LuxU connects quorum sensing to biofilm formation in Vibrio fischeri

Molecular Microbiology

Volumn 86, Issue 4, 2012, Pages 954-970

  Ray, Valerie A ^a   Visick, Karen L ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LUXQ KINASE; PHOSPHOTRANSFERASE LUXU; RESPONSE REGULATOR LUXO; RESPONSE REGULATOR SYPG; SENSOR KINASE AINR; SENSOR KINASE SYPG; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; BIOLUMINESCENCE; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE LOCUS; GENETIC SCREENING; MUTAGENESIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUORUM SENSING; TRANSCRIPTION REGULATION; TRANSPOSON; VIBRIO FISCHERI;

ALIIVIBRIO FISCHERI; BACTERIAL PROTEINS; BIOFILMS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENE LIBRARY; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; PHOSPHOPROTEINS; QUORUM SENSING;

VIBRIO FISCHERI;

EID: 84871801414     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12035     Document Type: Article

References (68)

1. Bassler, B.L.,Wright, M., and Silverman, M.R. (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 13: 273-286.
2. Biondi, E.G., Skerker, J.M., Arif, M., Prasol, M.S., Perchuk, B.S., and Laub, M.T. (2006) A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 59: 386-401.
3. Boettcher, K.J., and Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172: 3701-3706.
4. Bose, J.L., Kim, U., Bartkowski, W., Gunsalus, R.P., Overley, A.M., Lyell, N.L., et al. (2007) Bioluminescence in Vibrio fischeri is controlled by the redox-responsive regulator ArcA. Mol Microbiol 65: 538-553.
5. Bouquin, N., Johnson, A.L., Morgan, B.A., and Johnston, L.H. (1999) Association of the cell cycle transcription factor Mbp1 with the Skn7 response regulator in budding yeast. Mol Biol Cell 10: 3389-3400.
6. Cao, X., Studer, S.V., Wassarman, K., Zhang, Y., Ruby, E.G., and Miyashiro, T. (2012) The novel sigma factor-like regulator RpoQ controls luminescence, chitinase activity, and motility in Vibrio fischeri. MBio 3: e00285-00211.
7. Croxatto, A., Chalker, V.J., Lauritz, J., Jass, J., Hardman, A., Williams, P., et al. (2002) VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J Bacteriol 184: 1617-1629.
8. Croxatto, A., Pride, J., Hardman, A., Williams, P., Camara, M., and Milton, D.L. (2004) A distinctive dual-channel quorum-sensing system operates in Vibrio anguillarum. Mol Microbiol 52: 1677-1689.
9. Davis, R.W., Botstein, D., and Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
10. DeLoney, C.R., Bartley, T.M., and Visick, K.L. (2002) Role for phosphoglucomutase in Vibrio fischeri-Euprymna scolopes symbiosis. J Bacteriol 184: 5121-5129.
11. Domian, I.J., Quon, K.C., and Shapiro, L. (1997) Cell typespecific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90: 415-424.
12. Egland, K.A., and Greenberg, E.P. (2000) Conversion of the Vibrio fischeri transcriptional activator, LuxR, to a repressor. J Bacteriol 182: 805-811.
13. Enos-Berlage, J.L., Guvener, Z.T., Keenan, C.E., and McCarter, L.L. (2005) Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol Microbiol 55: 1160-1182.
14. Fidopiastis, P.M., Miyamoto, C.M., Jobling, M.G., Meighen, E.A., and Ruby, E.G. (2002) LitR, a new transcriptional activator in Vibrio fischeri, regulates luminescence and symbiotic light organ colonization. Mol Microbiol 45: 131- 143.
15. Freeman, J.A., and Bassler, B.L. (1999a) A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol 31: 665-677.
16. Freeman, J.A., and Bassler, B.L. (1999b) Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J Bacteriol 181: 899-906.
17. Gilson, L., Kuo, A., and Dunlap, P.V. (1995) AinS and a new family of autoinducer synthesis proteins. J Bacteriol 177: 6946-6951.
18. Graf, J., Dunlap, P.V., and Ruby, E.G. (1994) Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol 176: 6986-6991.
19. Gyllborg, M.C., Sahl, J.W., Cronin, D.C., 3rd, Rasko, D.A., and Mandel, M.J. (2012) Draft genome sequence of Vibrio fischeri SR5, a strain isolated from the light organ of theMediterranean squid Sepiola robusta. J Bacteriol 194: 1639.
20. Hammer, B.K., and Bassler, B.L. (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50: 101-104.
21. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
22. Hussa, E.A., O'Shea, T.M., Darnell, C.L., Ruby, E.G., and Visick, K.L. (2007) Two-component response regulators of Vibrio fischeri: identification, mutagenesis, and characterization. J Bacteriol 189: 5825-5838.
23. Hussa, E.A., Darnell, C.L., and Visick, K.L. (2008) RscS functions upstream of SypG to control the syp locus and biofilm formation in Vibrio fischeri. J Bacteriol 190: 4576- 4583.
24. Iniesta, A.A., McGrath, P.T., Reisenauer, A., McAdams, H.H., and Shapiro, L. (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci USA 103: 10935-10940.
25. Jacobs, C., Ausmees, N., Cordwell, S.J., Shapiro, L., and Laub, M.T. (2003) Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol Microbiol 47: 1279- 1290.
26. Janiak-Spens, F., Sparling, D.P., andWest, A.H. (2000) Novel role for an HPt domain in stabilizing the phosphorylated state of a response regulator domain. J Bacteriol 182: 6673-6678.
27. Kuo, A., Callahan, S.M., and Dunlap, P.V. (1996) Modulation of luminescence operon expression by N-octanoyl-Lhomoserine lactone in ainS mutants of Vibrio fischeri. J Bacteriol 178: 971-976.
28. Le Roux, F., Binesse, J., Saulnier, D., and Mazel, D. (2007) Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 73: 777- 784.
29. Lee, J.H., Rhee, J.E., Park, U., Ju, H.M., Lee, B.C., Kim, T.S., et al. (2007) Identification and functional analysis of Vibrio vulnificus SmcR, a novel global regulator. J Microbiol Biotechnol 17: 325-334.
30. Li, S., Ault, A., Malone, C.L., Raitt, D., Dean, S., Johnston, L.H., et al. (1998) The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J 17: 6952-6962.
31. Liu, H., Gu, D., Cao, X., Liu, Q., Wang, Q., and Zhang, Y. (2011) Characterization of a new quorum sensing regulator luxT and its roles in the extracellular protease production, motility, and virulence in fish pathogen Vibrio alginolyticus. Arch Microbiol 194: 439-452.
32. Lupp, C., and Ruby, E.G. (2005) Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J Bacteriol 187: 3620-3629.
33. Lupp, C., Urbanowski, M., Greenberg, E.P., and Ruby, E.G. (2003) The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol 50: 319-331.
34. Lyell, N.L., Dunn, A.K., Bose, J.L., Vescovi, S.L., and Stabb, E.V. (2008) Effective mutagenesis of Vibrio fischeri by using hyperactive mini-Tn5 derivatives. Appl Environ Microbiol 74: 7059-7063.
35. Lyell, N.L., Dunn, A.K., Bose, J.L., and Stabb, E.V. (2010) Bright mutants of Vibrio fischeri ES114 reveal conditions and regulators that control bioluminescence and expression of the lux operon. J Bacteriol 192: 5103-5114.
36. McCann, J., Stabb, E.V., Millikan, D.S., and Ruby, E.G. (2003) Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl Environ Microbiol 69: 5928-5934.
37. Mandel, M.J., Wollenberg, M.S., Stabb, E.V., Visick, K.L., and Ruby, E.G. (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature 458: 215-218.
38. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
39. Milton, D.L. (2006) Quorum sensing in vibrios: complexity for diversification. Int J Med Microbiol 296: 61-71.
40. Miyamoto, C.M., Lin, Y.H., and Meighen, E.A. (2000) Control of bioluminescence in Vibrio fischeri by the LuxO signal response regulator. Mol Microbiol 36: 594-607.
41. Miyamoto, C.M., Dunlap, P.V., Ruby, E.G., and Meighen, E.A. (2003) LuxO controls luxR expression in Vibrio harveyi: evidence for a common regulatory mechanism in Vibrio. Mol Microbiol 48: 537-548.
42. Miyashiro, T., and Ruby, E.G. (2012) Shedding light on bioluminescence regulation in Vibrio fischeri. Mol Microbiol 84: 795-806.
43. Miyashiro, T., Wollenberg, M.S., Cao, X., Oehlert, D., and Ruby, E.G. (2010) A single qrr gene is necessary and sufficient for LuxO-mediated regulation in Vibrio fischeri. Mol Microbiol 77: 1556-1567.
44. Morgan, B.A., Bouquin, N., Merrill, G.F., and Johnston, L.H. (1995) A yeast transcription factor bypassing the requirement for SBF and DSC1/MBF in budding yeast has homology to bacterial signal transduction proteins. EMBO J 14: 5679-5689.
45. Morris, A.R., Darnell, C.L., and Visick, K.L. (2011) Inactivation of a novel response regulator is necessary for biofilm formation and host colonization by Vibrio fischeri. Mol Microbiol 82: 114-130.
46. Neiditch, M.B., Federle, M.J., Miller, S.T., Bassler, B.L., and Hughson, F.M. (2005) Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18: 507-518.
47. Neiditch, M.B., Federle, M.J., Pompeani, A.J., Kelly, R.C., Swem, D.L., Jeffrey, P.D., et al. (2006) Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126: 1095-1108.
48. Ng, W.L., and Bassler, B.L. (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
49. Posas, F., and Saito, H. (1998) Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J 17: 1385-1394.
50. Posas, F., Wurgler-Murphy, S.M., Maeda, T., Witten, E.A., Thai, T.C., and Saito, H. (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 'two-component' osmosensor. Cell 86: 865-875.
51. Quon, K.C., Yang, B., Domian, I.J., Shapiro, L., and Marc-zynski, G.T. (1998) Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci USA 95: 120- 125.
52. Sanders, D.A., Gillece-Castro, B.L., Stock, A.M., Burlingame, A.L., and Koshland, D.E., Jr (1989) Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J Biol Chem 264: 21770-21778.
53. Sanders, D.A., Gillece-Castro, B.L., Burlingame, A.L., and Koshland, D.E., Jr (1992) Phosphorylation site of NtrC, a protein phosphatase whose covalent intermediate activates transcription. J Bacteriol 174: 5117-5122.
54. Shibata, S., and Visick, K.L. (2012) Sensor kinase RscS induces the production of antigenically distinct outer membrane vesicles that depend on the symbiosis polysaccharide locus in Vibrio fischeri. J Bacteriol 194: 185-194.
55. Shikuma, N.J., Fong, J.C., Odell, L.S., Perchuk, B.S., Laub, M.T., and Yildiz, F.H. (2009) Overexpression of VpsS, a hybrid sensor kinase, enhances biofilm formation in Vibrio cholerae. J Bacteriol 191: 5147-5158.
56. Sitnikov, D.M., Schineller, J.B., and Baldwin, T.O. (1995) Transcriptional regulation of bioluminesence genes from Vibrio fischeri. Mol Microbiol 17: 801-812.
57. Stabb, E., Schaefer, A., Bose, J.L., and Ruby, E.G. (2008) Quorum signalling and symbiosis in the marine luminous bacterium Vibrio fischeri. In Chemical Communication among Bacteria. Winans, S.C., and Bassler, B.L. (eds). Washington, D.C.: ASM Press, pp. 233-250.
58. Stabb, E.V., and Ruby, E.G. (2002) RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol 358: 413-426.
59. Stevens, A.M., Dolan, K.M., and Greenberg, E.P. (1994) Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region. Proc Natl Acad Sci USA 91: 12619-12623.
60. Stock, A.M., Robinson, V.L., and Goudreau, P.N. (2000) Twocomponent signal transduction. Annu Rev Biochem 69: 183-215.
61. Studer, S.V., Mandel, M.J., and Ruby, E.G. (2008) AinS quorum sensing regulates the Vibrio fischeri acetate switch. J Bacteriol 190: 5915-5923.
62. Visick, K.L. (2005) Layers of signaling in a bacterium-host association. J Bacteriol 187: 3603-3606.
63. Visick, K.L., and Skoufos, L.M. (2001) Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J Bacteriol 183: 835-842.
64. Weber, B., Lindell, K., El Qaidi, S., Hjerde, E., Willassen, N.P., and Milton, D.L. (2011) The phosphotransferase VanU represses expression of four qrr genes antagonizing VanO-mediated quorum-sensing regulation in Vibrio anguillarum. Microbiology 157: 3324-3339.
65. West, A.H., and Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
66. Yip, E.S., Grublesky, B.T., Hussa, E.A., and Visick, K.L. (2005) A novel, conserved cluster of genes promotes symbiotic colonization and sigma(54)-dependent biofilm formation by Vibrio fischeri. Mol Microbiol 57: 1485-1498.
67. Yip, E.S., Geszvain, K., DeLoney-Marino, C.R., and Visick, K.L. (2006) The symbiosis regulator rscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol Microbiol 62: 1586-1600.
68. Zhang, Y., Qiu, Y., Tan, Y., Guo, Z., Yang, R., and Zhou, D. (2012) Transcriptional regulation of opaR, qrr2-4 and aphA by the master quorum-sensing regulator OpaR in Vibrio parahaemolyticus. PLoS ONE 7: e34622.