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Vibrio fischeri Symbiotically Synchronizes Bioluminescence in Marine Animals via Quorum Sensing Mechanism

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Implication of Quorum Sensing System in Biofilm Formation and Virulence

Abstract

The process of intercellular communication called quorum sensing (QS) was first described in the marine bioluminescent bacterium Vibrio fischeri which lives in symbiotic associations with a number of marine animal hosts. A luciferase enzyme complex is found to be responsible for light production in V. fischeri. The bioluminescence emitted by these bacteria is a striking result of individual microbial cells coordinating a group behavior. In V. fischeri, QS controls bioluminescence, the ability of the bacteria to produce light, at high cell density. The mechanism of sensing involves an AI synthase, LuxI in V. fischeri, which makes small auto inducer molecules (AHLs). The autoinducer builds up in medium at high concentrations binds to a transcription regulator, LuxR in V. fischeri, which then alters the gene expression by coordinating bioluminescence among the local cell population. The genes responsible for light production are principally regulated by LuxR-LuxI QS system. This review primarily emphasizes the role of AHL signal molecules in QS network between the bacteria-animal symbiotic associations.

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References

  1. Applegate, B. M., Kehrmeyer, S. R., & Sayler, G. S. (1998). A chromosomally based tod-Luxcdabe whole-cell reporter for benzene, toluene, ethybenzene, and xylene (BTEX) sensing. Applied and Environmental Microbiology, 64(7), 2730–2735.

    Google Scholar 

  2. Arfsten, D., Davenport, R., & Schaeffer, D. J. (1994). Reversion of bioluminescent bacteria (Mutatox) to their luminescent state upon exposure to organic compounds, munitions, and metal salts. Biomedical and Environmental Sciences: BES, 7(2), 144–149.

    CAS  PubMed  Google Scholar 

  3. Neiditch, M. B., Federle, M. J., Pompeani, A. J., Kelly, R. C., Swem, D. L., Jeffrey, P. D., Bassler, B. L., & Hughson, F. M. (2006). Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell, 126, 1095–1108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bar, R., & Ulitzur, S. (1994). Bacterial toxicity of cyclodextrins: Luminuous Escherichia coli as a model. Applied Microbiology and Biotechnology, 41(5), 574–577.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  6. Boettcher, K. J., & Ruby, E. G. (1990). Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. Journal of Bacteriology, 172(7), 3701–3706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bourgois, J. J., Sluse, F. E., Baguet, F., & Mallefet, J. (2001). Kinetics of light emission and oxygen consumption by bioluminescent bacteria. Journal of Bioenergetics and Biomembranes, 33(4), 353–363.

    Article  CAS  PubMed  Google Scholar 

  8. Bulich, A. A. (1982). A practical and reliable method for monitoring the toxicity of aquatic samples. Process Biochemistry, 17(2), 45–47.

    Google Scholar 

  9. Charrier, T., Durand, M. J., Jouanneau, S., Dion, M., Pernetti, M., Poncelet, D., et al. (2011a). A multi-channel bioluminescent bacterial biosensor for the on-line detection of metals and toxicity. Part I: Design and optimization of bioluminescent bacterial strains. Analytical and Bioanalytical Chemistry, 400, 1051–1060.

    Article  CAS  PubMed  Google Scholar 

  10. Charrier, T., Chapeau, C., Bendria, L., Picart, P., Daniel, P., & Thouand, G. (2011b). A multi-channel bioluminescent bacterial biosensor for the on-line detection of metals and toxicity. Part II: Technical development and proof of concept of the biosensor. Analytical and Bioanalytical Chemistry, 400, 1061–1070.

    Article  CAS  PubMed  Google Scholar 

  11. Czyz, A., Jasiecki, J., Bogdan, A., Szpilewska, H., & We, G. (2000). Genetically modified Vibrio harveyi strains as potential bioindicators of mutagenic pollution of marine environments. Applied and Environmental Microbiology, 66(2), 599–605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. De Kievit, T. R., & Iglewski, B. H. (2000). Bacterial quorum sensing in pathogenic relationships. Infection and Immunity, 68(9), 4839–4849.

    Article  PubMed  PubMed Central  Google Scholar 

  13. De Wet, J. R., Wood, K. V., DeLuca, M., Helinski, D. R., & Subramani, S. (1987). Firefly luciferase gene: Structure and expression in mammalian cells. Molecular and Cellular Biology, 7(2), 725–737.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Dunlap, P. V. (1991). Organization and regulation of bacterial luminescence genes. Photochemistry and Photobiology, 54(6), 1157–1170.

    Article  CAS  Google Scholar 

  15. Engebrecht, J., & Silverman, M. (1984). Identification of genes and gene products necessary for bacterial bioluminescence. Proceedings of the National Academy of Sciences, 81(13), 4154–4158.

    Article  CAS  Google Scholar 

  16. Engebrecht, J., Simon, M., & Silverman, M. (1985). Measuring gene expression with light. Science, 227(4692), 1345–1347.

    Article  CAS  PubMed  Google Scholar 

  17. Ferri, S. R., & Meighen, E. A. (1991). A lux-specific myristoyl transferase in luminescent bacteria related to eukaryotic serine esterases. Journal of Biological Chemistry, 266(20), 12852–12857.

    CAS  PubMed  Google Scholar 

  18. Friedrich, W. F., & Greenberg, E. P. (1983). Glucose repression of luminescence and luciferase in Vibrio fischeri. Archives of Microbiology, 134(2), 87–91.

    Article  CAS  Google Scholar 

  19. Hagen, S. (2015). The physical basis of bacterial quorum communication. Berlin: Springer.

    Book  Google Scholar 

  20. Hanzelka, B. L., & Greenberg, E. P. (1995). Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain. Journal of Bacteriology, 177, 815–817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hastings, J. W., Gibson, Q. H., & Greenwood, C. (1964). On the molecular mechanism of bioluminescence, I. The role of long-chain aldehyde. Proceedings of the National Academy of Sciences, 52(6), 1529–1535.

    Article  CAS  Google Scholar 

  22. Hastings, J. W., & Nealson, K. H. (1977). Bacterial bioluminescence. Annual Reviews in Microbiology, 31(1), 549–595.

    Article  CAS  Google Scholar 

  23. Hastings, J. W. (1983). Biological diversity, chemical mechanisms, and the evolutionary origins of bioluminescent systems. Journal of Molecular Evolution, 19(5), 309–321.

    Article  CAS  PubMed  Google Scholar 

  24. Hastings, J. W., Potrikusv, C. J., Gupta, S. C., Kurfürst, M., & Makemson, J. C. (1985). Biochemistry and physiology of bioluminescent bacteria. In Advances in microbial physiology (Vol. 26, pp. 235–291). Academic Press.

    Google Scholar 

  25. Haygood, M., & Allen, S. (2000). Luminous bacteria. In Journey to diverse microbial worlds (pp. 269–285). Dordrecht: Springer.

    Chapter  Google Scholar 

  26. Heath-Heckman, E. A., Peyer, S. M., Whistler, C. A., Apicella, M. A., Goldman, W. E., & McFall-Ngai, M. J. (2013). Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. MBio, 4. https://doi.org/10.1128/mBio.00167-13.

  27. Heitzer, A., Webb, O. F., Thonnard, J. E., & Sayler, G. S. (1992). Specific and quantitative assessment of naphthalene and salicylate bioavailability by using a bioluminescent catabolic reporter bacterium. Applied and Environmental Microbiology, 58(6), 1839–1846.

    Google Scholar 

  28. Hense, B. A., & Schuster, M. (2015). Core principles of bacterial autoinducer systems. Microbiology and Molecular Biology Reviews, 79(1), 153–169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Horry, H., Charrier, T., Durand, M. J., Vrignaud, B., Picart, P., Daniel, P., et al. (2007). Technological conception of an optical biosensor with a disposable card for use. Sensors and Actuators B: Chemical, 122, 527–534.

    Article  CAS  Google Scholar 

  30. Ivask, A., Hakkila, K., & Virta, M. (2001). Detection of organomercurials with sensor bacteria. Analytical Chemistry, 73(21), 5168–5171.

    Article  CAS  PubMed  Google Scholar 

  31. Jones, B. W., & Nishiguchi, M. K. (2004). Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Marine Biology, 144, 1151–1155.

    Article  Google Scholar 

  32. Jouanneau, S., Durand, M. J., Courcoux, P., Blusseau, T., & Thouand, G. (2011). Improvement of the identification of four heavy metals in environmental samples by using predictive decision tree models coupled with a set of five bioluminescent bacteria. Environmental Science & Technology, 45, 2925–2931.

    Article  CAS  Google Scholar 

  33. Jouanneau, S., Durand, M. J., & Thouand, G. (2012). Online detection of metals in environmental samples: Comparing two concepts of bioluminescent bacterial biosensors. Environmental Science & Technology, 46, 11979–11987.

    Article  CAS  Google Scholar 

  34. Jouanneau, S., Durand-Thouand, M. J., & Thouand, G. (2016). Design of a toxicity biosensor based on Aliivibrio fischeri entrapped in a disposable card. Environmental Science and Pollution Research, 23, 4340–4345.

    Article  CAS  PubMed  Google Scholar 

  35. Lampinen, J., Korpela, M., Saviranta, P., Kroneld, R., & Karp, M. (1990). Use of Escherichia coli cloned with genes encoding bacterial luciferase for evaluation of chemical toxicity. Environmental Toxicology, 5(4), 337–350.

    CAS  Google Scholar 

  36. Lewis, J. C., Feltus, A., Ensor, C. M., Ramanathan, S., & Daunert, A. S. (1998). Peer reviewed: Applications of reporter genes. Analytical Chemistry, 70(17), 579A–585A.

    Article  CAS  PubMed  Google Scholar 

  37. Lupp, C., & Ruby, E. G. (2005). Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. Journal of Bacteriology, 187(11), 3620–3629.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mandel, M. J., Wollenberg, M. S., Stabb, E. V., Visick, K. L., & Ruby, E. G. (2009). A single regulatory gene is sufficient to alter bacterial host range. Nature, 458, 215–218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. McFall-Ngai, M. (2014a). Divining the essence of symbiosis: Insights from the squid-vibrio model. PLoS Biology, 12(2), e1001783.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. McFall-Ngai, M. J. (2014b). The importance of microbes in animal development: Lessons from the squid-vibrio symbiosis. Annual Review of Microbiology, 68, 177–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Meighen, E. (1991). Molecular biology of bacterial bioluminescence. Microbiological Reviews, 55(1), 123–142.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Meighen, E. A. (1988). Enzymes and genes from the lux operons of bioluminescent bacteria. Annual Reviews in Microbiology, 42(1), 151–176.

    Article  CAS  Google Scholar 

  43. Meighen, E. A. (1993). Bacterial bioluminescence: Organization, regulation, and application of the lux genes. The FASEB Journal, 7(11), 1016–1022.

    Article  CAS  PubMed  Google Scholar 

  44. Meighen, E. A., & Dunlap, P. V. (1993). Physiological, biochemical and genetic control of bacterial bioluminescence. Advances in Microbial Physiology, 34, 1–67 Academic Press.

    Article  CAS  PubMed  Google Scholar 

  45. Meighen, E. A. (1994). Genetics of bacterial bioluminescence. Annual Review of Genetics, 28(1), 117–139.

    Article  CAS  PubMed  Google Scholar 

  46. Miyamoto, C. M., Meighen, E. A., & Graham, A. F. (1990). Transcriptional regulation of lux genes transferred into Vibrio harveyi. Journal of Bacteriology, 172(4), 2046–2054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Miyamoto, C., Boylan, M., Cragg, L., & Meighen, E. (1989). Comparison of the lux systems in Vibrio harveyi and Vibrio fischeri. Luminescence, 3(4), 193–199.

    CAS  Google Scholar 

  48. Miyashiro, T., & Ruby, E. G. (2012). Shedding light on bioluminescence regulation in Vibrio fischeri. Molecular Microbiology, 84(5), 795–806.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nealson, K. H., & Hastings, J. W. (1979). Bacterial bioluminescence: Its control and ecological significance. Microbiological Reviews, 43(4), 496.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Nealson, K. H., & Hastings, J. W. (1991). The luminous bacteria. In The prokaryotes, a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications (pp. 625–639). Berlin/Heidelberg/New York: Springer.

    Google Scholar 

  51. Nealson, K. H., Platt, T., & Hastings, J. W. (1970). Cellular control of the synthesis and activity of the bacterial luminescent system. Journal of Bacteriology, 104(1), 313–322.

    Google Scholar 

  52. Ng, W. L., & Bassler, B. L. (2009). Bacterial quorum-sensing network architectures. Annual Review of Genetics, 43, 197–222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Norsworthy, A. N., & Visick, K. L. (2013). Gimme shelter: How Vibrio fischeri successfully navigates an animal’s multiple environments. Frontiers in Microbiology, 4, 356.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Nyholm, S. V., & McFall-Ngai, M. J. (2004). The winnowing: Establishing the squid-vibrio symbiosis. Nature Reviews Microbiology, 2, 632–642.

    Article  CAS  PubMed  Google Scholar 

  55. Perez, P. D., & Hagen, S. J. (2010). Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri. PLoS One, 5, e15473.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Ribo, J. M., & Kaiser, K. L. (1987). Photobacterium phosphoreum toxicity bioassay. I. Test procedures and applications. Environmental Toxicology, 2(3), 305–323.

    CAS  Google Scholar 

  57. Ruby, E. G. (1996). Lessons from a cooperative, bacterial-animal association: The vibrio fischeri–Euprymna scolopes light organ symbiosis. Annual Reviews in Microbiology, 50(1), 591–624.

    Article  CAS  PubMed  Google Scholar 

  58. Schaefer, A. L., Val, D. L., Hanzelka, B. L., Cronan, J. E., Jr., & Greenberg, E. P. (1996). Generation of cell-to-cell signals in quorum sensing: Acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proceedings of the National Academy of Sciences of the United States of America, 93, 9505–9509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Seckbach, J. (Ed.) (2000). Journey to diverse microbial worlds: Adaptation to exotic environments (Vol. 2). Springer Science & Business Media.

    Google Scholar 

  60. Selifonova, O., Burlage, R., & Barkay, T. (1993). Bioluminescent sensors for detection of bioavailable Hg (II) in the environment. Applied and Environmental Microbiology, 59(9), 3083–3090.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Steinberg, S. M., Poziomek, E. J., Engelmann, W. H., & Rogers, K. R. (1995). A review of environmental applications of bioluminescence measurements. Chemosphere, 30(11), 2155–2197.

    Article  CAS  Google Scholar 

  62. Stevens, A. M., Dolan, K. M., & Greenberg, E. P. (1994). Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region. Proceedings of the National Academy of Sciences of the United States of America, 91, 12619–12623.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Stevens, A. M., & Greenberg, E. P. (1997). Quorum sensing in Vibrio fischeri: Essential elements for activation of the luminescence genes. Journal of Bacteriology, 179(2), 557–562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tauriainen, S., Karp, M., Chang, W., & Virta, M. (1998). Luminescent bacterial sensor for cadmium and lead. Biosensors and Bioelectronics, 13(9), 931–938.

    Article  CAS  PubMed  Google Scholar 

  65. Tescione, L., & Belfort, G. (1993). Construction and evaluation of a metal ion biosensor. Biotechnology and Bioengineering, 42(8), 945–952.

    Article  CAS  PubMed  Google Scholar 

  66. Virta, M., Karp, M., & Vuorinen, P. (1994). Nitric oxide donor-mediated killing of bioluminescent Escherichia coli. Antimicrobial Agents and Chemotherapy, 38(12), 2775–2779.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Virta, M., Lampinen, J., & Karp, M. (1995). A luminescence-based mercury biosensor. Analytical Chemistry, 67(3), 667–669.

    Article  CAS  Google Scholar 

  68. Von Bodman, S. B., Majerczak, D. R., & Coplin, D. L. (1998). A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proceedings of the National Academy of Sciences, 95(13), 7687–7692.

    Article  Google Scholar 

  69. Waters, C., & Bassler, B. (2005). Quorum sensing: Cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 21, 319–346.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

PVBC is grateful to Krishna University for providing necessary facilities to carry out the research work and for extending constant support.

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Pallaval Veera Bramhachari, Mohana Sheela, G. (2018). Vibrio fischeri Symbiotically Synchronizes Bioluminescence in Marine Animals via Quorum Sensing Mechanism. In: Pallaval Veera Bramhachari (eds) Implication of Quorum Sensing System in Biofilm Formation and Virulence. Springer, Singapore. https://doi.org/10.1007/978-981-13-2429-1_13

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