The phosphorylation flow of the Vibrio harveyi quorum-sensing cascade determines levels of phenotypic heterogeneity in the population

Journal of Bacteriology

Volumn 197, Issue 10, 2015, Pages 1747-1756

  Plener, Laure ^a   Lorenz, Nicola ^a   Reiger, Matthias ^a,b   Ramalho, Tiago ^b   Gerland, Ulrich ^b   Jung, Kirsten ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LUXO PROTEIN; LUXU PROTEIN; PHOSPHATASE; PHOSPHOTRANSFERASE; SYNTHETASE; TRANSCRIPTION FACTOR LUXR; TRANSFER RNA; UNCLASSIFIED DRUG; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ARTICLE; BACTERIAL GROWTH; BEHAVIOR ASSESSMENT; CELL DENSITY; COPY NUMBER VARIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEEDBACK SYSTEM; GENE EXPRESSION; GENETIC HETEROGENEITY; HYBRID; LUMINESCENCE; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; QUORUM SENSING; SINGLE CELL ANALYSIS; VIBRIO HARVEYI; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; VIBRIO;

BACTERIA (MICROORGANISMS); VIBRIO HARVEYI;

PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; QUORUM SENSING; SIGNAL TRANSDUCTION; VIBRIO;

EID: 84928533083     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02544-14     Document Type: Article

References (48)

1. Eberhard A. 1972. Inhibition and activation of bacterial luciferase synthesis. J Bacteriol 109:1101-1105
2. Kaplan HB, Greenberg EP. 1985. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163: 1210-1214
3. Nealson KH, Platt T, Hastings JW. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313-322
4. Drees B, Reiger M, Jung K, Bischofs IB. 2014. A modular view of the diversity of cell-density-encoding schemes in bacterial quorum-sensing systems. Biophys J 107:266-277. http://dx.doi.org/10.1016/j.bpj.2014.05.031.
5. Bassler BL, Losick R. 2006. Bacterially speaking. Cell 125:237-246. http://dx.doi.org/10.1016/j.cell.2006.04.001.
6. Lin B, Wang Z, Malanoski AP, O'Grady EA, Wimpee CF, Vuddhakul V, Alves N, Jr, Thompson FL, Gomez-Gil B, Vora GJ. 2010. Comparative genomic analyses identify the Vibrio harveyi genome sequenced strains BAA-1116 and HY01 as Vibrio campbellii. Environ Microbiol Rep 2:81-89. http://dx.doi.org/10.1111/j.1758-2229.2009.00100.x.
7. Cao JG, Meighen EA. 1989. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem 264:21670-21676
8. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM. 2002. Structural identification of a bacterial quorumsensing signal containing boron. Nature 415:545-549. http://dx.doi.org/10.1038/415545a.
9. Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL. 2011. Signal production and detection specificity in Vibrio CqsA/CqsS quorumsensing systems. Mol Microbiol 79:1407-1417. http://dx.doi.org/10.1111/j.1365-2958.2011.07548.x.
10. Xavier KB, Bassler BL. 2003. LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191-197. http://dx.doi.org/10.1016/S1369-5274(03)00028-6.
11. Henke JM, Bassler BL. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186:6902-6914. http://dx.doi.org/10.1128/JB.186.20.6902-6914.2004.
12. Bassler BL, Greenberg EP, Stevens AM. 1997. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol 179:4043-4045
13. Anetzberger C, Reiger M, Fekete A, Schell U, Stambrau N, Plener L, Kopka J, Schmitt-Kopplin P, Hilbi H, Jung K. 2012. Autoinducers act as biological timers in Vibrio harveyi. PLoS One 7:e48310. http://dx.doi.org/10.1371/journal.pone.0048310.
14. Freeman JA, Lilley BN, Bassler BL. 2000. A genetic analysis of the functions of LuxN: a two-component hybrid sensor kinase that regulates quorum sensing in Vibrio harveyi. Mol Microbiol 35:139-149. http://dx.doi.org/10.1046/j.1365-2958.2000.01684.x.
15. Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM. 2005. Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18:507-518. http://dx.doi.org/10.1016/j.molcel.2005.04.020.
16. Freeman JA, Bassler BL. 1999. 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. http://dx.doi.org/10.1046/j.1365-2958.1999.01208.x.
17. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82. http://dx.doi.org/10.1016/j.cell.2004.06.009.
18. Lilley BN, Bassler BL. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol 36:940-954. http://dx.doi.org/10.1046/j.1365-2958.2000.01913.x.
19. Tu KC, Bassler BL. 2007. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21:221-233. http://dx.doi.org/10.1101/gad.1502407.
20. Timmen M, Bassler BL, Jung K. 2006. AI-1 influences the kinase activity but not the phosphatase activity of LuxN of Vibrio harveyi. J Biol Chem 281:24398-24404. http://dx.doi.org/10.1074/jbc. M604108200.
21. Bassler BL, Wright M, Silverman MR. 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. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00422.x.
22. Anetzberger C, Pirch T, Jung K. 2009. Heterogeneity in quorum sensingregulated bioluminescence of Vibrio harveyi. Mol Microbiol 73:267-277. http://dx.doi.org/10.1111/j.1365-2958.2009.06768.x.
23. Mok KC, Wingreen NS, Bassler BL. 2003. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22:870-881. http://dx.doi.org/10.1093/emboj/cdg085.
24. Chatterjee J, Miyamoto CM, Meighen EA. 1996. Autoregulation of luxR: the Vibrio harveyi lux-operon activator functions as a repressor. Mol Microbiol 20:415-425. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02628.x.
25. Tu KC, Waters CM, Svenningsen SL, Bassler BL. 2008. A small-RNAmediated negative feedback loop controls quorum-sensing dynamics in Vibrio harveyi. Mol Microbiol 70:896-907. http://dx.doi.org/10.1111/j.1365-2958.2008.06452.x.
26. Feng L, Rutherford ST, Papenfort K, Bagert JD, van Kessel JC, Tirrell DA, Wingreen NS, Bassler BL. 2015. A qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics. Cell 160:228-240. http://dx.doi.org/10.1016/j.cell.2014.11.051.
27. Tu KC, Long T, Svenningsen SL, Wingreen NS, Bassler BL. 2010. Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response. Mol Cell 37:567-579. http://dx.doi.org/10.1016/j.molcel.2010.01.022.
28. Teng SW, Schaffer JN, Tu KC, Mehta P, Lu W, Ong NP, Bassler BL, Wingreen NS. 2011. Active regulation of receptor ratios controls integration of quorum-sensing signals in Vibrio harveyi. Mol Syst Biol 7:491. http://dx.doi.org/10.1038/msb.2011.30.
29. Rutherford ST, van Kessel JC, Shao Y, Bassler BL. 2011. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25:397-408. http://dx.doi.org/10.1101/gad.2015011.
30. Long T, Tu KC, Wang Y, Mehta P, Ong NP, Bassler BL, Wingreen NS. 2009. Quantifying the integration of quorum-sensing signals with singlecell resolution. PLoS Biol 7:e68. http://dx.doi.org/10.1371/journal.pbio.1000068.
31. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Greenberg EP, Hastings JW, Ulitzur S. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87-91. http://dx.doi.org/10.1007/BF00409093.
33. Inoue H, Nojima H, Okayama H. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 96:23-28. http://dx.doi.org/10.1016/0378-1119(90)90336-P.
34. Lassak J, Henche AL, Binnenkade L, Thormann KM. 2010. ArcS, the cognate sensor kinase in an atypical Arc system of Shewanella oneidensis MR-1. Appl Environ Microbiol 76:3263-3274. http://dx.doi.org/10.1128/AEM.00512-10.
35. Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, Hayakawa Y, Spormann AM. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188:2681-2691. http://dx.doi.org/10.1128/JB.188.7.2681-2691.2006.
36. Thormann KM, Saville RM, Shukla S, Spormann AM. 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187:1014-1021. http://dx.doi.org/10.1128/JB.187.3.1014-1021.2005.
37. Shi X, Wegener-Feldbrugge S, Huntley S, Hamann N, Hedderich R, Sogaard-Andersen L. 2008. Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J Bacteriol 190:613-624. http://dx.doi.org/10.1128/JB.01502-07.
38. Fritz G, Koller C, Burdack K, Tetsch L, Haneburger I, Jung K, Gerland U. 2009. Induction kinetics of a conditional pH stress response system in Escherichia coli. J Mol Biol 393:272-286. http://dx.doi.org/10.1016/j.jmb.2009.08.037.
39. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. http://dx.doi.org/10.1038/nprot.2008.73.
40. Roerdink JBTM, Meijster A. 2001. The watershed transform: definitions, algorithms and parallelization strategies. Fundam Inform 41:187-228. http://dx.doi.org/10.3233/FI-2000-411207.
41. Koch AL. 1966. The logarithm in biology 1. Mechanisms generating the log-normal distribution exactly. J Theor Biol 12:276-290. http://dx.doi.org/10.1016/0022-5193(66)90119-6.
42. Lehmann EL, Romano JP. 2008. Testing statistical hypotheses. Springer, New York, NY.
43. Nackerdien ZE, Keynan A, Bassler BL, Lederberg J, Thaler DS. 2008. Quorum sensing influences Vibrio harveyi growth rates in a manner not fully accounted for by the marker effect of bioluminescence. PLoS One 3:e1671. http://dx.doi.org/10.1371/journal.pone.0001671.
44. Genin S, Denny TP. 2012. Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 50:67-89. http://dx.doi.org/10.1146/annurev-phyto-081211-173000.
45. Milton DL. 2006. Quorum sensing in vibrios: complexity for diversification. Int J Med Microbiol 296:61-71. http://dx.doi.org/10.1016/j.ijmm.2006.01.044.
46. Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26-41. http://dx.doi.org/10.1007/s13238-014-0100-x.
47. Korobkova E, Emonet T, Vilar JM, Shimizu TS, Cluzel P. 2004. From molecular noise to behavioural variability in a single bacterium. Nature 428:574-578. http://dx.doi.org/10.1038/nature02404.
48. Thattai M, van Oudenaarden A. 2004. Stochastic gene expression in fluctuating environments. Genetics 167:523-530. http://dx.doi.org/10.1534/genetics.167.1.523.