EVALUATION OF QUORUM SENSING SIGNALS OF STRONG BIOFILM PRODUCING BACTERIA VIA LC-MSMS, HPLC AND BIOSENSORS
Year 2023,
, 23 - 30, 15.10.2023
Dilvin İpek
Abstract
This study aimed to show presence of Quorum Sensing (QS) signals of Gram-negative and Gram-positive biofilm producing bacteria isolated from real dairy process lines. Defining the profile and chemical composition of QS-signals is an important factor in control of microbial resistance and biofilm production. We especially focused on unusual behaviour of Gram-positive and Gram-negative isolates. Long-chain acyl-homoserine lactones (AHLs) signals (C14-HSL, C16-HSL and C18-HSL) and DFD (4,5-dihidroksi-2,3-pentanedione)-AI-2 signals of the isolates were studied by High-performance liquid chromatography (HPLC) and Liquid Chromatography with tandem mass spectrometry (LC-MSMS) methods. All Gram-positive isolates were defined as AHL-producers. All Gram-negative isolates, formerly defined as non-AHL producers by both biosensors and HPLC methods, were identified as AHL-producers. DFD signal was only detected from Gram-negative Klebsiella pneumonia, Enterobacter cloacae and Klebsiella oxytoca isolates. The results demonstrated that the QS-system is a complex system and biosensor microorganism may not be the best method for QS-signal identification. The results also provided new insights in defining the profile and chemical composition of QS-signals importance for interrupting the chemical communication completely to reduce biofilm formation and prevent resistance gain of microorganisms.
Supporting Institution
Scientific Research Project Commission of Çanakkale Onsekiz Mart University
Project Number
FBA-2018-1438
Thanks
I am thankful to Assoc.Prof.Dr. Nükhet N. Demirel Zorba’s laboratory members for their kind support, Food Engineering Department, Çanakkale Onsekiz Mart University, Çanakkale, Turkey. I am also thankful to Çanakkale Onsekiz Mart University Science and Technology Application and Research Center, Çanakkale Onsekiz Mart University, Çanakkale, Turkey for their cooperation in LC-MSMS study. I express my sincere thanks to Prof.Dr. Ji Hyang Kweon and Assist. Prof.Dr. Harshade Lade and their research team, Water Treatment and Membrane Laboratory, Department of Environmental Engineering, Konkuk University, Seoul, Korea for their kind cooperation in HPLC study.
References
- 1. Abbondio, M., Fois, I., Longheu, C., Azara, E. & Tola, S. 2019. Biofilm production, quorum sensing system and analysis of virulence factors of Staphylococcus epidermidis collected from sheep milk samples. Small Ruminant Research, 174, 83-87.
https://doi.org/10.1016/j.smallrumres.2019.03.017
- 2. Almasoud, A., Hettiarachchy, N., Rayaprolu. S., Babu, D., Kwon, Y.M. & Mauromoustakos, A. 2016. Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157: H7 and Salmonella typhimurium. LWT-Food Science and Technology, 66, 560-564.
https://doi.org/10.1016/j.lwt.2015.11.013
- 3. Barriuso, J., Ramos Solano, B., Fray, R.G., Cámara, M., Hartmann, A. & Gutiérrez Mañero, F.J. 2008. Transgenic tomato plants alter quorum sensing in plant growth‐promoting rhizobacteria. Plant Biotechnology Journal, 6(5): 442-452. https://doi.org/10.1111/j.1467-7652.2008.00331.x
- 4. Biswa, P. & Doble, M. 2013. Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiology Letters, 343(1): 34-41. https://doi.org/10.1111/1574-6968.12123
- 5. Churchill, M.E., Sibhatu, H.M. & Uhlson, C.L. 2011. Defining the structure and function of acyl-homoserine lactone autoinducers. pp. 159-171. In: Rumbaugh, K.P. (ed). Quorum Sensing Methods and Protocols, New Jersey: Humana Press, 315 pp. https://doi.org/10.1007/978-1-60761-971-0_12
- 6. Duanis-Assaf, D., Steinberg, D., Chai, Y. & Shemesh, M. 2016. The LuxS based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Frontiers in Microbiology, 6, 1517.
https://doi.org/10.3389/fmicb.2015.01517
- 7. Federle, M.J. & Bassler, B.L. 2003. Interspecies communication in bacteria. The Journal of clinical investigation, 112(9): 1291-1299.
https://doi.org/10.1172/JCI20195
- 8. Haslan, E. & Kimiran-Erdem, A. 2013. Investigation of N-acyl homoserine lactone (AHL) molecule production in Gram-negative bacteria isolated from cooling tower water and biofilm samples. Folia Microbiologica, 58(5): 349-360. https://doi.org/10.1007/s12223-012-0216-4
- 9. Highlander, S.K., Hultén, K.G., Qin, X., Jiang, H., Yerrapragada, S., Mason, E.O. & Igboeli, O. 2007. Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiology, 7(1): 99. https://doi.org/10.1186/1471-2180-7-99
- 10. Hong, K.W., Koh, C.L., Sam, C.K., Yin, W.F. & Chan, K.G. 2012. Quorum quenching revisited from signal decays to signaling confusion. Sensors 12(4): 4661-4696. https://doi.org/10.3390/s120404661
- 11. How, K.Y., Hong, K.W. & Chan, K.G. 2015. Whole genome sequencing enables the characterization of BurI, a LuxI homologue of Burkholderia epacian strain GG4. PeerJ., 3, e1117. https://doi.org/10.7717/peerj.1117
- 12. İpek, D. 2017. Applicability of Ezine Cheese Process Lines Disinfection By New Disinfectant Formulas: Antibiofilm-Antiquorum Sensing Agents [dissertation]. Çanakkale: Çanakkale Onsekiz Mart University. 195pp.
- 13. İpek, D. & Zorba, N.N. 2016. Ezine Peyniri Üretim Hattında Pseudomonas spp, Bacillus spp., Enterobacteriacea spp.ve Listeria spp.’nin Biofilm Oluşturma Kapasitesi (FBA-2014-332). Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırmalar Koordinasyon Birimi. 30 pp.
- 14. İpek, D. & Zorba, N.N. 2017. Ezine Peyniri Üretim Hattında Dezenfeksiyonun Yeni Teknolojiler ile Yapılabilirliği: Antibiofilm-Antiquorum Sensing Maddeler (FDK-2016-908). Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırmalar Koordinasyon Birimi. 40 pp.
- 15. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M., Alloni, G.O., Azevedo, V. & Borriss, R. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature, 390(6657): 249-256. https://doi.org/10.1038/36786
- 16. Lade, H., Paul, D. & Kweon, J. 2014. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. International Journal of Molecular Sciences, 15(2): 2255-2273. https://doi.org/10.3390/ijms15022255
- 17. Mesa, R., Kabir, A., Samanidou, V. & Furton, K.G. 2019. Simultaneous determination of selected estrogenic endocrine disrupting chemicals and bisphenol A residues in whole milk using fabric phase sorptive extraction coupled to HPLC‐UV detection and LC‐MSMS. Journal of Separation Science, 42(2): 598-608. https://doi.org/10.1002/jssc.201800901
- 18. Mizan, M.F.R., Jahid, I.K., Kim, M., Lee, K.H., Kim, T.J. & Ha, S.D. 2016. Variability in biofilm formation correlates with hydrophobicity and quorum sensing among Vibrio parahaemolyticus isolates from food contact surfaces and the distribution of the genes involved in biofilm formation. Biofouling, 32(4): 497-509. https://doi.org/10.1080/08927014.2016.1149571
- 19. Naik, M.M., Bhangui, P. & Bhat, C. 2017. The First report on Listeria monocytogenes producing siderophores and responds positively to N-acyl homoserine lactone (AHL) molecules by enhanced biofilm formation. Archives of Microbiology, 199(10):1409-1415.
https://doi.org/10.1007/s00203-017-1416-8
- 20. Naik, M.M., Prabhu, M.S. & Manerikar, V. 2018. Enhanced exopolysaccharide production and biofilm forming ability in methicillin resistant Staphylococcus sciuri isolated from dairy in response to acyl homoserine lactone (AHL). Journal of food science and technology, 55, 2087-2094.
- 21. Niu, C., Clemmer, K.M., Bonomo, R.A. & Rather, P.N. 2008. Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. Journal of Bacteriology, 190(9): 3386-3392.
https://doi.org/10.1128/JB.01929-07
- 22. Patel, N.M., Moore, J. D, Blackwell, H.E. & Amador-Noguez, D. 2016. Identification of unanticipated and novel N-acyl L-homoserine lactones (AHLs) using a sensitive non-targeted LC-MSMS method. PloS One, 11(10): e0163469. https://doi.org/10.1371/journal.pone.0163469
- 23. Püning, C., Su, Y., Lu, X. & Gölz, G. 2021. Molecular mechanisms of Campylobacter biofilm formation and quorum sensing. Current Topics in Microbiology and Immunology, 431, 293-319. https://doi.org/10.1007/978-3-030-65481-8_11
- 24. Qian, M., Zhou, D., Wang, Q., Gao, J., Li, D., Li, Y. & Yang, B. 2019. A reliable, simple and cost-efficient TLC-HPLC method for simultaneously determining florfenicol and florfenicol amine in porcine urine: application to residue surveillance. Food Additives & Contaminants Part A, 1-10. https://doi.org/10.1080/19440049.2019.1627004
- 25. Rajput, A. & Kumar, M. 2017. In silico analyses of conservational, functional and phylogenetic distribution of the LuxI and LuxR homologs in Gram-positive bacteria. Scientific Reports, 7(1): 6969. https://doi.org/10.1038/s41598-017-07241-5
- 26. Saurav, K., Burgsdorf, I., Teta, R., Esposito, G., Bar‐Shalom, R., Costantino, V. & Steindler, L. 2016. Isolation of Marine Paracoccus sp. Ss63 from the Sponge Sarcotragus sp. and Characterization of its Quorum‐Sensing Chemical‐Signaling Molecules by LC‐MSMS Analysis. Israel Journal of Chemistry, 56(5): 330-340. https://doi.org/10.1002/ijch.201600003
- 27. Shih, P.C. & Huang, C.T. 2002. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. Journal of Antimicrobial Chemotherapy, 49(2): 309-314.
https://doi.org/10.1093/jac/49.2.309
- 28. Steindler, L. & Venturi, V. 2007. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiology Letters, 266(1): 1-9. https://doi.org/10.1111/j.1574-6968.2006.00501.x
- 29. Suntharalingam, P. & Cvitkovitch, D.G. 2005. Quorum sensing in streptococcal biofilm formation. Trends in Microbiology, 13(1): 3-6.
https://doi.org/10.1016/j.tim.2004.11.009
- 30. Tang, K., Zhang, Y., Yu, M., Shi, X., Coenye, T., Bossier, P. & Zhang, X.H. 2013. Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Scientific Reports, 3, 2935. https://doi.org/10.1038/srep02935
- 31. Verbeke, F., De Craemer, S., Debunne, N., Janssens, Y., Wynendaele, E., Van de Wiele, C. & De Spiegeleer, B. 2017. Peptides as quorum sensing molecules: measurement techniques and obtained levels in vitro and in vivo. Frontiers in Neuroscience, 11, 183.
https://doi.org/10.3389/fnins.2017.00183
- 32. Wang, Y., Bian, Z., & Wang, Y. 2022. Biofilm formation and inhibition mediated by bacterial quorum sensing. Applied Microbiology and Biotechnology, 106(19-20): 6365-6381. https://doi.org/10.1007/s00253-022-12150-3
- 33. Xu, F., Song, X., Cai, P., Sheng, G. & Yu, H. 2017. Quantitative determination of AI-2 quorum-sensing signal of bacteria using high performance liquid chromatography–tandem mass spectrometry. Journal of Environmental Sciences, 52, 204-209.
https://doi.org/10.1016/j.jes.2016.04.018
- 34. Zhang, Y., Zheng, L., Wang, S., Zhao, Y., Xu, X., Han, B., & Hu, T. 2022. Quorum sensing bacteria in the phycosphere of hab microalgae and their ecological functions related to cross-kingdom interactions. International Journal of Environmental Research and Public Health, 19(1): 163.
https://doi.org/10.3390/ijerph19010163
- 35. Zhao, A., Zhu, J., Ye, X., Ge, Y. & Li, J. 2016. Inhibition of biofilm development and spoilage potential of Shewanella baltica by quorum sensing signal in cell-free supernatant from Pseudomonas fluorescens. International Journal of Food Microbiology, 230, 73-80. https://doi.org/10.1016/j.ijfoodmicro.2016.04.015
- 36. Zhu, S., Wu, H., Zeng, M., Zunying, L., Zhao, Y. & Dong, S. 2015. Regulation of Spoilage‐Related Activities of Shewanella putrefaciens and Shewanella baltica by an Autoinducer‐2 Analogue,(Z)‐5‐(Bromomethylene) furan‐2 (5H)‐One. Journal of Food Processing and Preservation, 39(6):719-728. https://doi.org/10.1111/jfpp.12281
- 37. Zimmer, B.L., May, A.L., Bhedi, C.D., Dearth, S.P., Prevatte, C.W., Pratte, Z. & Richardson, L.L. 2014. Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLoS One, 9(9): e108541.
Year 2023,
, 23 - 30, 15.10.2023
Dilvin İpek
Abstract
Bu çalışma, süt ürünleri proses hatlarından izole edilen hem Gram-negatif hem de biyofilm üreticisi bakterilerin Quorum Sensing (QS) sinyallerini göstermeyi amaçlamıştır. QS sinyallerinin profilinin ve kimyasal bileşiminin tanımlanması, mikrobiyal direnç gelişimi ve biyofilm oluşumunun kontrolü için önemli bir faktördür. Özellikle Gram-pozitif ve Gram-negatif izolatların olağan dışı davranışlarına odaklanılmıştır. İzolatların uzun zincirli açil-homoserin lakton (AHL) sinyalleri (C14-HSL, C16-HSL ve C18-HSL) ve DFD (4,5-dihidroksi-2,3-pentanedion)-AI-2 sinyalleri yüksek performanslı sıvı kromatografisi (HPLC) ve Tandem kütle spektrometresi ile Sıvı Kromatografisi (LC-MSMS) yöntemleri ile incelenmiştir. Sonuç olarak, tüm Gram-pozitif izolatların olağandışı olarak AHL üreticisi olduğu tespit edilmiştir. Biyosensör ve HPLC yöntemleri ile AHL üreticisi olmadığı tespit edilen Gram-negatif bakteriler, LC-MSMS yöntemi ile AHL üreticileri olarak tanımlandı. Gram-pozitif izolatlar tarafından üretilen DFD sinyali, Gram-negatif izolatlardan Klebsiella pneumonia, Enterobacter cloacae ve Klebsiella oxytoca'da tespit edilmiştir. Sonuçlar, QS sisteminin karmaşık bir sistem olduğunu ve biyosensör mikroorganizmaların QS sinyal tanımlaması için en iyi yöntem olmayabileceğini göstermiştir. Bu çalışma, mikroorganizmaların biyofilm oluşumunu azaltmak ve direnç kazanımını önlemek için kimyasal iletişimi tamamen kesmek adına QS sinyallerinin profilini ve kimyasal bileşimini tanımlama konusunda önemli bir bakış açısı sunmaktadır.
Project Number
FBA-2018-1438
References
- 1. Abbondio, M., Fois, I., Longheu, C., Azara, E. & Tola, S. 2019. Biofilm production, quorum sensing system and analysis of virulence factors of Staphylococcus epidermidis collected from sheep milk samples. Small Ruminant Research, 174, 83-87.
https://doi.org/10.1016/j.smallrumres.2019.03.017
- 2. Almasoud, A., Hettiarachchy, N., Rayaprolu. S., Babu, D., Kwon, Y.M. & Mauromoustakos, A. 2016. Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157: H7 and Salmonella typhimurium. LWT-Food Science and Technology, 66, 560-564.
https://doi.org/10.1016/j.lwt.2015.11.013
- 3. Barriuso, J., Ramos Solano, B., Fray, R.G., Cámara, M., Hartmann, A. & Gutiérrez Mañero, F.J. 2008. Transgenic tomato plants alter quorum sensing in plant growth‐promoting rhizobacteria. Plant Biotechnology Journal, 6(5): 442-452. https://doi.org/10.1111/j.1467-7652.2008.00331.x
- 4. Biswa, P. & Doble, M. 2013. Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiology Letters, 343(1): 34-41. https://doi.org/10.1111/1574-6968.12123
- 5. Churchill, M.E., Sibhatu, H.M. & Uhlson, C.L. 2011. Defining the structure and function of acyl-homoserine lactone autoinducers. pp. 159-171. In: Rumbaugh, K.P. (ed). Quorum Sensing Methods and Protocols, New Jersey: Humana Press, 315 pp. https://doi.org/10.1007/978-1-60761-971-0_12
- 6. Duanis-Assaf, D., Steinberg, D., Chai, Y. & Shemesh, M. 2016. The LuxS based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Frontiers in Microbiology, 6, 1517.
https://doi.org/10.3389/fmicb.2015.01517
- 7. Federle, M.J. & Bassler, B.L. 2003. Interspecies communication in bacteria. The Journal of clinical investigation, 112(9): 1291-1299.
https://doi.org/10.1172/JCI20195
- 8. Haslan, E. & Kimiran-Erdem, A. 2013. Investigation of N-acyl homoserine lactone (AHL) molecule production in Gram-negative bacteria isolated from cooling tower water and biofilm samples. Folia Microbiologica, 58(5): 349-360. https://doi.org/10.1007/s12223-012-0216-4
- 9. Highlander, S.K., Hultén, K.G., Qin, X., Jiang, H., Yerrapragada, S., Mason, E.O. & Igboeli, O. 2007. Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiology, 7(1): 99. https://doi.org/10.1186/1471-2180-7-99
- 10. Hong, K.W., Koh, C.L., Sam, C.K., Yin, W.F. & Chan, K.G. 2012. Quorum quenching revisited from signal decays to signaling confusion. Sensors 12(4): 4661-4696. https://doi.org/10.3390/s120404661
- 11. How, K.Y., Hong, K.W. & Chan, K.G. 2015. Whole genome sequencing enables the characterization of BurI, a LuxI homologue of Burkholderia epacian strain GG4. PeerJ., 3, e1117. https://doi.org/10.7717/peerj.1117
- 12. İpek, D. 2017. Applicability of Ezine Cheese Process Lines Disinfection By New Disinfectant Formulas: Antibiofilm-Antiquorum Sensing Agents [dissertation]. Çanakkale: Çanakkale Onsekiz Mart University. 195pp.
- 13. İpek, D. & Zorba, N.N. 2016. Ezine Peyniri Üretim Hattında Pseudomonas spp, Bacillus spp., Enterobacteriacea spp.ve Listeria spp.’nin Biofilm Oluşturma Kapasitesi (FBA-2014-332). Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırmalar Koordinasyon Birimi. 30 pp.
- 14. İpek, D. & Zorba, N.N. 2017. Ezine Peyniri Üretim Hattında Dezenfeksiyonun Yeni Teknolojiler ile Yapılabilirliği: Antibiofilm-Antiquorum Sensing Maddeler (FDK-2016-908). Çanakkale Onsekiz Mart Üniversitesi Bilimsel Araştırmalar Koordinasyon Birimi. 40 pp.
- 15. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M., Alloni, G.O., Azevedo, V. & Borriss, R. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature, 390(6657): 249-256. https://doi.org/10.1038/36786
- 16. Lade, H., Paul, D. & Kweon, J. 2014. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. International Journal of Molecular Sciences, 15(2): 2255-2273. https://doi.org/10.3390/ijms15022255
- 17. Mesa, R., Kabir, A., Samanidou, V. & Furton, K.G. 2019. Simultaneous determination of selected estrogenic endocrine disrupting chemicals and bisphenol A residues in whole milk using fabric phase sorptive extraction coupled to HPLC‐UV detection and LC‐MSMS. Journal of Separation Science, 42(2): 598-608. https://doi.org/10.1002/jssc.201800901
- 18. Mizan, M.F.R., Jahid, I.K., Kim, M., Lee, K.H., Kim, T.J. & Ha, S.D. 2016. Variability in biofilm formation correlates with hydrophobicity and quorum sensing among Vibrio parahaemolyticus isolates from food contact surfaces and the distribution of the genes involved in biofilm formation. Biofouling, 32(4): 497-509. https://doi.org/10.1080/08927014.2016.1149571
- 19. Naik, M.M., Bhangui, P. & Bhat, C. 2017. The First report on Listeria monocytogenes producing siderophores and responds positively to N-acyl homoserine lactone (AHL) molecules by enhanced biofilm formation. Archives of Microbiology, 199(10):1409-1415.
https://doi.org/10.1007/s00203-017-1416-8
- 20. Naik, M.M., Prabhu, M.S. & Manerikar, V. 2018. Enhanced exopolysaccharide production and biofilm forming ability in methicillin resistant Staphylococcus sciuri isolated from dairy in response to acyl homoserine lactone (AHL). Journal of food science and technology, 55, 2087-2094.
- 21. Niu, C., Clemmer, K.M., Bonomo, R.A. & Rather, P.N. 2008. Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. Journal of Bacteriology, 190(9): 3386-3392.
https://doi.org/10.1128/JB.01929-07
- 22. Patel, N.M., Moore, J. D, Blackwell, H.E. & Amador-Noguez, D. 2016. Identification of unanticipated and novel N-acyl L-homoserine lactones (AHLs) using a sensitive non-targeted LC-MSMS method. PloS One, 11(10): e0163469. https://doi.org/10.1371/journal.pone.0163469
- 23. Püning, C., Su, Y., Lu, X. & Gölz, G. 2021. Molecular mechanisms of Campylobacter biofilm formation and quorum sensing. Current Topics in Microbiology and Immunology, 431, 293-319. https://doi.org/10.1007/978-3-030-65481-8_11
- 24. Qian, M., Zhou, D., Wang, Q., Gao, J., Li, D., Li, Y. & Yang, B. 2019. A reliable, simple and cost-efficient TLC-HPLC method for simultaneously determining florfenicol and florfenicol amine in porcine urine: application to residue surveillance. Food Additives & Contaminants Part A, 1-10. https://doi.org/10.1080/19440049.2019.1627004
- 25. Rajput, A. & Kumar, M. 2017. In silico analyses of conservational, functional and phylogenetic distribution of the LuxI and LuxR homologs in Gram-positive bacteria. Scientific Reports, 7(1): 6969. https://doi.org/10.1038/s41598-017-07241-5
- 26. Saurav, K., Burgsdorf, I., Teta, R., Esposito, G., Bar‐Shalom, R., Costantino, V. & Steindler, L. 2016. Isolation of Marine Paracoccus sp. Ss63 from the Sponge Sarcotragus sp. and Characterization of its Quorum‐Sensing Chemical‐Signaling Molecules by LC‐MSMS Analysis. Israel Journal of Chemistry, 56(5): 330-340. https://doi.org/10.1002/ijch.201600003
- 27. Shih, P.C. & Huang, C.T. 2002. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. Journal of Antimicrobial Chemotherapy, 49(2): 309-314.
https://doi.org/10.1093/jac/49.2.309
- 28. Steindler, L. & Venturi, V. 2007. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiology Letters, 266(1): 1-9. https://doi.org/10.1111/j.1574-6968.2006.00501.x
- 29. Suntharalingam, P. & Cvitkovitch, D.G. 2005. Quorum sensing in streptococcal biofilm formation. Trends in Microbiology, 13(1): 3-6.
https://doi.org/10.1016/j.tim.2004.11.009
- 30. Tang, K., Zhang, Y., Yu, M., Shi, X., Coenye, T., Bossier, P. & Zhang, X.H. 2013. Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Scientific Reports, 3, 2935. https://doi.org/10.1038/srep02935
- 31. Verbeke, F., De Craemer, S., Debunne, N., Janssens, Y., Wynendaele, E., Van de Wiele, C. & De Spiegeleer, B. 2017. Peptides as quorum sensing molecules: measurement techniques and obtained levels in vitro and in vivo. Frontiers in Neuroscience, 11, 183.
https://doi.org/10.3389/fnins.2017.00183
- 32. Wang, Y., Bian, Z., & Wang, Y. 2022. Biofilm formation and inhibition mediated by bacterial quorum sensing. Applied Microbiology and Biotechnology, 106(19-20): 6365-6381. https://doi.org/10.1007/s00253-022-12150-3
- 33. Xu, F., Song, X., Cai, P., Sheng, G. & Yu, H. 2017. Quantitative determination of AI-2 quorum-sensing signal of bacteria using high performance liquid chromatography–tandem mass spectrometry. Journal of Environmental Sciences, 52, 204-209.
https://doi.org/10.1016/j.jes.2016.04.018
- 34. Zhang, Y., Zheng, L., Wang, S., Zhao, Y., Xu, X., Han, B., & Hu, T. 2022. Quorum sensing bacteria in the phycosphere of hab microalgae and their ecological functions related to cross-kingdom interactions. International Journal of Environmental Research and Public Health, 19(1): 163.
https://doi.org/10.3390/ijerph19010163
- 35. Zhao, A., Zhu, J., Ye, X., Ge, Y. & Li, J. 2016. Inhibition of biofilm development and spoilage potential of Shewanella baltica by quorum sensing signal in cell-free supernatant from Pseudomonas fluorescens. International Journal of Food Microbiology, 230, 73-80. https://doi.org/10.1016/j.ijfoodmicro.2016.04.015
- 36. Zhu, S., Wu, H., Zeng, M., Zunying, L., Zhao, Y. & Dong, S. 2015. Regulation of Spoilage‐Related Activities of Shewanella putrefaciens and Shewanella baltica by an Autoinducer‐2 Analogue,(Z)‐5‐(Bromomethylene) furan‐2 (5H)‐One. Journal of Food Processing and Preservation, 39(6):719-728. https://doi.org/10.1111/jfpp.12281
- 37. Zimmer, B.L., May, A.L., Bhedi, C.D., Dearth, S.P., Prevatte, C.W., Pratte, Z. & Richardson, L.L. 2014. Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLoS One, 9(9): e108541.