Microbiol., 14(9), 576. https://doi.org/10.1038%2Fnrmicro.2016.89 https://doi.org/10.1038%2Fnrmicro.2016.89
  26. Reichhardt, C. and Parsek, M.R. (2019), "Confocal laser scanning microscopy for analysis of Pseudomonas aeruginosa biofilm architecture and matrix localization", Front. Microbiol., 10, 677. https://doi.org/10.3389/fmicb.2019.00677
  27. Percival, S.L., Mayer, D. and Salisbury, A.M. (2017), "Efficacy of a surfactant-based wound dressing on biofilm control", Wound Repair Regenerat., 25(5), 767-773. https://doi.org/10.1111/wrr.12581
  28. Ryu, J., Jung, J., Park, K., Song, W., Choi, B. and Kweon, J., (2021) "Humic acid removal and microbial community function in membrane bioreactor", J. Hazard. Mater., 417, 126088. https://doi.org/10.1016/j.jhazmat.2021.126088.
  29. Sehar, S. and Naz, I. (2016), "Role of the biofilms in wastewater treatment", Microbial Biofilms-importance Applicat., 121-144. http://doi.org/10.5772/63499
  30. Shi, S., Zhang, Y., Tang, Q. and Mo, J. (2021), "Modeling of biofilm growth and the related changes in hydraulic properties of porous media", Membr. Water Treat., 12(5), 217-225. https://doi.org/10.12989/MWT.2021.12.5.217
  31. Song, W., Lade, H., Yu, Y. and Kweon, J. (2018), "Effects of N-acetylcysteine on biofilm formation by MBR sludge", Membr. Water Treat., 9(3), 195-203. https://doi.org/10.12989/mwt.2018.9.3.195
  32. Stewart, C.R., Muthye, V. and Cianciotto, N.P. (2012), "Legionella pneumophila persists within biofilms formed by Klebsiella pneumoniae, Flavobacterium sp., and Pseudomonas fluorescens under dynamic flow conditions", PloS one, 7(11), e50560. https://doi.org/10.1371/journal.pone.0050560
  33. Tan, C.H., Koh, K.S., Xie, C., Tay, M., Zhou, Y., Williams, R., Ng, W.J., Rice, S.A. and Kjelleberg, S. (2014), "The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules", The ISME J, 8(6), 1186-1197. https://doi.org/10.1038/ismej.2013.240
  34. Wang, Y., Zhong, C., Huang, D., Wang, Y. and Zhu, J. (2013), "The membrane fouling characteristics of MBRs with different aerobic granular sludges at high flux", Bioresour. Technol., 136, 488-495. https://doi.org/10.1016/j.biortech.2013.03.066
  35. Waters, C.M. and Bassler, B.L. (2005), "Quorum sensing: Cell-to-cell communication in bacteria", Annual Rev. Cell Develop. Biol., 21, 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  36. Wilen, B.M., Liebana, R., Persson, F., Modin, O. and Hermansson, M. (2018), "The mechanisms of granulation of activated sludge in wastewater treatment, its optimization, and impact on effluent quality", Appl. Microbiol. Biotechnol., 102(12), 5005-5020. https://doi.org/10.1007/s00253-018-8990-9
  37. Yang, X., Beyenal, H., Harkin, G and Lewandowski, Z. (2000), "Quantifying biofilm structure using image analysis", J. Microbiol. Method, 39(2), 109-119. https://doi.org/10.1016/S0167-7012(99)00097-4
  38. Yeon, K.M., Cheong, W.S., Oh, H.S., Lee, W.N., Hwang, B.K., Lee, C.H., Beyenal, H. and 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. https://doi.org/10.1021/es8019275
  39. Zhang, W., Liang, W., Zhang, Z. and Hao, T. (2021), "Aerobic granular sludge (AGS) scouring to mitigate membrane fouling: Performance, hydrodynamic mechanism and contribution quantification model", Water Res., 188, 116518. https://doi.org/10.1016/j.watres.2020.116518
  40. Zhu, Y.L., Hou, H.M., Zhang, G.L., Wang, Y.F. and Hao, H.S. (2019), "AHLs regulate biofilm formation and swimming motility of Hafnia alvei H4", Front. Microbiol., 10, 1330. https://doi.org/10.3389/fmicb.2019.01330