Quorum-Sensing Mechanisms in Bacterial Communities and Their Potential Applications

세균의 의사 소통(Quorum-Sensing) 기구와 그 잠재적 응용성

  • Yoon, Sung-Sik (Department of Biological Resources and Technology, Yonsei University)
  • 윤성식 (연세대학교 생물자원공학과)
  • Published : 2006.09.30

Abstract

Although microorganisms are, in fact, the most diverse and abundant type of organism on Earth, the ecological functions of microbial populations remains poorly understood. A variety of bacteria including marine Vibrios encounter numerous ecological challenges, such as UV light, predation, competition, and seasonal variations in seawater including pH, salinity, nutrient levels, temperature and so forth. In order to survive and proliferate under variable conditions, they have to develop elaborate means of communication to meet the challenges to which they are exposed. In bacteria, a range of biological functions have recently been found to be regulated by a population density-dependent cell-cell signaling mechanism known as quorum-sensing (QS). In other words, bacterial cells sense population density by monitoring the presence of self-produced extracellular autoinducers (AI). N-acylhomoserine lactone (AHL)-dependent quorum-sensing was first discovered in two luminescent marine bacteria, Vibrio fischeri and Vibrio harveyi. The LuxI/R system of V. fischeriis the paradigm of Gram-negative quorum-sensing systems. At high population density, the accumulated signalstrigger the expression of target genes and thereby initiate a new set of biological activities. Several QS systems have been identified so far. Among them, an AHL-dependent QS system has been found to control biofilm formation in several bacterial species, including Pseudomonas aeruginosa, Aeromonas hydrophila, Burkholderia cepacia, and Serratia liquefaciens. Bacterial biofilm is a structured community of bacterial cells enclosed in a self-produced polymeric matrix that adheres to an inert or living surface. Extracellular signal molecules have been implicated in biofilm formation. Agrobacterium tumefaciens strain NT1(traR, tra::lacZ749) and Chromobacterium violaceum strain CV026 are used as biosensors to detect AHL signals. Quorum sensing in lactic acid bacteria involves peptides that are directly sensed by membrane-located histidine kinases, after which the signal is transmitted to an intracellular regulator. In the nisin autoregulation process in Lactococcus lactis, the NisK protein acts as the sensor for nisin, and NisR protein as the response regulator activatingthe transcription of target genes. For control over growth and survival in bacterial communities, various strategies need to be developed by which receptors of the signal molecules are interfered with or the synthesis and release of the molecules is controlled. However, much is still unknown about the metabolic processes involved in such signal transduction and whether or not various foods and food ingredients may affect communication between spoilage or pathogenic bacteria. In five to ten years, we will be able to discover new signal molecules, some of which may have applications in food preservation to inhibit the growth of pathogens on foods.

Keywords

References

  1. Bassler, B. L., Greenberg, E. P., and Stevens, A. M. (1997) Cross-species induction of luminescence in the quorum- sensing bacterium Vibrio harveyi. J. Bacteriol. 179, 4043-4045 https://doi.org/10.1128/jb.179.12.4043-4045.1997
  2. Brandl, M. T., Miller, W. G., Bates, A. H., and Mandrell, R. E. (2005) Production of AI-2 in Salmonella enterica serovar Thompson contributes to its fitness in chickens but not on cilantro leaf surfaces. Appl. Environ. MicrobioI. 71, 2653-2662 https://doi.org/10.1128/AEM.71.5.2653-2662.2005
  3. Cloak, O. M., Solow, B. T., Briggs, C. E., Chen, C. Y., and Fratamico, P. M. (2002) Quorum sensing and production of autoinducer-2 in Campylobacter spp., Escherichia coli 0157: H7, and Salmonella enterica serovar typhimurium in foods. Appl. Environ. Microbiol. 68, 4666-4671 https://doi.org/10.1128/AEM.68.9.4666-4671.2002
  4. Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., and Greenberg, E. P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298 https://doi.org/10.1126/science.280.5361.295
  5. de Vos, W. M., Kleerebezem, M., and Kuipers, O. P. (1997) Expression systems for industrial Gram-positive bacteria with low guanine and cytosine content. Curr. Opinion Biotechnol. 8, 547-553 https://doi.org/10.1016/S0958-1669(97)80027-4
  6. Dunstall, G., Rowe, M. T., Wisdom, G. B., and Kilpatrick, D. (2005) Effect of quorum sensing agents on the growth kinetics of Pseudomonas spp. of raw milk origin. J. Dairy Res. 72, 276-280 https://doi.org/10.1017/S0022029905000713
  7. Finch, R. G., Pritchard, D. I. Bycroft, B. W., Williams, P., and Stewart, G. S. (1998) Quorum sensing - a novel target for anti-infective therapy. J. Antimicrob. Chemother. 42, 569-571 https://doi.org/10.1093/jac/42.5.569
  8. Gram, L., Ravn, L., Rasch, M., Bruhn, J. B., Christensen, A. B., and Givskov, M. (2002) Interactions between food spoilage bacteria. Int. J. Food Microbiol. 78, 79-97 https://doi.org/10.1016/S0168-1605(02)00233-7
  9. Heal, R. D. and Parsons, A. T. (2002) Novel intercellular communication system in Escherichia coli that confers antibiotic resistance between physically separated populations. J. Appl. Microbiol. 92, 1116-1122 https://doi.org/10.1046/j.1365-2672.2002.01647.x
  10. Hastings, J. W. and Greenberg, E. P. (1999) Quorum sensing: the explanation of a curious phenomenon reveals a common characteristics of bacteria. J. Bacteriol. 181, 2667-2668
  11. Kleerebezem, M., Quadri, L. E. N., Kuipers, O. P., and de Vos, W. M. (1997) Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol. Microbiol. 24, 895-904 https://doi.org/10.1046/j.1365-2958.1997.4251782.x
  12. Kuipers, O. P., Deruyter, P. G. G. A., Kleerebezem, M., and de Vos, W. M. (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64, 15-21 https://doi.org/10.1016/S0168-1656(98)00100-X
  13. Lu, L., Hume, M. E., and Pillai, S. D. (2004) Autoinducer-2-1ike activity associated with foods and its interaction with food additives. J. Food Protec. 67, 1457-1462
  14. Lu, L., Hume, M. E., and Pillai, S. D. (2005) Autoinducer-2-like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Pathogen Dis. 2, 242-249 https://doi.org/10.1089/fpd.2005.2.242
  15. McLean, R. J. C, Whiteley, M., StickIer, D. J., and Fuqua, W. C (1997) Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol. Lett. 154, 259-263 https://doi.org/10.1111/j.1574-6968.1997.tb12653.x
  16. Nealson, K. H. and Hastings, J. W. (1979) Bacterial bioluminescence: Its control and ecological significance. Microbiol. Rev. 43, 496-518
  17. Novick, R. P. and Muir, W. M. (1999) Virulence gene regulation by peptides in staphylococci and other Grampositive bacteria. Curr. Opin. Microbiol. 2, 40-45 https://doi.org/10.1016/S1369-5274(99)80007-1
  18. Pearson, J. P., Passador, L., Iglewski, B. H., and Greenberg, E. P. (1995) A. second N-acyl homoserine lactone signal produced by P. aeruginosa. Proc. Natl. Acad. Sci. USA 92, 1490-1494
  19. Rasch, M., Andersen, J. B., Nielsen, K. F., Flodgaard, L. R., Christensen, H., Givskov, M., and Gram, L. (2005) Involvement of bacterial quorum sensing signals in spoilage of bean sprouts. Appl. Environ. Microbiol. 71, 3321-3330 https://doi.org/10.1128/AEM.71.6.3321-3330.2005
  20. Rasmussen, T. B., Bjarnsholt, T., Skindersoe,M. E., Hentzer, M., Kristoffersen, P., Kote, M., Nielsen, J. Eberl, L., and Givskov, M. (2005) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol. 187, 1799-1814 https://doi.org/10.1128/JB.187.5.1799-1814.2005
  21. Reading, N. C. and Sperandio, V. (2006) Quorum sensing: The many languages of bacteria. FEMS Microbiol. Lett. 254, 1-11 https://doi.org/10.1111/j.1574-6968.2005.00001.x
  22. Riedel, K., Hentzer, M., Geisenberger, O., Huber, B., Steidle, A., Wu, H., Hoiby, N., Givskov, M., Molin, S., and Eberl, L. (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147, 3249-3262 https://doi.org/10.1099/00221287-147-12-3249
  23. Sperandio, V., Torres, A. G., Jarvis, B., Nataro, J. P., and Kaper, J. B. (2003) Bacteria host communication: The language of hormones. Proc. Natl. Acad. Sci. USA 100, 8951-8956
  24. Swift, S., Bainton, N. J. and Winson, M. K. (1994) Gramnegative bacterial communication by N-acylhomoserine lactones: A. universal language? Trends Microbiol. 2, 193-198 https://doi.org/10.1016/0966-842X(94)90110-Q
  25. Vendeville, A, Winzer, K., Heurlier, K., Tang, C. M., and Hardie, K. R. (2005). Making sense of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3, 383-396 https://doi.org/10.1038/nrmicro1146
  26. Wang, L., Li, J. March, J. C., Valdes, J. J. and Bentley, W. E. (2005) LuxS-dependent gene regulation in Escherichia coli K.-12 revealed by genomic expression profiling. J. Bacteriol. 187, 8350-8360 https://doi.org/10.1128/JB.187.24.8350-8360.2005
  27. Waters, C. M. and Bassler, B. L. (2005) Quorum sensing: Cell to cell communication in bacteria. Ann. Rev. Cell. Dev. Biol. 21, 319-346 https://doi.org/10.1146/annurev.cellbio.21.012704.131001