Bacterial biofilms: role of quorum sensing and quorum quenching

DHRITISHREE  GHOSH; MADHUPA  SETH; PRIYAJIT MONDAL; SUBHRA KANTI MUKHOPADHYAY

doi:10.18006/2022.10(2).278.293

Authors

DHRITISHREE GHOSH https://orcid.org/0000-0001-8650-2906
MADHUPA SETH https://orcid.org/0000-0003-1736-5869
PRIYAJIT MONDAL https://orcid.org/0000-0002-0903-4050
SUBHRA KANTI MUKHOPADHYAY PROFESSOR https://orcid.org/0000-0001-9284-0880

DOI:

https://doi.org/10.18006/2022.10(2).278.293

Keywords:

Bacterial biofilms, Multi-drug resistance, N-acyl homoserine lactones, Quorum sensing, Quorum quenching

Abstract

Bacterial biofilms provide an adjustable strategy to manage themselves in the existing conditions. Biofilms of pathogenic bacteria act as a reservoir for various device and non-device related diseases which are tough to cure. Exposure to a high dose of antibiotics is not an appropriate solution to this problem as high antibiotic concentrations lead to the generation of Multi-drug resistant strains as well as affect the human body. So, it is needed to bypass the use of antibiotics to prevent bacterial biofilms. In this context, Quorum Sensing (QS) may be a potential target since biofilm formation is regulated by QS. N-acyl homoserine lactones (N-AHL) act as predominant QS signal molecules in Gram-negative bacteria. Counteraction of the QS-regulated activities using quorum quenching may be an alternative way to combat biofilm formation in bacteria. Quorum sensing inhibitors (QSIs) and QQ enzymes play a significant role in this regard either by interference with the signal generation, perception, or by degradation, and chemical modification, respectively. Many quorum quenching enzymes have been reported from bacteria. Extremophilic bacteria have also been reported to produce potent quorum quenching enzymes which can effectively break down N-AHLs.

References

Abebe, G.M. (2020) The Role of Bacterial Biofilm in Antibiotic Resistance and Food Contamination. International Journal of Microbiology, Article ID 1705814, https://doi.org/10.1155/ 2020/1705814 DOI: https://doi.org/10.1155/2020/1705814

Abed, R. M., Dobretsov, S., Al-Fori, M., Gunasekera, S. P., Sudesh, K., & Paul, V. J. (2013). Quorum-sensing inhibitory compounds from extremophilic microorganisms isolated from a hypersaline cyanobacterial mat. Journal of Industrial Microbiology and Biotechnology, 40(7), 759-772. DOI: https://doi.org/10.1007/s10295-013-1276-4

Alkawash, M. A., Soothill, J. S., & Schiller, N. L. (2006). Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. Apmis, 114(2), 131-138 DOI: https://doi.org/10.1111/j.1600-0463.2006.apm_356.x

Bagge, N., Hentzer, M., Andersen, J. B., Ciofu, O., Givskov, M., & Høiby, N. (2004). Dynamics and spatial distribution of β-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 48(4), 1168-1174 DOI: https://doi.org/10.1128/AAC.48.4.1168-1174.2004

Bhattacharjee, A., Nusca, T. D., & Hochbaum, A. I. (2016). Rhamnolipids mediate an interspecies biofilm dispersal signaling pathway. ACS Chemical Biology, 11(11), 3068-3076 DOI: https://doi.org/10.1021/acschembio.6b00750

Boehm, A., Steiner, S., Zaehringer, F., Casanova, A., et al. (2009). Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Molecular Microbiology, 72(6), 1500-1516 DOI: https://doi.org/10.1111/j.1365-2958.2009.06739.x

Boles, B. R., Thoendel, M., & Singh, P. K. (2005). Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Molecular Microbiology, 57(5), 1210-1223 DOI: https://doi.org/10.1111/j.1365-2958.2005.04743.x

Cadavid, E., & Echeverri, F. (2019). The search for natural inhibitors of biofilm formation and the activity of the autoinductor C6-AHL in Klebsiella pneumoniae ATCC 13884. Biomolecules, 9(2), 49 DOI: https://doi.org/10.3390/biom9020049

Cao, Y., He, S., Zhou, Z., Zhang, M., et al. (2012). Orally administered thermostable N-acyl homoserine lactonase from Bacillus sp. strain AI96 attenuates Aeromonas hydrophila infection in zebrafish. Applied and Environmental Microbiology, 78(6), 1899-1908 DOI: https://doi.org/10.1128/AEM.06139-11

Chan, B. K., Abedon, S. T., & Loc-Carrillo, C. (2013). Phage cocktails and the future of phage therapy. Future Microbiology, 8(6), 769-783 DOI: https://doi.org/10.2217/fmb.13.47

Chen, X., Chen, J., Yan, Y., Chen, S., et al. (2019). Quorum sensing inhibitors from marine bacteria Oceanobacillus sp. XC22919. Natural Product Research, 33(12), 1819-1823 DOI: https://doi.org/10.1080/14786419.2018.1437436

Chmielewski, R. A. N., & Frank, J. F. (2003). Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2(1), 22-32 DOI: https://doi.org/10.1111/j.1541-4337.2003.tb00012.x

Chu, Y. Y., Nega, M., Wölfle, M., Plener, L., et al. (2013) A new class of quorum quenching molecules from Staphylococcus species affects communication and growth of gram-negative bacteria. PLoS Pathogens 9:e1003654. https://doi.org/10.1371/ journal.ppat.1003654 DOI: https://doi.org/10.1371/journal.ppat.1003654

Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I., & Penadés, J. R. (2001). Bap, a Staphylococcus aureus surface protein involved in biofilm formation. Journal of Bacteriology, 183(9), 2888-2896 DOI: https://doi.org/10.1128/JB.183.9.2888-2896.2001

Curtin, J. J., & Donlan, R. M. (2006). Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrobial Agents and Chemotherapy, 50(4), 1268-1275 DOI: https://doi.org/10.1128/AAC.50.4.1268-1275.2006

Dales, L., Ferris, W., Vandemheen, K., & Aaron, S. D. (2009). Combination antibiotic susceptibility of biofilm-grown Burkholderia cepacia and Pseudomonas aeruginosa isolated from patients with pulmonary exacerbations of cystic fibrosis. European Journal of Clinical Microbiology & Infectious Diseases, 28(10), 1275-1279 DOI: https://doi.org/10.1007/s10096-009-0774-9

Davey, M. E., Caiazza, N. C., & O'Toole, G. A. (2003). Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 185(3), 1027-1036 DOI: https://doi.org/10.1128/JB.185.3.1027-1036.2003

Davies, D. G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., & Greenberg, E.P. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 280, 295-298 DOI: https://doi.org/10.1126/science.280.5361.295

Donelli, G., Francolini, I., Romoli, D., Guaglianone, E., et al. (2007). Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrobial Agents and Chemotherapy, 51(8), 2733-2740 DOI: https://doi.org/10.1128/AAC.01249-06

Dong, W., Zhu, J., Guo, X., Kong, D., et al. (2018). Characterization of AiiK, an AHL lactonase, from Kurthia huakui LAM0618T and its application in quorum quenching on Pseudomonas aeruginosa PAO1. Scientific Reports, 8(1), 1-11 DOI: https://doi.org/10.1038/s41598-018-24507-8

Dong, Y. H., Xu, J. L., Li, X. Z., & Zhang, L. H. (2000). AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proceedings of the National Academy of Sciences, 97(7), 3526-3531 DOI: https://doi.org/10.1073/pnas.97.7.3526

Dong, Y., Zhang, X. F., An, S. W., Xu, J. L., & Zhang, L. H. (2008). A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa. Communicative & Integrative Biology, 1(1), 88-96. DOI: https://doi.org/10.4161/cib.1.1.6717

Donlan, R. M. (2002). Biofilms: microbial life on surfaces. Emerging infectious diseases, 8(9), 881 DOI: https://doi.org/10.3201/eid0809.020063

Dueholm, M. S., Søndergaard, M. T., Nilsson, M., Christiansen, G., et al. (2013). Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen, 2(3), 365-382 DOI: https://doi.org/10.1002/mbo3.81

Dufour, D., Leung, V., & Lévesque, C. M. (2010). Bacterial biofilm: structure, function, and antimicrobial resistance. Endodontic Topics, 22(1), 2-16. DOI: https://doi.org/10.1111/j.1601-1546.2012.00277.x

Dwivedi, D., & Singh, V. (2016). Effects of the natural compounds embelin and piperine on the biofilm-producing property of Streptococcus mutans. Journal of Traditional and Complementary Medicine, 6(1), 57-61 DOI: https://doi.org/10.1016/j.jtcme.2014.11.025

Eckhart, L., Fischer, H., Barken, K. B., Tolker‐Nielsen, T., & Tschachler, E. (2007). DNase1L2 suppresses biofilm formation by Pseudomonas aeruginosa and Staphylococcus aureus. British Journal of Dermatology, 156(6), 1342-1345 DOI: https://doi.org/10.1111/j.1365-2133.2007.07886.x

Fauconnier, A. (2017). Regulating phage therapy: the biological master file concept could help to overcome regulatory challenge of personalized medicines. EMBO Reports, 18(2), 198-200 DOI: https://doi.org/10.15252/embr.201643250

Ferriol-González, C., & Domingo-Calap, P. (2020). Phages for biofilm removal. Antibiotics, 9(5), 268 DOI: https://doi.org/10.3390/antibiotics9050268

Fetzner, S. (2015). Quorum quenching enzymes. Journal of Biotechnology, 201, 2-14 DOI: https://doi.org/10.1016/j.jbiotec.2014.09.001

Fleming, D., Chahin, L., & Rumbaugh, K. (2017). Glycoside hydrolases degrade polymicrobial bacterial biofilms in wounds. Antimicrobial Agents and Chemotherapy, 61(2), e01998-16. https://doi.org/10.1128/AAC.01998-16 DOI: https://doi.org/10.1128/AAC.01998-16

Friedman, L., & Kolter, R. (2004a). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Molecular Microbiology, 51(3), 675-690 DOI: https://doi.org/10.1046/j.1365-2958.2003.03877.x

Friedman, L., & Kolter, R. (2004b). Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. Journal of Bacteriology, 186(14):4457-4465 DOI: https://doi.org/10.1128/JB.186.14.4457-4465.2004

Fu, W., Forster, T., Mayer, O., Curtin, J. J., Lehman, S. M., & Donlan, R. M. (2010). Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrobial Agents and Chemotherapy, 54(1), 397-404 DOI: https://doi.org/10.1128/AAC.00669-09

Fuqua, C., & Greenberg, E. P. (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nature Reviews Molecular Cell biology, 3(9), 685-695 DOI: https://doi.org/10.1038/nrm907

Gillis, R. J., White, K. G., Choi, K. H., Wagner, V. E., Schweizer, H. P., & Iglewski, B. H. (2005). Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 49(9), 3858-3867 DOI: https://doi.org/10.1128/AAC.49.9.3858-3867.2005

Givskov, M., de Nys, R. O. C. K. Y., Manefield, M., Gram, L., et al. (1996). Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. Journal of Bacteriology, 178(22), 6618-6622 DOI: https://doi.org/10.1128/jb.178.22.6618-6622.1996

Goldman, G., Starosvetsky, J., & Armon, R. (2009). Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. Journal of Membrane Science, 342(1-2), 145-152. DOI: https://doi.org/10.1016/j.memsci.2009.06.036

Gowrishankar, S., Duncun Mosioma, N., & Karutha Pandian, S. (2012). Coral-associated bacteria as a promising antibiofilm agent against methicillin-resistant and-susceptible Staphylococcus aureus biofilms. Evidence-Based Complementary and Alternative Medicine, 2012. https://doi.org/10.1155/2012/862374 DOI: https://doi.org/10.1155/2012/862374

Grandclément, C., Tannières, M., Moréra, S., Dessaux, Y., & Faure, D. (2016). Quorum quenching: role in nature and applied developments. FEMS Microbiology Reviews, 40(1), 86-116 DOI: https://doi.org/10.1093/femsre/fuv038

Gueriri, I., Cyncynatus, C., Dubrac, S., Arana, A. T., Dussurget, O., & Msadek, T. (2008). The DegU orphan response regulator of Listeria monocytogenes autorepresses its own synthesis and is required for bacterial motility, virulence and biofilm formation. Microbiology, 154(8), 2251-2264 DOI: https://doi.org/10.1099/mic.0.2008/017590-0

Ha, D. G., & O'Toole, G. A. (2015). c-di-GMP and its effects on biofilm formation and dispersion: a Pseudomonas aeruginosa review. Microbiology Spectrum, 3(2), 3-2 DOI: https://doi.org/10.1128/microbiolspec.MB-0003-2014

Hall‐Stoodley, L., & Stoodley, P. (2009). Evolving concepts in biofilm infections. Cellular Microbiology, 11(7), 1034-1043 DOI: https://doi.org/10.1111/j.1462-5822.2009.01323.x

Hamilton, H. L., Domínguez, N. M., Schwartz, K. J., Hackett, K. T., & Dillard, J. P. (2005). Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Molecular Microbiology, 55(6), 1704-1721 DOI: https://doi.org/10.1111/j.1365-2958.2005.04521.x

Haruna, Z., Idris, A. H., Muhammad, M. I., Abdulwahab, N. M., Abdullahi, S., & Wada, N. M. (2022). Biofilm forming Enterococci and their Status as Emerging Multidrug Resistant Bacteria. International Journal of Biological, Physical and Chemical Studies, 4(1), 01-06 DOI: https://doi.org/10.32996/ijbpcs.2022.4.1.1

Heurlier, K., Dénervaud, V., Pessi, G., Reimmann, C., & Haas, D. (2003). Negative control of quorum sensing by RpoN (σ54) in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 185(7), 2227-2235 DOI: https://doi.org/10.1128/JB.185.7.2227-2235.2003

Hiblot, J., Gotthard, G., Chabriere, E., & Elias, M. (2012). Structural and enzymatic characterization of the lactonase sis lac from Sulfolobus islandicus. https://doi.org/10.1371/journal.pone.0047028 DOI: https://doi.org/10.1371/journal.pone.0047028

Hornby, J. M., Jensen, E. C., Lisec, A. D., Tasto, J. J., et al. (2001). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Applied and Environmental Microbiology, 67(7), 2982-2992 DOI: https://doi.org/10.1128/AEM.67.7.2982-2992.2001

Hu, H., He, J., Liu, J., Yu, H., Tang, J., & Zhang, J. (2016). Role of N-acyl-homoserine lactone (AHL) based quorum sensing on biofilm formation on packing media in wastewater treatment process. Rsc Advances, 6(14), 11128-11139 DOI: https://doi.org/10.1039/C5RA23466B

Huang, J. J., Han, J. I., Zhang, L. H., & Leadbetter, J. R. (2003). Utilization of acyl-homoserine lactone quorum signals for growth by a soil Pseudomonas and Pseudomonas aeruginosa PAO1. Applied and Environmental Microbiology, 69(10), 5941-5949 DOI: https://doi.org/10.1128/AEM.69.10.5941-5949.2003

Huber, B., Riedel, K., Hentzer, M., Heydorn, A., et al. (2001). The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology, 147(9), 2517-2528 DOI: https://doi.org/10.1099/00221287-147-9-2517

Ivanova, K., Fernandes, M. M., Francesko, A., Mendoza, E., et al. (2015b). Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS applied materials & interfaces, 7(49), 27066-27077 DOI: https://doi.org/10.1021/acsami.5b09489

Ivanova, K., Fernandes, M. M., Mendoza, E., & Tzanov, T. (2015a). Enzyme multilayer coatings inhibit Pseudomonas aeruginosa biofilm formation on urinary catheters. Applied Microbiology and Biotechnology, 99(10), 4373-4385 DOI: https://doi.org/10.1007/s00253-015-6378-7

Jefferson, K. K. (2004). What drives bacteria to produce a biofilm?. FEMS Microbiology Letters, 236(2), 163-173 DOI: https://doi.org/10.1111/j.1574-6968.2004.tb09643.x

Jefferson, K. K., Pier, D. B., Goldmann, D. A., & Pier, G. B. (2004). The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. Journal of Bacteriology, 186(8), 2449-2456 DOI: https://doi.org/10.1128/JB.186.8.2449-2456.2004

Jenal, U., Reinders, A., & Lori, C. (2017). Cyclic di-GMP: second messenger extraordinaire. Nature Reviews Microbiology, 15(5), 271-284 DOI: https://doi.org/10.1038/nrmicro.2016.190

Jensen, P. Ø., Bjarnsholt, T., Phipps, R., Rasmussen, T. B., et al. (2007). Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology, 153(5), 1329-1338 DOI: https://doi.org/10.1099/mic.0.2006/003863-0

Jordan, S. J., Perni, S., Glenn, S., Fernandes, I., et al. (2008). Listeria monocytogenes biofilm-associated protein (BapL) may contribute to surface attachment of L. monocytogenes but is absent from many field isolates. Applied and Environmental Microbiology, 74(17), 5451-5456 DOI: https://doi.org/10.1128/AEM.02419-07

Kalia, V. C., Raju, S. C., & Purohit, H. J. (2011). Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and-lactonase. The Open Microbiology Journal, 5, 1. https://dx.doi.org/ 10.2174%2F1874285801105010001

Kalpana, B. J., Aarthy, S., & Pandian, S. K. (2012). Antibiofilm activity of α-amylase from Bacillus subtilis S8-18 against biofilm forming human bacterial pathogens. Applied Biochemistry and Biotechnology, 167(6), 1778-1794 DOI: https://doi.org/10.1007/s12010-011-9526-2

Kaplan, J. Á. (2010). Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. Journal of Dental Research, 89(3), 205-218 DOI: https://doi.org/10.1177/0022034509359403

Kaplan, J. B., Meyenhofer, M. F., & Fine, D. H. (2003a). Biofilm growth and detachment of Actinobacillus actinomycetemcomitans, 185 (4), https://doi.org/10.1128/JB.185.4.1399-1404.2003 DOI: https://doi.org/10.1128/JB.185.4.1399-1404.2003

Kaplan, J. B., Ragunath, C., Ramasubbu, N., & Fine, D. H. (2003b). Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β-hexosaminidase activity. Journal of Bacteriology, 185(16), 4693-4698 DOI: https://doi.org/10.1128/JB.185.16.4693-4698.2003

Karatan, E., & Watnick, P. (2009). Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiology and Molecular Biology Reviews, 73(2), 310-347 DOI: https://doi.org/10.1128/MMBR.00041-08

Kaur, J., & Yogalakshmi, K. N. (2022). Degradation of n-hexanoyl homoserine lactone with quorum quenching bacteria immobilised magnetic nanocomposite beads. Environmental Technology, 43(6), 885-892 DOI: https://doi.org/10.1080/09593330.2020.1811389

Kırmusaoğlu, S. (2016). Staphylococcal biofilms: Pathogenicity, mechanism and regulation of biofilm formation by quorum sensing system and antibiotic resistance mechanisms of biofilm embedded microorganisms. Microbial biofilms: importance and applications. IntechOpen, 189-209. DOI: https://doi.org/10.5772/62943

Kokai-Kun, J. F., Chanturiya, T., & Mond, J. J. (2009). Lysostaphin eradicates established Staphylococcus aureus biofilms in jugular vein catheterized mice. Journal of Antimicrobial Chemotherapy, 64(1), 94-100 DOI: https://doi.org/10.1093/jac/dkp145

Lade, H., Paul, D., & Kweon, J. H. (2014). Quorum quenching mediated approaches for control of membrane biofouling. International Journal of Biological Sciences, 10(5), 550. DOI: https://doi.org/10.7150/ijbs.9028

LaSarre, B., & Federle, M. J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiology and Molecular Biology Reviews, 77(1), 73-111 DOI: https://doi.org/10.1128/MMBR.00046-12

Lebeaux, D., & Ghigo, J. M. (2012). Infections associées aux biofilms-Quelles perspectives thérapeutiques issues de la recherche fondamentale?. Médecine/sciences, 28(8-9), 727-739 DOI: https://doi.org/10.1051/medsci/2012288015

Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013). From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens, 2(2), 288-356 DOI: https://doi.org/10.3390/pathogens2020288

Leid, J. G., Willson, C. J., Shirtliff, M. E., Hassett, D. J., Parsek, M. R., & Jeffers, A. K. (2005). The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. The Journal of Immunology, 175(11), 7512-7518 DOI: https://doi.org/10.4049/jimmunol.175.11.7512

Lemon, K. P., Higgins, D. E., & Kolter, R. (2007). Flagellar motility is critical for Listeria monocytogenes biofilm formation. Journal of Bacteriology, 189(12), 4418-4424 DOI: https://doi.org/10.1128/JB.01967-06

Lewis, K. (2001). Riddle of biofilm resistance. Antimicrobial Agents and Chemotherapy, 45(4), 999-1007 DOI: https://doi.org/10.1128/AAC.45.4.999-1007.2001

Liu, N., Yu, M., Zhao, Y., Cheng, J., An, K., & Zhang, X. H. (2017). PfmA, a novel quorum-quenching N-acylhomoserine lactone acylase from Pseudoalteromonas flavipulchra. Microbiology, 163(10), 1389-1398 DOI: https://doi.org/10.1099/mic.0.000535

Liu, P., Chen, Y., Shao, Z., Chen, J., et al. (2019). AhlX, an N-acylhomoserine lactonase with unique properties. Marine Drugs, 17(7), 387 DOI: https://doi.org/10.3390/md17070387

Loo, C. Y. (2003). Oral streptococcal genes that encode biofilm formation. Medical implications of biofilms, 1, 212-227. DOI: https://doi.org/10.1017/CBO9780511546297.010

Lu, L., Li, M., Yi, G., Liao, L., et al. (2021). Screening strategies for quorum sensing inhibitors in combating bacterial infection. Journal of Pharmaceutical Analysis, 12(1), 1-4. https://doi.org/10.1016/j.jpha.2021.03.009 DOI: https://doi.org/10.1016/j.jpha.2021.03.009

Lu, T. K., & Collins, J. J. (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proceedings of the National Academy of Sciences, 104(27), 11197-11202 DOI: https://doi.org/10.1073/pnas.0704624104

Lynch, D. J., Fountain, T. L., Mazurkiewicz, J. E., & Banas, J. A. (2007). Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiology Letters, 268(2), 158-165 DOI: https://doi.org/10.1111/j.1574-6968.2006.00576.x

Ma, L., Conover, M., Lu, H., Parsek, M. R., Bayles, K., & Wozniak, D. J. (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathogens, 5(3), e1000354. https://doi.org/10.1371/journal.ppat.1000354 DOI: https://doi.org/10.1371/journal.ppat.1000354

Ma, L., Wang, J., Wang, S., Anderson, E. M., et al. (2012). Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post‐transcriptionally regulated. Environmental Microbiology, 14(8), 1995-2005 DOI: https://doi.org/10.1111/j.1462-2920.2012.02753.x

Madsen, J. S., Burmølle, M., Hansen, L. H., & Sørensen, S. J. (2012). The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunology & Medical Microbiology, 65(2), 183-195 DOI: https://doi.org/10.1111/j.1574-695X.2012.00960.x

Mai-Prochnow, A., Lucas-Elio, P., Egan, S., Thomas, T., et al. (2008). Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria. Journal of Bacteriology, 190(15), 5493-5501 DOI: https://doi.org/10.1128/JB.00549-08

Mayer, C., Romero, M., Muras, A., & Otero, A. (2015). Aii20J, a wide-spectrum thermostable N-acylhomoserine lactonase from the marine bacterium Tenacibaculum sp. 20J, can quench AHL-mediated acid resistance in Escherichia coli. Applied Microbiology and Biotechnology, 99(22), 9523-9539 DOI: https://doi.org/10.1007/s00253-015-6741-8

Meschwitz, S. M., Teasdale, M. E., Mozzer, A., Martin, N., et al. (2019). Antagonism of quorum sensing phenotypes by analogs of the marine bacterial secondary metabolite 3-methyl-N-(2′-phenylethyl)-butyramide. Marine Drugs, 17(7), 389 DOI: https://doi.org/10.3390/md17070389

Möker, N., Dean, C. R., & Tao, J. (2010). Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. Journal of Bacteriology, 192(7), 1946-1955 DOI: https://doi.org/10.1128/JB.01231-09

Morgan, R., Kohn, S., Hwang, S. H., Hassett, D. J., & Sauer, K. (2006). BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. Journal of Bacteriology, 188(21), 7335-7343 DOI: https://doi.org/10.1128/JB.00599-06

Morohoshi, T., Nakazawa, S., Ebata, A., Kato, N., & Ikeda, T. (2008). Identification and characterization of N-acylhomoserine lactone-acylase from the fish intestinal Shewanella sp. strain MIB015. Bioscience, Biotechnology, and Biochemistry, 72(7), 1887-1893 DOI: https://doi.org/10.1271/bbb.80139

Newell, P. D., Monds, R. D., & O'Toole, G. A. (2009). LapD is a bis-(3′, 5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0–1. Proceedings of the National Academy of Sciences, 106(9), 3461-3466 DOI: https://doi.org/10.1073/pnas.0808933106

Ng, F. S., Wright, D. M., & Seah, S. Y. (2011). Characterization of a phosphotriesterase-like lactonase from Sulfolobus solfataricus and its immobilization for disruption of quorum sensing. Applied and Environmental Microbiology, 77(4), 1181-1186 DOI: https://doi.org/10.1128/AEM.01642-10

Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., et al. (2011). Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science, 334(6058), 982-986 DOI: https://doi.org/10.1126/science.1211037

Ning, Q., Wang, D., & You, J. (2021). Joint effects of antibiotics and quorum sensing inhibitors on resistance development in bacteria. Environmental Science: Processes & Impacts, 23(7), 995-1005 DOI: https://doi.org/10.1039/D1EM00047K

O'Toole, G., Kaplan, H. B., & Kolter, R. (2000). Biofilm formation as microbial development. Annual Reviews in Microbiology, 54(1), 49-79 DOI: https://doi.org/10.1146/annurev.micro.54.1.49

Pamp, S. J., & Tolker-Nielsen, T. (2007). Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. Journal of Bacteriology, 189(6), 2531-2539 DOI: https://doi.org/10.1128/JB.01515-06

Papaioannou, E., Wahjudi, M., Nadal-Jimenez, P., Koch, G., Setroikromo, R., & Quax, W. J. (2009). Quorum-quenching acylase reduces the virulence of Pseudomonas aeruginosa in a Caenorhabditis elegans infection model. Antimicrobial Agents and Chemotherapy, 53(11), 4891-4897 DOI: https://doi.org/10.1128/AAC.00380-09

Pei, R., & Lamas-Samanamud, G. R. (2014). Inhibition of biofilm formation by T7 bacteriophages producing quorum-quenching enzymes. Applied and Environmental Microbiology, 80(17), 5340-5348 DOI: https://doi.org/10.1128/AEM.01434-14

Pires, D. P., Dötsch, A., Anderson, E. M., Hao, Y., et al. (2017). A genotypic analysis of five P. aeruginosa strains after biofilm infection by phages targeting different cell surface receptors. Frontiers in Microbiology, 8, 1229 DOI: https://doi.org/10.3389/fmicb.2017.01229

Prigent‐Combaret, C., Prensier, G., Le Thi, T. T., Vidal, O., Lejeune, P., & Dorel, C. (2000) Developmental pathway for biofilm formation in curli‐producing Escherichia coli strains: role of flagella, curli and colanic acid. Environmental Microbiology, 2(4), 450-464 DOI: https://doi.org/10.1046/j.1462-2920.2000.00128.x

Purevdorj-Gage, B., Costerton, W. J., & Stoodley, P. (2005). Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology, 151(5), 1569-1576 DOI: https://doi.org/10.1099/mic.0.27536-0

Rabin, N., Zheng, Y., Opoku-Temeng, C., Du, Y., Bonsu, E., & Sintim, H. O. (2015). Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Medicinal Chemistry, 7 (4): 493–512 DOI: https://doi.org/10.4155/fmc.15.6

Rajasekharan, S. K., & Ramesh, S. (2013). Cellulase inhibits Burkholderia cepacia biofilms on diverse prosthetic materials. Polish Journal of Microbiology, 62(3), 327-330 DOI: https://doi.org/10.33073/pjm-2013-044

Reina, J. C., Pérez, P., & Llamas, I. (2022). Quorum Quenching Strains Isolated from the Microbiota of Sea Anemones and Holothurians Attenuate Vibrio corallilyticus Virulence Factors and Reduce Mortality in Artemia salina. Microorganisms, 10(3), 631 DOI: https://doi.org/10.3390/microorganisms10030631

Reina, J. C., Romero, M., Salto, R., Cámara, M., & Llamas, I. (2021). AhaP, A Quorum Quenching Acylase from Psychrobacter sp. M9-54-1 That Attenuates Pseudomonas aeruginosa and Vibrio coralliilyticus Virulence. Marine drugs, 19(1), 16 DOI: https://doi.org/10.3390/md19010016

Reina, J. C., Torres, M., & Llamas, I. (2019). Stenotrophomonas maltophilia AHL-degrading strains isolated from marine invertebrate microbiota attenuate the virulence of Pectobacterium carotovorum and Vibrio coralliilyticus. Marine Biotechnology, 21(2), 276-290 DOI: https://doi.org/10.1007/s10126-019-09879-w

Rémy, B., Plener, L., Poirier, L., Elias, M., Daudé, D., & Chabrière, E. (2016). Harnessing hyperthermostable lactonase from Sulfolobus solfataricus for biotechnological applications. Scientific reports, 6(1), 1-11 DOI: https://doi.org/10.1038/srep37780

Ren, D., Sims, J. J., & Wood, T. K. (2001). Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)‐4‐bromo‐5‐(bromomethylene)‐3‐butyl‐2 (5H)‐furanone. Environmental Microbiology, 3(11), 731-736 DOI: https://doi.org/10.1046/j.1462-2920.2001.00249.x

Romero, D., Aguilar, C., Losick, R., & Kolter, R. (2010). Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proceedings of the National Academy of Sciences, 107(5), 2230-2234 DOI: https://doi.org/10.1073/pnas.0910560107

Romero, M., Muras, A., Mayer, C., Buján, N., Magariños, B., & Otero, A. (2014). In vitro quenching of fish pathogen Edwardsiella tarda AHL production using marine bacterium Tenacibaculum sp. strain 20J cell extracts. Diseases of Aquatic Organisms, 108(3), 217-225 DOI: https://doi.org/10.3354/dao02697

Saggu, S. K., Jha, G., & Mishra, P. C. (2019). Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10. Frontiers in Bioengineering and Biotechnology, 192. https://doi.org/10.3389/fbioe.2019.00192 DOI: https://doi.org/10.1101/655092

Sakuragi, Y., & Kolter, R. (2007). Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. Journal of Bacteriology, 189(14), 5383-5386 DOI: https://doi.org/10.1128/JB.00137-07

Santhakumari, S., Jayakumar, R., Logalakshmi, R., Prabhu, N. M., et al. (2018). In vitro and in vivo effect of 2, 6-Di-tert-butyl-4-methylphenol as an antibiofilm agent against quorum sensing mediated biofilm formation of Vibrio spp. International Journal of Food Microbiology, 281, 60-71 DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.05.024

Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., & Davies, D. G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Journal of Bacteriology, 184(4), https://doi.org/10.1128/jb.184.4.1140-1154.2002 DOI: https://doi.org/10.1128/jb.184.4.1140-1154.2002

Savage, V. J., Chopra, I., & O’Neill, A. J. (2013). Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial Agents and Chemotherapy, 57(4), https://doi.org/10.1128/AAC.02008-12 DOI: https://doi.org/10.1128/AAC.02008-12

Simm, R., Morr, M., Kader, A., Nimtz, M., & Römling, U. (2004). GGDEF and EAL domains inversely regulate cyclic di‐GMP levels and transition from sessility to motility. Molecular Microbiology, 53(4), 1123-1134 DOI: https://doi.org/10.1111/j.1365-2958.2004.04206.x

Small, H. J., & Pagenkopp, K. M. (2011). Reservoirs and alternate hosts for pathogens of commercially important crustaceans: a review. Journal of Invertebrate Pathology, 106(1), 153-164 DOI: https://doi.org/10.1016/j.jip.2010.09.016

Stewart, P. S., & Costerton, J. W. (2001). Antibiotic resistance of bacteria in biofilms. The Lancet, 358(9276), 135-138 DOI: https://doi.org/10.1016/S0140-6736(01)05321-1

Sun, S., Dai, X., Sun, J., Bu, X., et al. (2016). A diketopiperazine factor from Rheinheimera aquimaris QSI02 exhibits anti-quorum sensing activity. Scientific reports, 6(1), 1-10 DOI: https://doi.org/10.1038/srep39637

Sutrina, S. L., Callender, S., Grazette, T., Scantlebury, P., et al. (2019). The quantity and distribution of biofilm growth of Escherichia coli strain ATCC 9723 depends on the carbon/energy source. Microbiology, 165(1), 47-64 DOI: https://doi.org/10.1099/mic.0.000745

Sutrina, S. L., Daniel, K., Lewis, M., Charles, N. T., Anselm, C. K., & Holder, N. (2015). Biofilm growth of Escherichia coli is subject to cAMP-dependent and cAMP-independent inhibition. Microbial Physiology, 25(2-3), 209-225 DOI: https://doi.org/10.1159/000375498

Swift, S., Downie, A. J., Whitehead, N. A., Barnard, A. M., Salmond, G.P., Williams, Quorum, P. (2001) Sensing as a population-density dependent determinant of bacterial physiology. Advances in Microbial Physiology, 45, 199-270 DOI: https://doi.org/10.1016/S0065-2911(01)45005-3

Taghadosi, R., Shakibaie, M. R., & Masoumi, S. (2015). Biochemical detection of N-Acyl homoserine lactone from biofilm-forming uropathogenic Escherichia coli isolated from urinary tract infection samples. Reports of Biochemistry & Molecular Biology, 3(2), 56

Tan, D., Zhang, Y., Cheng, M., Le, S., et al. (2019). Characterization of Klebsiella pneumoniae ST11 isolates and their interactions with lytic phages. Viruses, 11(11), 1080 DOI: https://doi.org/10.3390/v11111080

Taylor, C. M., Beresford, M., Epton, H. A., Sigee, D. C., et al. (2002). Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. Journal of Bacteriology, 184(3), 621-628 DOI: https://doi.org/10.1128/JB.184.3.621-628.2002

Teasdale, M. E., Liu, J., Wallace, J., Akhlaghi, F., & Rowley, D. C. (2009). Secondary metabolites produced by the marine bacterium Halobacillus salinus that inhibit quorum sensing-controlled phenotypes in gram-negative bacteria. Applied and Environmental Microbiology, 75(3), 567-572 DOI: https://doi.org/10.1128/AEM.00632-08

Thenmozhi, R., Nithyanand, P., Rathna, J., & Karutha Pandian, S. (2009). Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunology & Medical Microbiology, 57(3), 284-294 DOI: https://doi.org/10.1111/j.1574-695X.2009.00613.x

Thormann, K. M., Saville, R. M., Shukla, S., & Spormann, A. M. (2005). Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. Journal of Bacteriology, 187(3), 1014-1021 DOI: https://doi.org/10.1128/JB.187.3.1014-1021.2005

Todhanakasem, T., & Young, G. M. (2008). Loss of flagellum-based motility by Listeria monocytogenes results in formation of hyperbiofilms. Journal of Bacteriology, 190(17), 6030-6034 DOI: https://doi.org/10.1128/JB.00155-08

Torres, M., Romero, M., Prado, S., Dubert, J., Tahrioui, A., Otero, A., & Llamas, I. (2013). N-acylhomoserine lactone-degrading bacteria isolated from hatchery bivalve larval cultures. Microbiological research, 168(9), 547-554 DOI: https://doi.org/10.1016/j.micres.2013.04.011

Torres, M., Rubio-Portillo, E., Antón, J., Ramos-Esplá, A. A., Quesada, E., & Llamas, I. (2016). Selection of the N-acylhomoserine lactone-degrading bacterium Alteromonas stellipolaris PQQ-42 and of its potential for biocontrol in aquaculture. Frontiers in Microbiology, 7, 646 DOI: https://doi.org/10.3389/fmicb.2016.00646

Uroz, S., Chhabra, S. R., Camara, M., Williams, P., Oger, P., & Dessaux, Y. (2005). N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology, 151(10), 3313-3322 DOI: https://doi.org/10.1099/mic.0.27961-0

Vallet, I., Olson, J. W., Lory, S., Lazdunski, A., & Filloux, A. (2001). The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proceedings of the National Academy of Sciences, 98(12), 6911-6916 DOI: https://doi.org/10.1073/pnas.111551898

Van Acker, H., Van Dijck, P., & Coenye, T. (2014). Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends in Microbiology, 22(6), 326-333 DOI: https://doi.org/10.1016/j.tim.2014.02.001

Verma, V., Harjai, K., & Chhibber, S. (2009). Restricting ciprofloxacin-induced resistant variant formation in biofilm of Klebsiella pneumoniae B5055 by complementary bacteriophage treatment. Journal of Antimicrobial Chemotherapy, 64(6), 1212-1218 DOI: https://doi.org/10.1093/jac/dkp360

Vinoj, G., Vaseeharan, B., Thomas, S., Spiers, A. J., & Shanthi, S. (2014). Quorum-quenching activity of the AHL-lactonase from Bacillus licheniformis DAHB1 inhibits Vibrio biofilm formation in vitro and reduces shrimp intestinal colonisation and mortality. Marine Biotechnology, 16(6), 707-715 DOI: https://doi.org/10.1007/s10126-014-9585-9

Walters III, M. C., Roe, F., Bugnicourt, A., Franklin, M. J., & Stewart, P. S. (2003). Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrobial agents and Chemotherapy, 47(1), 317-323 DOI: https://doi.org/10.1128/AAC.47.1.317-323.2003

Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology 21, 319-346 DOI: https://doi.org/10.1146/annurev.cellbio.21.012704.131001

Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J., & Salmond, G. P. (2001). Quorum-sensing in Gram-negative bacteria. FEMS Microbiology Reviews, 25(4), 365-404 DOI: https://doi.org/10.1111/j.1574-6976.2001.tb00583.x

Williams, P., Winzer, K., Chan, W. C., & Camara, M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1483), 1119-1134 DOI: https://doi.org/10.1098/rstb.2007.2039

Yildiz, F. H., & Visick, K. L. (2009). Vibrio biofilms: so much the same yet so different. Trends in Microbiology, 17(3), 109-118 DOI: https://doi.org/10.1016/j.tim.2008.12.004

You, J., Xue, X., Cao, L., Lu, X., et al. (2007). Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Applied Microbiology and Biotechnology, 76(5), 1137-1144 DOI: https://doi.org/10.1007/s00253-007-1074-x

Zhang, J. W., Xuan, C. G., Lu, C. H., Guo, S., et al. (2019). AidB, a novel thermostable N-acylhomoserine lactonase from the bacterium Bosea sp. Applied and Environmental microbiology, 85(24), e02065-19 DOI: https://doi.org/10.1128/AEM.02065-19

Zhang, L., & Mah, T. F. (2008). Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. Journal of Bacteriology, 190(13), 4447-4452 DOI: https://doi.org/10.1128/JB.01655-07