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

Zhuoying WU, Qing WANG, Feng GUO, Shenghua ZHANG, Qipei JIANG, Xin YU

PDF(347 KB)
PDF(347 KB)
Front. Environ. Sci. Eng. ›› 2014, Vol. 8 ›› Issue (2) : 205-214. DOI: 10.1007/s11783-013-0492-5
RESEARCH ARTICLE

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

Author information +
History +

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

Cite this article

Download citation ▾
Zhuoying WU, Qing WANG, Feng GUO, Shenghua ZHANG, Qipei JIANG, Xin YU. Responses of bacterial strains isolated from drinking water environments to N-acyl-L-homoserine lactones and their analogs during biofilm formation. Front Envir Sci Eng, 2014, 8(2): 205‒214 https://doi.org/10.1007/s11783-013-0492-5

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
CrossRef Google scholar
[8]
Tsai Y P. Impact of flow velocity on the dynamic behaviour of biofilm bacteria. Biofouling, 2005, 21(5–6): 267–277
CrossRef Google scholar
[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
CrossRef Google scholar
[10]
Miller M B, Bassler B L. Quorum sensing in bacteria. Annual Review of Microbiology, 2001, 55(1): 165–199
CrossRef Google scholar
[11]
Bassler B L. Small talk: cell-to-cell communication in bacteria. Cell, 2002, 109(4): 421–424
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[27]
Kirisits M J, Parsek M R. Does Pseudomonas aeruginosa use intercellular signaling to build biofilm communities? Cellular Microbiology, 2006, 8(12): 1841–1849
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[30]
Parsek M R, Greenberg E P. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends in Microbiology, 2005, 13(1): 27–33
CrossRef Google scholar
[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
CrossRef Google scholar
[32]
Hammer B K, Bassler B L. Quorum sensing controls biofilm formation in Vibrio cholera. Molecular Microbiology, 2003, 50(1): 101–104
CrossRef Google scholar
[33]
Zhu J, Mekalanos J J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholera. Developmental Cell, 2003, 5(4): 647–656
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[39]
O’Toole G A, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm. Molecular Microbiology, 1998, 30(2): 295–304
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar

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
AI Summary AI Mindmap
PDF(347 KB)

Accesses

Citations

Detail

Sections
Recommended

/