Skip to main content

Advertisement

Log in

Biofouling in Membrane Bioreactors—Mitigation and Current Status: a Review

  • Review Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Biological fouling as termed biofouling is caused by varied living organisms and is difficult to eliminate from the environment thus becoming a major issue during membrane bioreactors. Biofouling in membrane bioreactors (MBRs) is a crucial problem in increasing liquid pressure due to reduced pore diameter, clogging of the membrane pores, and alteration of the chemical composition of the water which greatly limits the growth of MBRs. Thus, membrane biofouling and/or microbial biofilms is a hot research topic to improve the market competitiveness of the MBR technology. Though several antibiofouling strategies (addition of bioflocculant or sponge into MBRs) came to light, biological approaches are sustainable and more practicable. Among the biological approaches, quorum sensing-based biofouling control (so-called quorum quenching) is an interesting and promising tool in combating biofouling issues in the MBRs. Several review articles have been published in the area of membrane biofouling and mitigation approaches. However, there is no single source of information about biofouling and/or biofilm formation in different environmental settings and respective problems, antibiofilm strategies and current status, quorum quenching, and its futurity. Thus, the objectives of the present review were to provide latest insights on mechanism of membrane biofouling, quorum sensing molecules, biofilm-associated problems in different environmental setting and antibiofilm strategies, special emphasis on quorum quenching, and its futurity in the biofilm/biofouling control. We believe that these insights greatly help in the better understanding of biofouling and aid in the development of sustainable antibiofouling strategies.

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
Fig. 4

Similar content being viewed by others

Data Availability

NA.

References

  1. Aslam, M., Ahmad, R., & Kim, J. (2018). Recent developments in biofouling control in membrane bioreactors for domestic wastewater treatment. Separation and Purification Technology, 206, 297–315.

    Article  CAS  Google Scholar 

  2. Bachosz, K., Vu, M. T., Nghiem, L. D., Zdarta, J., Nguyen, L. N. and Jesionowski, T. (2021). Enzyme-based control of membrane biofouling for water and wastewater purification: A comprehensive review. Environmental Technology & Innovation, 102106.

  3. Baker, J., & Dudley, L. (1998). Biofouling in membrane systems—a review. Desalination, 118, 81–89.

    Article  CAS  Google Scholar 

  4. Ban, H., Chai, X., Lin, Y., Zhou, Y., Peng, D., Zhou, Y., Zou, Y., Yu, Z., & Sun, M. (2009). Transgenic Amorphophallus konjac expressing synthesized acyl-homoserine lactonase (aiiA) gene exhibit enhanced resistance to soft rot disease. Plant Cell Reports, 28, 1847–1855.

    Article  CAS  PubMed  Google Scholar 

  5. Bao, X., Wu, Q., Shi, W., Wang, W., Yu, H., Zhu, Z., Zhang, X., Zhang, Z., Zhang, R., & Cui, F. (2019). Polyamidoamine dendrimer grafted forward osmosis membrane with superior ammonia selectivity and robust antifouling capacity for domestic wastewater concentration. Water Research, 153, 1–10.

    Article  CAS  PubMed  Google Scholar 

  6. Bhoj, Y., Tharmavaram, M., & Rawtani, D. (2021). A comprehensive approach to antifouling strategies in desalination, marine environment, and wastewater treatment. Chemical Physics Impact, 2, 100008.

    Article  Google Scholar 

  7. Bjarnsholt, T., Ciofu, O., Molin, S., Givskov, M., & Høiby, N. (2013). Applying insights from biofilm biology to drug development—can a new approach be developed? Nature Reviews Drug Discovery, 12, 791–808.

    Article  CAS  PubMed  Google Scholar 

  8. Bott, T. R. (2011). Chapter 7—Biofilms in Industry. In T. R. Bott (Ed.), Industrial biofouling (pp. 181–201). Elsevier.

  9. Bremere, I., Kennedy, M., Michel, P., van Emmerik, R., Witkamp, G.-J., & Schippers, J. (1999). Controlling scaling in membrane filtration systems using a desupersaturation unit. Desalination, 124, 51–62.

    Article  CAS  Google Scholar 

  10. Brooks, J. D., & Flint, S. H. (2008). Biofilms in the food industry: Problems and potential solutions. International Journal of Food Science & Technology, 43, 2163–2176.

    Article  CAS  Google Scholar 

  11. Byun, K.-H., Na, K. W., Ashrafudoulla, M., Choi, M. W., Han, S. H., Kang, I., Park, S. H., & Ha, S.-D. (2022). Combination treatment of peroxyacetic acid or lactic acid with UV-C to control Salmonella Enteritidis biofilms on food contact surface and chicken skin. Food Microbiology, 102, 103906.

    Article  CAS  PubMed  Google Scholar 

  12. Chan, K.-G., Atkinson, S., Mathee, K., Sam, C.-K., Chhabra, S. R., Cámara, M., Koh, C.-L., & 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 Microbiology, 11, 51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Characklis, W. G. (1981). Bioengineering report: Fouling biofilm development: A process analysis. Biotechnology and Bioengineering, 23, 1923–1960.

    Article  CAS  Google Scholar 

  14. Chen, H., & Fink, G. R. (2006). Feedback control of morphogenesis in fungi by aromatic alcohols. Genes & Development, 20, 1150–1161.

    Article  CAS  Google Scholar 

  15. Chen, Y., Sheng, Q., Wei, J., Wen, Q., Ma, D., Li, J., Xie, Y., Shen, J., & Sun, X. (2022). Novel strategy for membrane biofouling control in MBR with nano-MnO2 modified PVDF membrane by in-situ ozonation. Science of the Total Environment, 808, 151996.

    Article  CAS  PubMed  Google Scholar 

  16. Cheong, W.-S., Lee, C.-H., Moon, Y.-H., Oh, H.-S., Kim, S.-R., Lee, S. H., Lee, C.-H., & Lee, J.-K. (2013). Isolation and identification of indigenous quorum quenching bacteria, Pseudomonas sp. 1A1, for biofouling control in MBR. Industrial and Engineering Chemistry Research, 52, 10554–10560.

    Article  CAS  Google Scholar 

  17. Choo, K. H., Park, P. K. & Oh, H. S. (2020). Current developments in biotechnology and bioengineering: Advanced membrane separation processes for sustainable water and wastewater management – aerobic memebrane bioreactor processes and technologies. Elsevier, p. 245–274.

  18. Chowdhary, P. K., Keshavan, N., Nguyen, H. Q., Peterson, J. A., González, J. E., & Haines, D. C. (2007). Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biochemistry, 46, 14429–14437.

    Article  CAS  PubMed  Google Scholar 

  19. Coleman, D., O’Donnell, M., Shore, A., & Russell, R. (2009). Biofilm problems in dental unit water systems and its practical control. Journal of Applied Microbiology, 106, 1424–1437.

    Article  CAS  PubMed  Google Scholar 

  20. Colley, B., Dederer, V., Carnell, M., Kjelleberg, S., Rice, S. A., & Klebensberger, J. (2016). SiaA/D interconnects c-di-GMP and RsmA signaling to coordinate cellular aggregation of Pseudomonas aeruginosa in response to environmental conditions. Frontiers in Microbiology, 7, 179.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cui, T., Bai, F., Sun, M., Lv, X., Li, X., Zhang, D., & Du, H. (2020). Lactobacillus crustorum ZHG 2–1 as novel quorum-quenching bacteria reducing virulence factors and biofilms formation of Pseudomonas aeruginosa. LWT, 117, 108696.

    Article  CAS  Google Scholar 

  22. Cui, Y., Gao, H., Yu, R., Gao, L., & Zhan, M. (2021). Biological-based control strategies for MBR membrane biofouling: A review. Water Science and Technology, 83, 2597–2614.

    Article  CAS  PubMed  Google Scholar 

  23. D’Angelo-Picard, C., Chapelle, E., Ratet, P., Faure, D., & Dessaux, Y. (2011). Transgenic plants expressing the quorum quenching lactonase AttM do not significantly alter root-associated bacterial populations. Research in Microbiology, 162, 951–958.

    Article  PubMed  Google Scholar 

  24. Davidsson, S., Mölling, P., Rider, J. R., Unemo, M., Karlsson, M. G., Carlsson, J., Andersson, S.-O., Elgh, F., Söderquist, B., & Andrén, O. (2016). Frequency and typing of Propionibacterium acnes in prostate tissue obtained from men with and without prostate cancer. Infectious Agents and Cancer, 11, 1–10.

    Google Scholar 

  25. de Oliveira Souza, N., Cunha, D. A., de Sousa Rodrigues, N., Pereira, A. L., Medeiros, E. J. T., de AzevedoPinheiro, A., de Vasconcelos, M. A., do NascimentoNeto, L. G., Bezerra, T. T., & Mazzetto, S. E. (2022). Cashew nut shell liquids: Antimicrobial compounds in prevention and control of the oral biofilms. Archives of Oral Biology, 133, 105299.

    Article  Google Scholar 

  26. Defoirdt, T., Boon, N., & Bossier, P. (2010). Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathogens, 6, e1000989.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Dong, X., Qin, J., Zhang, Y., Chen, X., & Ge, S. (2022). Mitigation of membrane biofouling using quorum-quenching bacteria in a continuously operated membrane bioreactor. International Biodeterioration and Biodegradation, 166, 105339.

    Article  CAS  Google Scholar 

  28. Dong, X., Zhu, R., Li, Y., Qin, J., & Ge, S. (2020). Characterization of an indigenous quorum quenching bacterium and its effect on the SMP, EPS, and microbial community of sludge mixture during wastewater treatment. International Biodeterioration and Biodegradation, 152, 104995.

    Article  CAS  Google Scholar 

  29. Dong, Y.-H., Wang, L.-H., Xu, J.-L., Zhang, H.-B., Zhang, X.-F., & Zhang, L.-H. (2001). Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 411, 813–817.

    Article  CAS  PubMed  Google Scholar 

  30. Dong, Y. H., Gusti, A. R., Zhang, Q., Xu, J. L., & Zhang, L. H. (2002). Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Applied and Environment Microbiology, 68, 1754–1759.

    Article  CAS  Google Scholar 

  31. Dourou, D., Beauchamp, C. S., Yoon, Y., Geornaras, I., Belk, K. E., Smith, G. C., Nychas, G.-J.E., & Sofos, J. N. (2011). Attachment and biofilm formation by Escherichia coli O157: H7 at different temperatures, on various food-contact surfaces encountered in beef processing. International Journal of Food Microbiology, 149, 262–268.

    Article  PubMed  Google Scholar 

  32. Ergön-Can, T., Köse-Mutlu, B., Koyuncu, İ, & Lee, C.-H. (2017). Biofouling control based on bacterial quorum quenching with a new application: Rotary microbial carrier frame. Journal of Membrane Science, 525, 116–124.

    Article  Google Scholar 

  33. Fakhri, H., Shahi, A., Ovez, S., & Aydin, S. (2021). Bioaugmentation with immobilized endophytic Penicillium restrictum to improve quorum quenching activity for biofouling control in an aerobic hollow-fiber membrane bioreactor treating antibiotic-containing wastewater. Ecotoxicology and Environmental Safety, 210, 111831.

    Article  CAS  PubMed  Google Scholar 

  34. Flemming, H. C. (2011). Microbial biofouling: unsolved problems, insufficient approaches, and possible solutions. In H.C. Flemming, J. Wingender, & U. Szewzyk (Eds.), Biofilm highlights. Springer series on biofilms, 5. (pp. 81–109). Springer.

  35. Flemming, H. C. and Cloete, T. E. (2010). Environmental impact of controlling biofouling and biocorrosion in cooling water systems. In S. Rajagopal, H. A. Jenner, & V. P. Venugopalan  (Eds.), Operational and environmental consequences of large industrial cooling water systems, p 365–380.

  36. Flemming, H. C., Schaule, G., McDonogh, R. and Ridgway, H. F. (1994). Mechanism and extent of membrane biofouling. In  G.G. Geesey, Z. Lewandowski, & H. C. Flemming (Eds.), Biofouling and biocorrosion in industrial water systems (pp. 63–69). Lewis, Chelsea.

  37. Ganesh, P. S., & Rai, V. R. (2018). Attenuation of quorum-sensing-dependent virulence factors and biofilm formation by medicinal plants against antibiotic resistant Pseudomonas aeruginosa. Journal of Traditional and Complementary Medicine, 8, 170–177.

    Article  Google Scholar 

  38. García-Contreras, R., Maeda, T., & Wood, T. K. (2013). Resistance to quorum-quenching compounds. Applied and Environment Microbiology, 79, 6840–6846.

    Article  Google Scholar 

  39. Ghanei-Motlagh, R., Mohammadian, T., Gharibi, D., Khosravi, M., Mahmoudi, E., Zarea, M., El-Matbouli, M., & Menanteau-Ledouble, S. (2021). Quorum quenching probiotics modulated digestive enzymes activity, growth performance, gut microflora, haemato-biochemical parameters and resistance against Vibrio harveyi in Asian seabass (Lates calcarifer). Aquaculture, 531, 735874.

    Article  CAS  Google Scholar 

  40. Ghasemi, M., Chang, S., & Sivaloganathan, S. (2021). Development of an integrated ultrasonic biofilm detachment model for biofilm thickness control in membrane aerated bioreactors. Applied Mathematical Modelling, 100, 596–611.

    Article  Google Scholar 

  41. Gil, J., Túa, L., Rueda, A., Montaño, B., Rodríguez, M., & Prats, D. (2010). Monitoring and analysis of the energy cost of an MBR. Desalination, 250, 997–1001.

    Article  CAS  Google Scholar 

  42. Girennavar, B., Cepeda, M. L., Soni, K. A., Vikram, A., Jesudhasan, P., Jayaprakasha, G., Pillai, S. D., & Patil, B. S. (2008). Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. International Journal of Food Microbiology, 125, 204–208.

    Article  CAS  PubMed  Google Scholar 

  43. Global, M. (2012). market forecast to reach $888 million by 2017. Membrane Technology, 1, 8.

    Google Scholar 

  44. Grandclément, C., Tannières, M., Moréra, S., Dessaux, Y., & Faure, D. (2016). Quorum quenching: Role in nature and applied developments. FEMS Microbiology Reviews, 40, 86–116.

    Article  PubMed  Google Scholar 

  45. Gül, B. Y., Imer, D. Y., Park, P. K., & Koyuncu, I. (2018). Selection of quorum quenching (QQ) bacteria for membrane biofouling control: Effect of different Gram-staining QQ bacteria, Bacillus sp. T5 and Delftia sp. T6, on microbial population in membrane bioreactors. Water Science and Technology, 78, 358–366.

    Article  PubMed  Google Scholar 

  46. Guo, W., Ngo, H.-H., & Li, J. (2012). A mini-review on membrane fouling. Bioresource Technology, 122, 27–34.

    Article  CAS  PubMed  Google Scholar 

  47. Gurevich, D., Dor, S., Erov, M., Dan, Y., Moy, J. C., Mairesse, O., Dafny-Yelin, M., Adler-Abramovich, L., & Afriat-Jurnou, L. (2021). Directed enzyme evolution and encapsulation in peptide nanospheres of quorum quenching lactonase as an antibacterial treatment against plant pathogen. ACS Applied Materials & Interfaces, 13, 2179–2188.

    Article  CAS  Google Scholar 

  48. Ham, S.-Y., Kim, H.-S., Cha, E., Park, J.-H., & Park, H.-D. (2018). Mitigation of membrane biofouling by a quorum quenching bacterium for membrane bioreactors. Bioresource Technology, 258, 220–226.

    Article  CAS  PubMed  Google Scholar 

  49. Ham, S.-Y., Kim, H.-S., Jang, Y., Ryoo, H.-S., Lee, J.-H., Park, J.-H., & Park, H.-D. (2021). Synergistic control of membrane biofouling using linoleic acid and sodium hypochlorite. Chemosphere, 268, 128802.

    Article  CAS  PubMed  Google Scholar 

  50. Ham, S.-Y., Kim, H.-S., Jang, Y., Sun, P.-F., Park, J.-H., Lee, J. S., Byun, Y., & Park, H.-D. (2019). Control of membrane biofouling by 6-gingerol analogs: Quorum sensing inhibition. Fuel, 250, 79–87.

    Article  CAS  Google Scholar 

  51. Han, Q., Song, X., Zhang, Z., Fu, J., Wang, X., Malakar, P. K., Liu, H., Pan, Y., & Zhao, Y. (2017). Removal of foodborne pathogen biofilms by acidic electrolyzed water. Frontiers in Microbiology, 8, 988.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Haridas, D. V., Joshy, C., & Pillai, D. (2022). Optimization of the multispecies probiotic combination with N-acylhomoserine lactone-degrading ability for increased disease resistance of Carassius auratus using response surface methodology. Aquaculture, 548, 737597.

    Article  Google Scholar 

  53. Hemmati, F., Salehi, R., Ghotaslou, R., Kafil, H. S., Hasani, A., Gholizadeh, P., Nouri, R., & Rezaee, M. A. (2020). Quorum quenching: A potential target for antipseudomonal therapy. Infection and Drug Resistance, 13, 2989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hogan, D. A. (2006). Quorum sensing: Alcohols in a social situation. Current Biology, 16, R457–R458.

    Article  CAS  PubMed  Google Scholar 

  55. Hornby, J. M., Jensen, E. C., Lisec, A. D., Tasto, J. J., Jahnke, B., Shoemaker, R., Dussault, P., & Nickerson, K. W. (2001). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Applied and Environment Microbiology, 67, 2982–2992.

    Article  CAS  Google Scholar 

  56. Huang, J., Yang, Y., Zeng, G., Gu, Y., Shi, Y., Yi, K., Ouyang, Y., Hu, J., & Shi, L. (2019). Membrane layers intensifying quorum quenching alginate cores and its potential for membrane biofouling control. Bioresource Technology, 279, 195–201.

    Article  CAS  PubMed  Google Scholar 

  57. Husain, F. M., Ahmad, I., Khan, M. S., Ahmad, E., Tahseen, Q., Khan, M. S., & Alshabib, N. A. (2015). Sub-MICs of Mentha piperita essential oil and menthol inhibits AHL mediated quorum sensing and biofilm of Gram-negative bacteria. Frontiers in Microbiology, 6, 420.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ivanova, A., Ivanova, K., Tied, A., Heinze, T., & Tzanov, T. (2020). Layer-by-layer coating of aminocellulose and quorum quenching acylase on silver nanoparticles synergistically eradicate bacteria and their biofilms. Advanced Functional Materials, 30, 2001284.

    Article  CAS  Google Scholar 

  59. Ivanova, K., Fernandes, M. M., Francesko, A., Mendoza, E., Guezguez, J., Burnet, M., & Tzanov, T. (2015). Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS Applied Materials & Interfaces, 7, 27066–27077.

    Article  CAS  Google Scholar 

  60. Jenal, U., Reinders, A., & Lori, C. (2017). Cyclic di-GMP: Second messenger extraordinaire. Nature Reviews Microbiology, 15, 271–284.

    Article  CAS  PubMed  Google Scholar 

  61. Jiang, B., Zeng, Q., Hou, Y., Liu, J., Xu, J., Li, H., Du, C., Shi, S., & Ma, F. (2020). Quorum quenching bacteria bioaugmented GO/PPy modified membrane in EMBR for membrane antifouling. Science of the Total Environment, 718, 137412.

    Article  CAS  PubMed  Google Scholar 

  62. Jiang, W., Xia, S., Liang, J., Zhang, Z., & Hermanowicz, S. W. (2013). Effect of quorum quenching on the reactor performance, biofouling and biomass characteristics in membrane bioreactors. Water Research, 47, 187–196.

    Article  CAS  PubMed  Google Scholar 

  63. Judd, S. (2004). A review of fouling of membrane bioreactors in sewage treatment. Water Science and Technology, 49, 229–235.

    Article  CAS  PubMed  Google Scholar 

  64. Judd, S. (2005). Fouling control in submerged membrane bioreactors. Water Science and Technology, 51, 27–34.

    Article  CAS  PubMed  Google Scholar 

  65. Kalia, V. C. (2013). Quorum sensing inhibitors: An overview. Biotechnology Advances, 31, 224–245.

    Article  CAS  PubMed  Google Scholar 

  66. Kampouris, I. D., Karayannakidis, P. D., Banti, D. C., Sakoula, D., Konstantinidis, D., Yiangou, M., & Samaras, P. E. (2018). Evaluation of a novel quorum quenching strain for MBR biofouling mitigation. Water Research, 143, 56–65.

    Article  CAS  PubMed  Google Scholar 

  67. Kang, J. E., Han, J. W., Jeon, B. J., & Kim, B. S. (2016). Efficacies of quorum sensing inhibitors, piericidin A and glucopiericidin A, produced by Streptomyces xanthocidicus KPP01532 for the control of potato soft rot caused by Erwinia carotovora subsp. atroseptica. Microbiological Research, 184, 32–41.

    Article  CAS  PubMed  Google Scholar 

  68. Kaur, J., & Yogalakshmi, K. N. (2018). Control of sludge microbial biofilm by novel quorum quenching bacteria Pseudomonas nitroreducens JYQ3 and Pseudomonas JYQ4 encapsulated sodium alginate - Magnetic iron nanocomposites. International Biodeterioration and Biodegradation, 134, 68–75.

    Article  CAS  Google Scholar 

  69. Khalid, S. J., Ain, Q., Khan, S. J., Jalil, A., Siddiqui, M. F., Ahmad, T., Badshah, M. & Adnan, F. (2021). Targeting Acyl Homoserine Lactones (AHLs) by the quorum quenching bacterial strains to control biofilm formation in Pseudomonas aeruginosa. Saudi Journal of Biological Sciences 29(3), 1673–1682.

  70. Khalid, S. J., Ain, Q., Khan, S. J., Jalil, A., Siddiqui, M. F., Ahmad, T., Badshah, M., & Adnan, F. (2022). Targeting Acyl Homoserine Lactones (AHLs) by the quorum quenching bacterial strains to control biofilm formation in Pseudomonas aeruginosa. Saudi Journal of Biological Sciences, 29, 1673–1682.

    Article  CAS  PubMed  Google Scholar 

  71. Khan, R., Shen, F., Khan, K., Liu, L. X., Wu, H. H., Luo, J. Q. and Wan, Y. H. (2016). Biofouling control in a membrane filtration system by a newly isolated novel quorum quenching bacterium, Bacillus methylotrophicus sp. WY. RSC Advances, 6, 28895-28903.

  72. Kim, T. H., Lee, I., Yeon, K.-M., & Kim, J. (2018). Biocatalytic membrane with acylase stabilized on intact carbon nanotubes for effective antifouling via quorum quenching. Journal of Membrane Science, 554, 357–365.

    Article  CAS  Google Scholar 

  73. Kobayashi, H. (2001). Airway biofilm disease. International Journal of Antimicrobial Agents, 17, 351–356.

    Article  CAS  PubMed  Google Scholar 

  74. Kochkodan, V., & Hilal, N. (2015). A comprehensive review on surface modified polymer membranes for biofouling mitigation. Desalination, 356, 187–207.

    Article  CAS  Google Scholar 

  75. Komlenic, R. (2010). Rethinking the causes of membrane biofouling. Filtration & Separation, 47, 26–28.

    Article  Google Scholar 

  76. Kuehnast, T., Cakar, F., Weinhäupl, T., Pilz, A., Selak, S., Schmidt, M. A., Rüter, C., & Schild, S. (2018). Comparative analyses of biofilm formation among different Cutibacterium acnes isolates. International Journal of Medical Microbiology, 308, 1027–1035.

    Article  CAS  PubMed  Google Scholar 

  77. Lade, H., Song, W. J., Yu, Y. J., Ryu, J. H., Arthanareeswaran, G., & 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 Advances, 7, 16392–16400.

    Article  CAS  Google Scholar 

  78. Lazăr, V. (2003). Microbial adhesion. Romanian Academy Publish., pub house, Bucharest, pp.1–21.

  79. Lee, J., Lee, I., Nam, J., Hwang, D. S., Yeon, K.-M., & Kim, J. (2017). Immobilization and stabilization of acylase on carboxylated polyaniline nanofibers for highly effective antifouling application via quorum quenching. ACS Applied Materials & Interfaces, 9, 15424–15432.

    Article  CAS  Google Scholar 

  80. Lee, K., Kim, Y.-W., Lee, S., Lee, S. H., Nahm, C. H., Kwon, H., Park, P.-K., Choo, K.-H., Koyuncu, I., Drews, A., Lee, C.-H., & Lee, J.-K. (2018). Stopping autoinducer-2 chatter by means of an indigenous bacterium (Acinetobacter sp. DKY-1): A new antibiofouling strategy in a membrane bioreactor for wastewater treatment. Environmental Science and Technology, 52, 6237–6245.

    Article  CAS  PubMed  Google Scholar 

  81. Lee, K., Lee, S., Lee, S. H., Kim, S.-R., Oh, H.-S., Park, P.-K., Choo, K.-H., Kim, Y.-W., Lee, J.-K., & Lee, C.-H. (2016). Fungal quorum quenching: A paradigm shift for energy savings in membrane bioreactor (MBR) for wastewater treatment. Environmental Science and Technology, 50, 10914–10922.

    Article  CAS  PubMed  Google Scholar 

  82. Lee, S., Park, S.-K., Kwon, H., Lee, S. H., Lee, K., Nahm, C. H., Jo, S. J., 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. Environmental Science and Technology, 50, 1788–1795.

    Article  CAS  PubMed  Google Scholar 

  83. Li, S., Chen, P., Maddela, N. R., Yang, X., Chen, S., Feng, J., Zhang, S., & Zhang, L. (2022). Effects of filtration modes on fouling characteristic and microbial community of bio-cake in a membrane bioreactor. Journal of Environmental Chemical Engineering10, 107465.

  84. Li, Y., Tan, L., Guo, L., Zhang, P., Malakar, P. K., Ahmed, F., Liu, H., Wang, J. J., & Zhao, Y. (2020). Acidic electrolyzed water more effectively breaks down mature Vibrio parahaemolyticus biofilm than DNase I. Food Control, 117, 107312.

    Article  CAS  Google Scholar 

  85. Liao, B., Bagley, D., Kraemer, H., Leppard, G., & Liss, S. (2004). A review of biofouling and its control in membrane separation bioreactors. Water Environment Research, 76, 425–436.

    Article  CAS  PubMed  Google Scholar 

  86. Lindsay, A. K., Deveau, A., Piispanen, A. E., & Hogan, D. A. (2012). Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans. Eukaryotic Cell, 11, 1219–1225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Liu, J., Eng, C. Y., Ho, J. S., Chong, T. H., Wang, L., Zhang, P., & Zhou, Y. (2019). Quorum quenching in anaerobic membrane bioreactor for fouling control. Water Research, 156, 159–167.

    Article  CAS  PubMed  Google Scholar 

  88. Liu, J., Sun, F., Zhang, P., & Zhou, Y. (2021). Integrated powdered activated carbon and quorum quenching strategy for biofouling control in industrial wastewater membrane bioreactor. Journal of Cleaner Production, 279, 123551.

    Article  CAS  Google Scholar 

  89. Liu, Q., Ren, J., Lu, Y., Zhang, X., Roddick, F. A., Fan, L., Wang, Y., Yu, H., & Yao, P. (2021). A review of the current in-situ fouling control strategies in MBR: Biological versus physicochemical. Journal of Industrial and Engineering Chemistry, 98, 42–59.

    Article  CAS  Google Scholar 

  90. Liu, W., Lu, H., Chu, X., Lou, T., Zhang, N., Zhang, B., & Chu, W. (2020). Tea polyphenols inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances resistance to Klebsiella pneumoniae infection in Caenorhabditis elegans model. Microbial Pathogenesis, 147, 104266.

    Article  CAS  PubMed  Google Scholar 

  91. Liu, W., Røder, H. L., Madsen, J. S., Bjarnsholt, T., Sørensen, S. J. & Burmølle, M. (2016). Interspecific bacterial interactions are reflected in multispecies biofilm spatial organization. Frontiers in Microbiology, 7, 1366.

  92. Liu, X., Cao, B., Yang, L., & Gu, J.-D. (2022). Biofilm control by interfering with c-di-GMP metabolism and signaling. Biotechnology Advances, 56, 107915.

  93. Liu, Y., Shi, L., Su, L., van der Mei, H. C., Jutte, P. C., Ren, Y., & Busscher, H. J. (2019). Nanotechnology-based antimicrobials and delivery systems for biofilm-infection control. Chemical Society Reviews, 48, 428–446.

    Article  CAS  PubMed  Google Scholar 

  94. Luo, X., Xu, X., Cao, R., Wan, Q., Wang, J., Xu, H., Lin, Y., Wen, G., & Huang, T. (2021). The formation kinetics and control of biofilms by three dominant fungi species isolated from groundwater. Journal of Environmental Sciences, 109, 148–160.

    Article  CAS  Google Scholar 

  95. Luo, X., Zhang, B., Lu, Y., Mei, Y., & Shen, L. (2022). Advances in application of ultraviolet irradiation for biofilm control in water and wastewater infrastructure. Journal of Hazardous Materials, 421, 126682.

    Article  CAS  PubMed  Google Scholar 

  96. Maddela, N. R., & Meng, F. (2020). Discrepant roles of a quorum quenching bacterium (Rhodococcus sp. BH4) in growing dual-species biofilms. Science of the Total Environment, 713, 136402.

    Article  CAS  PubMed  Google Scholar 

  97. Maddela, N. R., Sheng, B., Yuan, S., Zhou, Z., Villamar-Torres, R., & Meng, F. (2019). Roles of quorum sensing in biological wastewater treatment: A critical review. Chemosphere, 221, 616–629.

    Article  CAS  PubMed  Google Scholar 

  98. Maddela, N. R., & Torres, R. O. V. (2021). The presence of low fouling-causing bacteria can lead to decreased membrane fouling potentials of mixed cultures. Journal of Environmental Chemical Engineering, 9, 105131.

    Article  CAS  Google Scholar 

  99. Maddela, N. R., Zhou, Z., Yu, Z., Zhao, S., and Meng, F. (2018). Functional determinants of extracellular polymeric substances in membrane biofouling: Experimental evidence from pure-cultured sludge bacteria. Applied and Environmental Microbiology, 84.

  100. Manefield, M., de Nys, R., Naresh, K., Roger, R., Givskov, M., Peter, S., & Kjelleberg, S. (1999). Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology (Reading, England), 145(Pt 2), 283–291.

    Article  CAS  PubMed  Google Scholar 

  101. Maria da Gloria, C. & Sarubbo, L. A. (2021). Synthetic and Biological Surfactants Used to Mitigate Biofouling on Industrial Facilities Surfaces, Biointerface Research in Applied Chemistry 12(2), 2560-2585.

  102. Marrot, B., Barrios-Martinez, A., Moulin, P., & Roche, N. (2004). Industrial wastewater treatment in a membrane bioreactor: A review. Environmental Progress, 23, 59–68.

    Article  CAS  Google Scholar 

  103. Marsh, R. L., Binks, M. J., Smith-Vaughan, H. C., Janka, M., Clark, S., Richmond, P., Chang, A. B., & Thornton, R. B. (2022). Prevalence and subtyping of biofilms present in bronchoalveolar lavage from children with protracted bacterial bronchitis or non-cystic fibrosis bronchiectasis: A cross-sectional study. The Lancet Microbe, 3(9).

  104. Mauermann, M., Eschenhagen, U., Bley, T., & Majschak, J.-P. (2009). Surface modifications–application potential for the reduction of cleaning costs in the food processing industry. Trends in Food Science & Technology, 20, S9–S15.

    Article  CAS  Google Scholar 

  105. Mehmood, C. T., Waheed, H., Tan, W., & Xiao, Y. (2021). Photocatalytic quorum quenching: A new antifouling and in-situ membrane cleaning strategy for an external membrane bioreactor coupled to UASB. Journal of Environmental Chemical Engineering, 9, 105470.

    Article  CAS  Google Scholar 

  106. Meng, F., Chae, S.-R., Drews, A., Kraume, M., Shin, H.-S., & Yang, F. (2009). Recent advances in membrane bioreactors (MBRs): Membrane fouling and membrane material. Water Research, 43, 1489–1512.

    Article  CAS  PubMed  Google Scholar 

  107. Meng, F., Zhang, S., Oh, Y., Zhou, Z., Shin, H.-S., & Chae, S.-R. (2017). Fouling in membrane bioreactors: An updated review. Water Research, 114, 151–180.

    Article  CAS  PubMed  Google Scholar 

  108. Meng, S., Wang, R., Zhang, M., Meng, X., Liu, H., & Wang, L. (2019). Insights into the fouling propensities of natural derived alginate blocks during the microfiltration process. Processes, 7, 858.

    Article  CAS  Google Scholar 

  109. Millanar-Marfa, J. M. J., Borea, L., Hasan, S. W., de Luna, M. D. G., Belgiorno, V. & Naddeo, V. (2020). Self-forming dynamic membrane: A review. In V. Naddeo et al. (Eds.), Frontiers in water-energy-nexus-naturebased solutions, advanced technologies and best practices for environmental sustainability, advances in science, technology and innovation. Springer nature switzerland AG.

  110. Mirzaei, R., Mohammadzadeh, R., Sholeh, M., Karampoor, S., Abdi, M., Dogan, E., Moghadam, M. S., Kazemi, S., Jalalifar, S., & Dalir, A. (2020). The importance of intracellular bacterial biofilm in infectious diseases. Microbial Pathogenesis, 147, 104393.

    Article  CAS  PubMed  Google Scholar 

  111. Moradi, F., & Hadi, N. (2021). Quorum-quenching activity of some Iranian medicinal plants. New Microbes and New Infections, 42, 100882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Moreira, J., Fulgêncio, R., Alves, P., Machado, I., Bialuch, I., Melo, L., Simões, M., & Mergulhão, F. (2016). Evaluation of SICAN performance for biofouling mitigation in the food industry. Food Control, 62, 201–207.

    Article  CAS  Google Scholar 

  113. Moreira, J., Gomes, L., Simões, M., Melo, L., & Mergulhão, F. (2015). The impact of material properties, nutrient load and shear stress on biofouling in food industries. Food and Bioproducts Processing, 95, 228–236.

    Article  Google Scholar 

  114. Musthafa, K. S., Ravi, A. V., Annapoorani, A., Packiavathy, I. S. V., & Pandian, S. K. (2010). Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl-homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa. Chemotherapy, 56, 333–339.

    Article  CAS  PubMed  Google Scholar 

  115. Nahar, S., Jeong, H. L., Kim, Y., Ha, A.J.-W., Roy, P. K., Park, S. H., Ashrafudoulla, M., Mizan, M. F. R., & Ha, S.-D. (2021). Inhibitory effects of Flavourzyme on biofilm formation, quorum sensing, and virulence genes of foodborne pathogens Salmonella Typhimurium and Escherichia coli. Food Research International, 147, 110461.

    Article  CAS  PubMed  Google Scholar 

  116. Nahm, C. H., Choi, D.-C., Kwon, H., Lee, S., Lee, S. H., Lee, K., Choo, K.-H., Lee, J.-K., Lee, C.-H., & Park, P.-K. (2017). Application of quorum quenching bacteria entrapping sheets to enhance biofouling control in a membrane bioreactor with a hollow fiber module. Journal of Membrane Science, 526, 264–271.

    Article  CAS  Google Scholar 

  117. Nakase, K., Koizumi, J., Midorikawa, R., Yamasaki, K., Tsutsui, M., Aoki, S., Nasu, Y., Hirai, Y., Nakaminami, H., & Noguchi, N. (2021). Cutibacterium acnes phylogenetic type IC and II isolated from patients with non-acne diseases exhibit high-level biofilm formation. International Journal of Medical Microbiology, 311, 151538.

    Article  CAS  PubMed  Google Scholar 

  118. Nithin, M., Girisha, S., Kushala, K., Chandan, D., Puneeth, T., BT, N. K., Vinay, T., Suresh, T., Sahoo, L., & Ramesh, K. (2021). Novel lytic bacteriophages (AhFM4 & AhFM5) as bio-control measures against multidrug resistant biofilm producing Aeromonas hydrophila (AhZ1K). Aquaculture, 544, 737106.

    Article  Google Scholar 

  119. Noori, A., Kim, H., Kim, M. H., Kim, K., Lee, K., & Oh, H.-S. (2022). Quorum quenching bacteria isolated from industrial wastewater sludge to control membrane biofouling. Bioresource Technology, 352, 127077.

    Article  CAS  PubMed  Google Scholar 

  120. Noori, M. T., Ghangrekar, M., Mukherjee, C., & Min, B. (2019). Biofouling effects on the performance of microbial fuel cells and recent advances in biotechnological and chemical strategies for mitigation. Biotechnology Advances, 37, 107420.

    Article  CAS  PubMed  Google Scholar 

  121. Oh, H.-S., & Lee, C.-H. (2018). Origin and evolution of quorum quenching technology for biofouling control in MBRs for wastewater treatment. Journal of Membrane Science, 554, 331–345.

    Article  CAS  Google Scholar 

  122. Omori, M., Bito, T., Yamada, M., Ogura, K., Eishi, Y., & Nishigori, C. (2015). Systemic sarcoidosis with bone marrow involvement showing Propionibacterium acnes in the lymph nodes. Journal of the European Academy of Dermatology and Venereology, 29, 2059–2060.

    Article  CAS  PubMed  Google Scholar 

  123. WHO and UNICEF (2017) Progress on drinking water, sanitation and hygiene: 2017 update and SDG baselines. World Health Organization, 9–10.

  124. Paluch, E., Rewak-Soroczyńska, J., Jędrusik, I., Mazurkiewicz, E., & Jermakow, K. (2020). Prevention of biofilm formation by quorum quenching. Applied Microbiology and Biotechnology, 104, 1871–1881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Pande, G. S. J., Natrah, F. M. I., Flandez, A. V. B., Kumar, U., Niu, Y., Bossier, P., & Defoirdt, T. (2015). Isolation of AHL-degrading bacteria from micro-algal cultures and their impact on algal growth and on virulence of Vibrio campbellii to prawn larvae. Applied Microbiology and Biotechnology, 99, 10805–10813.

    Article  CAS  PubMed  Google Scholar 

  126. Park, S.-J., Lee, M.-S., Choi, W., & Lee, J.-H. (2022). Biocidal surfactant-assisted fabrication of thin film composite membranes with excellent and durable anti-biofouling performance. Chemical Engineering Journal, 431, 134114.

    Article  CAS  Google Scholar 

  127. Parsek, M. R., & Singh, P. K. (2003). Bacterial biofilms: An emerging link to disease pathogenesis. Annual Reviews in Microbiology, 57, 677–701.

    Article  CAS  Google Scholar 

  128. Percival, S. L., McCarty, S. M., & Lipsky, B. (2015). Biofilms and wounds: An overview of the evidence. Advances in Wound Care, 4, 373–381.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Pérez-Sánchez, T., Mora-Sánchez, B., & Balcázar, J. L. (2018). Biological approaches for disease control in aquaculture: Advantages, limitations and challenges. Trends in Microbiology, 26, 896–903.

    Article  PubMed  Google Scholar 

  130. Ponnusamy, K., Paul, D., & Kweon, J. H. (2009). Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environmental Engineering Science, 26, 1359–1363.

    Article  CAS  Google Scholar 

  131. Popat, R., Cornforth, D., McNally, L., & Brown, S. (2015). Collective sensing and collective responses in quorum-sensing bacteria. Journal of the Royal Society Interface, 12, 20140882.

    Article  PubMed  PubMed Central  Google Scholar 

  132. Poulsen, L. V. (1999). Microbial Biofilm in Food Processing. LWT - Food Science and Technology, 32, 321–326.

    Article  CAS  Google Scholar 

  133. Quan, K., Zhang, Z., Ren, Y., Busscher, H. J., van der Mei, H. C., & Peterson, B. W. (2021). Possibilities and impossibilities of magnetic nanoparticle use in the control of infectious biofilms. Journal of Materials Science & Technology, 69, 69–78.

    Article  CAS  Google Scholar 

  134. Rahmani, K., Jadidian, R., & Haghtalab, S. (2016). Evaluation of inhibitors and biocides on the corrosion, scaling and biofouling control of carbon steel and copper–nickel alloys in a power plant cooling water system. Desalination, 393, 174–185.

    Article  CAS  Google Scholar 

  135. Ramesh, A., Lee, D., Wang, M., Hsu, J., Juang, R., Hwang, K., Liu, J., & Tseng, S. (2006). Biofouling in membrane bioreactor. Separation Science and Technology, 41, 1345–1370.

    Article  CAS  Google Scholar 

  136. Reynolds, T. & Fink, G. (2001). Saccharomyces cerevisiae as a model for fungal biofilms. Yeast, pp. S279-S279. John Wiley & Sons ltd baffins lane chichester, w sussex po19 1ud, england, 2, 291, 5505, 878–81.

  137. Ridgway, H., Ishida, K., Rodriguez, G., Safarik, J., Knoell, T., & Bold, R. (1999). [34] Biofouling of membranes: Membrane preparation, characterization, and analysis of bacterial adhesion. Methods in Enzymology, 310, 463–494.

    Article  CAS  PubMed  Google Scholar 

  138. Rocha, F. R., Regis, W. F., Duarte, S., Muniz, F. W., & Rodrigues, L. K. (2020). Effect of bioactive compounds on the regulation of quorum sensing network-associated genes and virulence in Streptococcus mutans—a systematic review. Archives of Oral Biology, 119, 104893.

    Article  CAS  PubMed  Google Scholar 

  139. Rosa, J. V. d., Conceição, N. V. d., Conceição, R. d. C. d. S. d. & Timm, C. D. (2018) Biofilm formation by Vibrio parahaemolyticus on different surfaces and its resistance to sodium hypochlorite. Ciência Rural, Santa Maria, 48, 12, e20180612.

  140. Rudrappa, T., & Bais, H. P. (2008). Curcumin, a known phenolic from Curcuma longa, attenuates the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. Journal of Agriculture and Food Chemistry, 56, 1955–1962.

    Article  CAS  Google Scholar 

  141. Sabouhi, M., Torabian, A., Bozorg, A., & Mehrdadi, N. (2020). A novel convenient approach toward the fouling alleviation in membrane bioreactors using the combined methods of oxidation and coagulation. Journal of Water Process Engineering, 33, 101018.

    Article  Google Scholar 

  142. Sadovskaya, I., Vinogradov, E., Li, J., Hachani, A., Kowalska, K., & Filloux, A. (2010). High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: The ndvB gene is involved in the production of highly glycerol-phosphorylated β-(1→ 3)-glucans, which bind aminoglycosides. Glycobiology, 20, 895–904.

    Article  CAS  PubMed  Google Scholar 

  143. Sand, W., & Gehrke, T. (2006). Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron (III) ions and acidophilic bacteria. Research in Microbiology, 157, 49–56.

    Article  CAS  PubMed  Google Scholar 

  144. Sardana, K., Gupta, T., Garg, V. K., & Ghunawat, S. (2015). Antibiotic resistance to Propionobacterium acnes: Worldwide scenario, diagnosis and management. Expert Review of Anti-Infective Therapy, 13, 883–896.

    Article  CAS  PubMed  Google Scholar 

  145. Schimel, A. M., Miller, D., & Flynn, H. W., Jr. (2013). Endophthalmitis isolates and antibiotic susceptibilities: A 10-year review of culture-proven cases. American Journal of Ophthalmology, 156(50–52), e51.

    Google Scholar 

  146. Sedghizadeh, P. P., Sun, S., Jones, A. C., Sodagar, E., Cherian, P., Chen, C., Junka, A. F., Neighbors, J. D., McKenna, C. E., & Russell, R. G. G. (2021). Bisphosphonates in dentistry: Historical perspectives, adverse effects, and novel applications. Bone, 147, 115933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Sekeli, R., Nazaruddin, N. H., Tamizi, A. A., Amin, N. M., Wee, C.-Y., Sarip, J., Abdullah, Ni., Saidi, N. I., Razak, R. A., & Zulkifli, Z. (2019). Enhancing Eksotika papaya resistance to dieback disease through quorum quenching. Journal of Tropical Plant Physiology, 11, 1–9.

    Google Scholar 

  148. Shaheer, P., Sreejith, V., Joseph, T., Murugadas, V., & Lalitha, K. (2021). Quorum quenching Bacillus spp.: An alternative biocontrol agent for Vibrio harveyi infection in aquaculture. Diseases of Aquatic Organisms, 146, 117–128.

    Article  CAS  PubMed  Google Scholar 

  149. Shen, H., Durkin, D. P., Aiello, A., Diba, T., Lafleur, J., Zara, J. M., Shen, Y., & Shuai, D. (2021). Photocatalytic graphitic carbon nitride-chitosan composites for pathogenic biofilm control under visible light irradiation. Journal of Hazardous Materials, 408, 124890.

    Article  CAS  PubMed  Google Scholar 

  150. Shi, X., & Zhu, X. (2009). Biofilm formation and food safety in food industries. Trends in Food Science & Technology, 20, 407–413.

    Article  CAS  Google Scholar 

  151. Shikongo-Nambabi, M. N. N. N., Kachigunda, B., & Venter, S. N. (2010). Evaluation of oxidising disinfectants to control Vibrio biofilms in treated seawater used for fish processing. Water Sa, 36, 215–220.

    CAS  Google Scholar 

  152. Siddiqui, M. F., Rzechowicz, M., Harvey, W., Zularisam, A. W., & Anthony, G. F. (2015). Quorum sensing based membrane biofouling control for water treatment: A review. Journal of Water Process Engineering, 7, 112–122.

    Article  Google Scholar 

  153. Sikdar, R., & Elias, M. (2020). Quorum quenching enzymes and their effects on virulence, biofilm, and microbiomes: A review of recent advances. Expert Review of Anti-Infective Therapy, 18, 1221–1233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Simoes, L. C., & Simões, M. (2013). Biofilms in drinking water: Problems and solutions. Rsc Advances, 3, 2520–2533.

    Article  Google Scholar 

  155. Simoes, M., Simões, L. C., & Vieira, M. J. (2010). A review of current and emergent biofilm control strategies. LWT-Food Science and Technology, 43, 573–583.

    Article  CAS  Google Scholar 

  156. Song, P., Xiao, Y., Ren, Z. J., Brooks, J. P., Lu, L., Zhou, B., Zhou, Y., Freguia, S., Liu, Z., & Zhang, N. (2021). Electrochemical biofilm control by reconstructing microbial community in agricultural water distribution systems. Journal of Hazardous Materials, 403, 123616.

    Article  CAS  PubMed  Google Scholar 

  157. Srey, S., Jahid, I. K., & Ha, S.-D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31, 572–585.

    Article  Google Scholar 

  158. Srivastava, A., Gupta, J., Kumar, S., & Kumar, A. (2017). Gut biofilm forming bacteria in inflammatory bowel disease. Microbial Pathogenesis, 112, 5–14.

    Article  PubMed  Google Scholar 

  159. Stoica, I. M., Vitzilaiou, E., Lyng Røder, H., Burmølle, M., Thaysen, D., Knøchel, S., & van den Berg, F. (2018). Biofouling on RO-membranes used for water recovery in the dairy industry. Journal of Water Process Engineering, 24, 1–10.

    Article  Google Scholar 

  160. Stoica, P., Chifiriuc, M. C., Rapa, M., & Lazăr, V. (2017). in Biofilms and Implantable Medical Devices, (Deng, Y. and Lv, W., eds.), Woodhead Publishing, pp. 3–23.

  161. Sun, L., Forauer, E. C., Brown, S. R., & D’Amico, D. J. (2021). Application of bioactive glycolipids to control Listeria monocytogenes biofilms and as post-lethality contaminants in milk and cheese. Food Microbiology, 95, 103683.

    Article  CAS  PubMed  Google Scholar 

  162. Syafiuddin, A., Boopathy, R., & Mehmood, M. A. (2021). Recent advances on bacterial quorum quenching as an effective strategy to control biofouling in membrane bioreactors. Bioresource Technology Reports, 15, 100745.

    Article  CAS  Google Scholar 

  163. Tabraiz, S., Shamurad, B., Petropoulos, E., Quintela-Baluja, M., Charlton, A., Dolfing, J., & Sallis, P. J. (2021). Mitigation of membrane biofouling in membrane bioreactor treating sewage by novel quorum quenching strain of Acinetobacter originating from a full-scale membrane bioreactor. Bioresource Technology, 334, 125242.

    Article  CAS  PubMed  Google Scholar 

  164. Tan Lim, A. M., Oyong, G. G., Tan, M. C. S., Chang Shen, C., Ragasa, C. Y., & Cabrera, E. C. (2021). Quorum quenching activity of Andrographis paniculata (Burm f.) Nees andrographolide compounds on metallo-β-lactamase-producing clinical isolates of Pseudomonas aeruginosa PA22 and PA247 and their effect on lasR gene expression. Heliyon, 7, e07002.

  165. Tan, Y., Leonhard, M., Moser, D., Ma, S., & Schneider-Stickler, B. (2016). Inhibition of mixed fungal and bacterial biofilms on silicone by carboxymethyl chitosan. Colloids and Surfaces. B, Biointerfaces, 148, 193–199.

    Article  CAS  PubMed  Google Scholar 

  166. Turan, N. B., and Engin, G. Ö. (2018). in Comprehensive Analytical Chemistry, vol. 81, Elsevier, pp. 117–149.

  167. Valdez, R. M. A., annXimenez-Fyvie, L., Caiaffa, K. S., Dos Santos, V. R., Cervantes, R. M. G., Almaguer-Flores, A., & Duque, C. (2021). Antagonist effect of probiotic bifidobacteria on biofilms of pathogens associated with periodontal disease. Microbial Pathogenesis, 150, 104657.

  168. Vasavi, H., Arun, A., & Rekha, P. (2016). Anti-quorum sensing activity of flavonoid-rich fraction from Centella asiatica L. against Pseudomonas aeruginosa PAO1. Journal of Microbiology, Immunology, and Infection, 49, 8–15.

    Article  CAS  PubMed  Google Scholar 

  169. Vikram, A., Jayaprakasha, G. K., Jesudhasan, P., Pillai, S., & Patil, B. (2010). Suppression of bacterial cell–cell signalling, biofilm formation and type III secretion system by citrus flavonoids. Journal of Applied Microbiology, 109, 515–527.

    Article  CAS  PubMed  Google Scholar 

  170. Vikram, A., Jesudhasan, P. R., Jayaprakasha, G., Pillai, S. D., & Patil, B. S. (2011). Citrus limonoids interfere with Vibrio harveyi cell–cell signalling and biofilm formation by modulating the response regulator LuxO. Microbiology, 157, 99–110.

    Article  CAS  PubMed  Google Scholar 

  171. Wang, D., Chen, H., Li, J., Li, T., Ren, L., Liu, J., & Shen, Y. (2022). Screening and validation of quorum quenching enzyme PF2571 from Pseudomonas fluorescens strain PF08 to inhibit the spoilage of red sea bream filets. International Journal of Food Microbiology, 362, 109476.

    Article  CAS  PubMed  Google Scholar 

  172. Wang, D., Flint, S. H., Palmer, J. S., Gagic, D., Fletcher, G. C. & On, S. L. (2022). Global expansion of Vibrio parahaemolyticus threatens the seafood industry: Perspective on controlling its biofilm formation. LWT-Food Science and Technology, 158, 113182.

  173. Wang, J., Lin, J., Zhang, Y., Zhang, J., Feng, T., Li, H., Wang, X., Sun, Q., Zhang, X., & Wang, Y. (2019). Activity improvement and vital amino acid identification on the marine-derived quorum quenching enzyme MomL by protein engineering. Marine Drugs, 17, 300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Wang, Z., Ma, J., Tang, C. Y., Kimura, K., Wang, Q., & Han, X. (2014). Membrane cleaning in membrane bioreactors: A review. Journal of Membrane Science, 468, 276–307.

    Article  CAS  Google Scholar 

  175. Weerasekara, N. A., Choo, K.-H., & Lee, C.-H. (2014). Hybridization of physical cleaning and quorum quenching to minimize membrane biofouling and energy consumption in a membrane bioreactor. Water Research, 67, 1–10.

    Article  CAS  PubMed  Google Scholar 

  176. Weerasekara, N. A., Choo, K.-H., & Lee, C.-H. (2016). Biofouling control: Bacterial quorum quenching versus chlorination in membrane bioreactors. Water Research, 103, 293–301.

    Article  CAS  PubMed  Google Scholar 

  177. Wolcott, R. D. (2020). Microbial biofilm may contribute to Alzheimer’s disease. Clinical Microbiology Newsletter, 42, 181–186.

    Article  Google Scholar 

  178. Wuersching, S. N., Huth, K. C., Hickel, R., & Kollmuss, M. (2021). Inhibitory effect of LL-37 and human lactoferricin on growth and biofilm formation of anaerobes associated with oral diseases. Anaerobe, 67, 102301.

    Article  CAS  PubMed  Google Scholar 

  179. Xu, F., Zhao, C., Lee, C. H., Wang, W., & Xu, Q. (2019). Anti-Biofouling Performance of an Immobilized Indigenous Quorum Quenching Bacterium Bacillus cereus HG10 and Its Influence on the Microbial Community in a Bioreactor. International Journal of Environmental Research Public Health, 16, 3777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Yang, Z., Ren, X., & Liu, Y. (2021). Multifunctional 3D printed porous GelMA/xanthan gum based dressing with biofilm control and wound healing activity. Materials Science and Engineering: C, 131, 112493.

    Article  CAS  PubMed  Google Scholar 

  181. 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. Environmental Science and Technology, 43, 380–385.

    Article  CAS  PubMed  Google Scholar 

  182. Yeon, K.-M., Lee, C.-H., & Kim, J. (2009). Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environmental Science and Technology, 43, 7403–7409.

    Article  CAS  PubMed  Google Scholar 

  183. Yu, C., Wu, J., Contreras, A. E., & Li, Q. (2012). Control of nanofiltration membrane biofouling by Pseudomonas aeruginosa using d-tyrosine. Journal of Membrane Science, 423, 487–494.

    Article  Google Scholar 

  184. Yu, H., Liang, H., Qu, F., He, J., Xu, G., Hu, H., & Li, G. (2016). Biofouling control by biostimulation of quorum-quenching bacteria in a membrane bioreactor for wastewater treatment. Biotechnology and Bioengineering, 113, 2624–2632.

    Article  CAS  PubMed  Google Scholar 

  185. Yu, P., Ye, H., Ma, S., & Shan, H. (2021). Study of quorum quenching bacteria Cobetia sp. reducing the mortality of Penaeus vannamei infected with Vibrio harveyi: In vitro and in vivo tests. Aquaculture, 534, 736244.

    Article  CAS  Google Scholar 

  186. Yuan, G., Tian, Y., Wang, B., You, X., & Liao, Y. (2022). Mitigation of membrane biofouling via immobilizing Ag-MOFs on composite membrane surface for extractive membrane bioreactor. Water Research, 209, 117940.

    Article  CAS  Google Scholar 

  187. Yue, X., Koh, Y. K. K., & Ng, H. Y. (2015). Effects of dissolved organic matters (DOMs) on membrane fouling in anaerobic ceramic membrane bioreactors (AnCMBRs) treating domestic wastewater. Water Research, 86, 96–107.

    Article  CAS  PubMed  Google Scholar 

  188. Zhang, J., Loong, W. L. C., Chou, S., Tang, C., Wang, R., & Fane, A. G. (2012). Membrane biofouling and scaling in forward osmosis membrane bioreactor. Journal of Membrane Science, 403, 8–14.

    Article  Google Scholar 

  189. Zhang, Y., Sass, A., Van Acker, H., Wille, J., Verhasselt, B., Van Nieuwerburgh, F., Kaever, V., Crabbé, A. & Coenye, T. (2018). Coumarin reduces virulence and biofilm formation in Pseudomonas aeruginosa by affecting quorum sensing, type III secretion and C-di-GMP levels. Frontiers in Microbiology, 21, 9, 1952.

  190. Zhao, X., & Kuipers, O. P. (2021). Synthesis of silver-nisin nanoparticles with low cytotoxicity as antimicrobials against biofilm-forming pathogens. Colloids and Surfaces. B, Biointerfaces, 206, 111965.

    Article  CAS  PubMed  Google Scholar 

  191. Zhu, Y., Li, C., Cui, H., & Lin, L. (2020). Feasibility of cold plasma for the control of biofilms in food industry. Trends in Food Science & Technology, 99, 142–151.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Naga Raju Maddela: conceptualization; investigation, and writing (original draft, review, and editing). Aransiola Sesan Abiodun: writing (review and editing) and validation. Shaoqing Zhang: writing (review and editing) and validation. Ram Prasad: conceptualization; supervision; and review and editing the final draft. All authors read the final manuscript.

Corresponding author

Correspondence to Ram Prasad.

Ethics declarations

Ethical Approval

This article does not contain any studies with human participants or animals.

Consent to Participate

All authors agree mutually with the participation and publication of this work and declare that this is original research.

Consent for Publication

All authors agree mutually to publication of this work.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maddela, N.R., Abiodun, A.S., Zhang, S. et al. Biofouling in Membrane Bioreactors—Mitigation and Current Status: a Review. Appl Biochem Biotechnol 195, 5643–5668 (2023). https://doi.org/10.1007/s12010-022-04262-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04262-3

Keywords

Navigation