Responses of bacterial strains isolated from drinking water environments to N-acyl-L-homoserine lactones and their analogs during biofilm formation

Abstract

Often as a result of biofilm formation, drinking water distribution systems (DWDS) are regularly faced with the problem of microbial contamination. Quorum sensing (QS) systems play a marked role in the regulation of microbial biofilm formation; thus, inhibition of QS systems may provide a promising approach to biofilm formation control in DWDS. In the present study, 22 bacterial strains were isolated from drinking water-related environments. The following properties of the strains were investigated: bacterial biofilm formation capacity, QS signal molecule N-acyl-L-homoserine lactones (AHLs) production ability, and responses to AHLs and AHL analogs, 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) and 2(5H)-furanone. Four AHLs were added to developed biofilms at dosages ranging from 0.1nmol·L^-1 to 100 nmol·L^-1. As a result, the biofilm growth of more than 1/4 of the isolates, which included AHL producers and non-producers, were significantly promoted. Further, the biofilm biomasses were closely associated with respective AHLs concentrations. These results provided evidence to support the idea that AHLs play a definitive role in biofilm formation in many of the studied bacteria. Meanwhile, two AHLs analogs demonstrated unexpectedly minimal negative effects on biofilm formation. This suggested that, in order to find an applicable QS inhibition approach for biofilm control in DWDS, the testing and analysis of more analogs is needed.

Keywords

drinking water distribution systems (DWDS) / biofilm / quorum sensing (QS) / N-acyl-L-homoserine lactones (AHLs) / (dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) / 2(5H)-furanone

References

[1] Lechevallier M W, Babcock R M, Lee R G. Examination and characterization of distribution system biofilms. Applied and Environmental Microbiology, 1987, 53(12): 2714–2724

[2] Momba M N B, Kfir R, Venter S N, Cloete T E. An overview of biofilm formation in distribution systems and its impact on the deterioration of water quality. Water SA, 2000, 26(1): 59–66

[3] Van Der Kooij D. Managing regrowth in drinking water distribution systems. In: Bartram J, Cotruvo J, Exner M, Fricker C, Glasmacher A, eds. Heterotrophic Plate Counts and Drinking-Water Safety. 1st ed. London: IWA Publishing, 2003, 199–232

[4] Nagy L A, Olson B H. Occurrence and significance of bacteria, fungi and yeasts associated with distribution pipe surfaces. In: Proceedings of the American Water Works Association, Water Quality Technical Conference 2005. American Water Works Association, Denver, Colo, 1985, 202–207

[5] Critchley M M, Fallowfield H J. The effect of distribution system bacterial biofilms on copper concentrations in drinking water. Water Science and Technology: Water Supply, 2001, 1(4): 247–252

[6] Block J C. Biofilms in drinking water distribution system. In: Melo L F, Bott T R, Fletcher M, Capdeville B, editors. Biofilms—Science and Technology. Dordrecht: Kluwer Academic, 1992, 469–485

[7] Niquette P, Servais P, Savoir R. Impacts of pipe materials on densities of fixed bacterial biomass in a drinking water distribution system. Water Research, 2000, 34(6): 1952–1956

[8] Tsai Y P. Impact of flow velocity on the dynamic behaviour of biofilm bacteria. Biofouling, 2005, 21(5–6): 267–277

[9] Simões L C, Azevedo N, Pacheco A, Keevil C W, Vieira M J. Drinking water biofilm assessment of total and culturable bacteria under different operating conditions. Biofouling, 2006, 22(2): 91–99

[10] Miller M B, Bassler B L. Quorum sensing in bacteria. Annual Review of Microbiology, 2001, 55(1): 165–199

[11] Bassler B L. Small talk: cell-to-cell communication in bacteria. Cell, 2002, 109(4): 421–424

[12] Waters C M, Bassler B L. Quorum sensing: cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 2005, 21(1): 319–346

[13] Parsek M R, Greenberg E P. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(16): 8789–8793

[14] Davies D G, Parsek M R, Pearson J P, Iglewski B H, Costerton J W, Greenberg E P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 1998, 280(5361): 295–298

[15] Baveja J K, Willcox M D P, Hume E B H, Kumar N, Odell R, Poole-Warren L A. Furanones as potential anti-bacterial coatings on biomaterials. Biomaterials, 2004, 25(20): 5003–5012

[16] Dong Y H, Wang L H, Xu J L, Zhang H B, Zhang X F, Zhang L H. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 2001, 411(6839): 813–817

[17] Yeon K, Cheong W, Oh H, Lee W, Hwang B, Lee C, Beyenal H, Lewandowski Z. Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environmental Science & Technology, 2009, 43(2): 380–385

[18] Kappachery S, Paul D, Yoon J, Kweon J H. Vanillin, a potential agent to prevent biofouling of reverse osmosis membrane. Biofouling, 2010, 26(6): 667–672

[19] Rice S A, Koh K S, Queck S Y, Labbate M, Lam K W, Kjelleberg S. Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. Journal of Bacteriology, 2005, 187(10): 3477–3485

[20] Morohoshi T, Shiono T, Takidouchi K, Kato M, Kato N, Kato J, Ikeda T. Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone. Applied and Environmental Microbiology, 2007, 73(20): 6339–6344

[21] Reasoner D J, Geldreich E E. A new medium for the enumeration and subculture of bacteria from potable water. Applied and Environmental Microbiology, 1985, 49(1): 1–7

[22] Gürtler V, Stanisich V A. New approaches to typing and identification of bacteria using the 16S–23S rDNA spacer region. Microbiology, 1996, 142(1): 3–16

[23] Altschul S F, Gish W, Miller W, Myers E W, Lipmanl D J. Basic local alignment search tool. Journal of Molecular Biology, 1990, 215(3): 403–410

[24] Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 2000, 40(2): 175–179

[25] McLean R J C, Pierson L S III, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. Journal of Microbiological Methods, 2004, 58(3): 351–360

[26] Zhu J, Chai Y, Zhong Z, Li S, Winans S C. Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in mesorhizobium huakuii. Applied and Environmental Microbiology, 2003, 69(11): 6949–6953

[27] Kirisits M J, Parsek M R. Does Pseudomonas aeruginosa use intercellular signaling to build biofilm communities? Cellular Microbiology, 2006, 8(12): 1841–1849

[28] Lynch M J, Swift S, Kirke D F, Keevil C W, Dodd C E, Williams P. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environmental Microbiology, 2002, 4(1): 18–28

[29] Tomlin K L, Malott R J, Ramage G, Storey D G, Sokol P A, Ceri H. Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Applied and Environmental Microbiology, 2005, 71(9): 5208–5218

[30] Parsek M R, Greenberg E P. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends in Microbiology, 2005, 13(1): 27–33

[31] Atkinson S, Throup J P, Stewart G S, Williams P. A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Molecular Microbiology, 1999, 33(6): 1267–1277

[32] Hammer B K, Bassler B L. Quorum sensing controls biofilm formation in Vibrio cholera. Molecular Microbiology, 2003, 50(1): 101–104

[33] Zhu J, Mekalanos J J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholera. Developmental Cell, 2003, 5(4): 647–656

[34] Simoes L C, Simoes M, Vieira M J. Influence of the diversity of bacterial isolates from drinking water on the resistance of biofilms to disinfection. Applied and Environmental Microbiology, 2010, 76(19): 6673–6679

[35] Leão R S, Pereira R H V, Ferreira A G, Lima A N, Albano R M, Marques E A. First report of Paenibacillus cineris from a patient with cystic fibrosis. Diagnostic Microbiology and Infectious Disease, 2010, 66(1): 101–103

[36] Kim S, Lee S, Hong S, Oh Y, Seoul M, Kweon J, Kim T. Biofouling of reverse osmosis membranes: microbial quorum sensing and fouling propensity. Desalination, 2009, 247(1–3): 303–315

[37] Ren T T, Yu H Q, Li X Y. The quorum-sensing effect of aerobic granules on bacterial adhesion, biofilm formation, and sludge granulation. Applied Microbiology and Biotechnology, 2010, 88(3): 789–797

[38] Wang H, Cai T, Weng M, Zhou J, Cao H, Zhong Z, Zhu J. Conditional production of acyl-homoserine lactone-type quorum-sensing signals in clinical isolates of enterobacteria. Journal of Medical Microbiology, 2006, 55(12): 1751–1753

[39] O’Toole G A, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm. Molecular Microbiology, 1998, 30(2): 295–304

[40] Pratt L A, Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Molecular Microbiology, 1998, 30(2): 285–293

[41] Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology, 2001, 147(9): 2517–2528

[42] Michael B, Smith J N, Swift S, Heffron F, Ahmer B M. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. Journal of Bacteriology, 2001, 183(19): 5733–5742

[43] Schauder S, Shokat K, Surette M G, Bassler B L. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Molecular Microbiology, 2001, 41(2): 463–476

[44] Rickard A H, Palmer R JBlehert D S, Campagna S R, Semmelhack M F, Egland P G, Bassler B L, Kolenbrander P E. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Molecular Microbiology, 2006, 60(6): 1446–1456

[45] Czajkowski R, Jafra S. Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochimica Polonica, 2009, 56(1): 1–16

[46] Xiong Y, Liu Y. Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Applied Microbiology and Biotechnology, 2010, 86(3): 825–837

[47] Hemming J, Holmbom B, Reunanen M, Kronberg L. Determination of the strong mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone in chlorinated drinking and humic waters. Chemosphere, 1986, 15(5): 549–556

[48] Persson T, Givskov M, Nielsen J. Quorum sensing inhibition: targeting chemical communication in gram-negative bacteria. Current Medicinal Chemistry, 2005, 12(26): 3103–3115

Acknowledgements

The authors are grateful for the financial support from the Chinese Academy of Sciences (KZCX2-YW-JC406), the National Natural Science Foundation of China (Grant Nos. 51108440 and 51708343), and the Fujian Provincial Department of Science and Technology (Nos. 2009J06028 and 2009J01262).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg