Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: Effects on small RNA and biofilm architecture

Journal of Bacteriology

Volumn 189, Issue 16, 2007, Pages 6011-6020

  Li, Jun ^a,c   Attila, Can ^e   Wang, Liang ^a,d   Wood, Thomas K ^e   Valdes, James J ^f   Bentley, William E ^a,b,c  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d Bldg 142   (United States)

^e Texas AandM University   (United States)

^f EDGEWOOD CHEMICAL BIOLOGICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CARRIER PROTEIN; PROTEIN LSRR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BIOFILM; ESCHERICHIA COLI; GENE DELETION; LSRK GENE; LSRR GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUORUM SENSING; REGULON; REPRESSOR GENE; SIGNAL TRANSDUCTION;

BIOFILMS; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; LACTONES; QUORUM SENSING; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI; VIBRIO HARVEYI;

EID: 34547768760     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00014-07     Document Type: Article

References (75)

1. Aarsman, M. E., A. Piette, C. Fraipont, T. M. Vinkenvleugel, M. Nguyen-Disteche, and T. den Blaauwen. 2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55:1631-1645.
2. Ahmer, B. M. 2004. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52:933-945.
3. Anton, B. P., and E. A. Raleigh. 2004. Transposon-mediated linker insertion scanning mutagenesis of the Escherichia coli McrA endonuclease. J. Bacteriol. 186:5699-5707.
4. Barnhart, M. M., and M. R. Chapman. 2006. Curli biogenesis and function. Annu. Rev. Microbiol. 60:131-147.
5. Beeston, A. L., and M. G. Surette. 2002. pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:3450-3456.
6. Beis, K., R. F. Collins, R. C. Ford, A. B. Kamis, C. Whitfield, and J. H. Naismith. 2004. Three-dimensional structure of Wza, the protein required for translocation of group 1 capsular polysaccharide across the outer membrane of Escherichia coli. J. Biol. Chem. 279:28227-28232.
7. Bouche, F., and J. P. Bouche. 1989. Genetic evidence that DicF, a second division inhibitor encoded by the Escherichia coli dicB operon, is probably RNA. Mol. Microbiol. 3:991-994.
8. Brescia, C. C., P. J. Mikulecky, A. L. Feig, and D. D. Sledjeski. 2003. Identification of the Hfq-binding site on DsrA RNA: Hfq binds without altering DsrA secondary structure. RNA 9:33-43.
9. Cam, K., A. Cuzange, and J. P. Bouche. 1995. Sigma S-dependent overexpression of ftsZ in an Escherichia coli K-12 rpoB mutant that is resistant to the division inhibitors DicB and DicF RNA. Mol. Gen. Genet. 248:190-194.
10. Camilli, A., and B. L. Bassler. 2006. Bacterial small-molecule signaling pathways. Science 311:1113-1116.
11. Canales, R. D., Y. Luo, J. C. Willey, B. Austermiller, C. C. Barbacioru, C. Boysen, K. Hunkapiller, R. V. Jensen, C. R. Knight, K. Y. Lee, Y. Ma, B. Maqsodi, A. Papallo, E. H. Peters, K. Poulter, P. L. Ruppel, R. R. Samaha, L. Shi, W. Yang, L. Zhang, and F. M. Goodsaid. 2006. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotechnol. 24:1115-1122.
12. Chen, J. C., and J. Beckwith. 2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42:395-413.
13. Chen, S., E. A. Lesnik, T. A. Hall, R. Sampath, R. H. Griffey, D. J. Ecker, and L. B. Blyn. 2002. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 65:157-177.
14. Chen, S., A. Zhang, L. B. Blyn, and G. Storz. 2004. MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J. Bacteriol. 186:6689-6697.
15. Chen, Y. W., P. Zhao, R. Borup, and E. P. Hoffman. 2000. Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J. Cell Biol. 151:1321-1336.
16. Danese, P. N., L. A. Pratt, S. L. Dove, and R. Kolter. 2000. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol. Microbiol. 37:424-432.
17. Danese, P. N., L. A. Pratt, and R. Kolter. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182:3593-3596.
18. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
19. De Keersmaecker, S. C., K. Sonck, and J. Vanderleyden. 2006. Let LuxS speak up in AI-2 signaling. Trends Microbiol. 14:114-119.
20. DeLisa, M. P., and W. E. Bentley. 2002. Bacterial autoinduction: looking outside the cell for new metabolic engineering targets. Microb. Cell Fact. 1:5.
21. DeLisa, M. P., J. J. Valdes, and W. E. Bentley. 2001. Quorum signaling via AI-2 communicates the "metabolic burden" associated with heterologous protein production in Escherichia coli. Biotechnol. Bioeng. 75:439-450.
22. Domka, J., J. Lee, and T. K. Wood. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72:2449-2459.
23. Drummelsmith, J., and C. Whitfield. 1999. Gene products required for surface expression of the capsular form of the group 1 K antigen in Escherichia coli (O9a:K30). Mol. Microbiol. 31:1321-1332.
24. Drummelsmith, J., and C. Whitfield. 2000. Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J. 19:57-66.
25. Faubladier, M., and J. P. Bouche. 1994. Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes. J. Bacteriol. 176:1150-1156.
26. Francetic, O., D. Belin, C. Badaut, and A. P. Pugsley. 2000. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. EMBO J. 19:6697-6703.
27. Fuqua, W. C., S. C. Winans, and E. P. Greenberg. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176:269-275.
28. Genin, S., and C. A. Boucher. 1994. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet. 243:112-118.
29. Hale, C. A., and P. A. de Boer. 2002. ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J. Bacteriol. 184:2552-2556.
30. Hammer, B. K., and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101-104.
31. Hardie, K. R., C. Cooksley, A. D. Green, and K. Winzer. 2003. Autoinducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase, LuxS. Microbiology 149:715-728.
32. Hasman, H., T. Chakraborty, and P. Klemm. 1999. Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J. Bacteriol. 181:4834-4841.
33. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
34. Henke, J. M., and B. L. Bassler. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemotyticus. J. Bacteriol. 186: 3794-3805.
35. Herzberg, M., I. K. Kaye, W. Peti, and T. K. Wood. 2006. YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J. Bacteriol. 188:587-598.
36. Houdt, R., A. Aertsen, P. Moons, K. Vanoirbeek, and C. W. Michiels. 2006. N-Acyl-L-homoserine lactone signal interception by Escherichia coli. FEMS Microbiol. Lett. 256:83-89.
37. Ichikawa, J. K., A. Norris, M. G. Bangera, G. K. Geiss, A. B. van 't Wout, R. E. Bumgarner, and S. Lory. 2000. Interaction of Pseudomonas aeruginosa with epithelial cells: identification of differentially regulated genes by expression microarray analysis of human cDNAs. Proc. Natl. Acad. Sci. USA 97:9659-9664.
38. Keller, L., and M. G. Surette. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4:562.
39. Kjaergaard, K., M. A. Schembri, C. Ramos, S. Molin, and P. Klemm. 2000. Antigen 43 facilitates formation of multispecies biofilms. Environ. Microbiol. 2:695-702.
40. Lease, R. A., and M. Belfort. 2000. A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl. Acad. Sci. USA 97:9919-9924.
41. Lease, R. A., D. Smith, K. McDonough, and M. Belfort. 2004. The small noncoding DsrA RNA is an acid resistance regulator in Escherichia coli. J. Bacteriol. 186:6179-6185.
42. Lenz, D. H., K. C. Mok, B. N. Lilley, R. V. Kulkarni, N. S. Wingreen, and B. L. Bassler. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82.
43. Li, J., L. Wang, Y. Hashimoto, C. Y. Tsao, J. J. Valdes, T. K. Wood, E. Zafiriou, and W. E. Bentley. 2006. A stochastic model of Escherichia, coli AI-2 quorum signal circuit reveals alternative synthesis pathways. Mol. Syst. Biol. 2:1-16.
44. Majdalani, N., C. Cunning, D. Sledjeski, T. Elliott, and S. Gottesman. 1998. DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. USA 95:12462-12467.
45. March, J. C., and W. E. Bentley. 2004. Quorum sensing and bacterial cross-talk in biotechnology. Curr. Opin. Biotechnol. 15:495-502.
46. Moll, I., T. Afonyushkin, O. Vytvytska, V. R. Kaberdin, and U. Blasi. 2003. Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9:1308-1314.
47. Nesper, J., C. M. Hill, A. Paiment, G. Harauz, K. Beis, J. H. Naismith, and C. Whitfield. 2003. Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. Structural and functional analysis of the outer membrane lipoprotein Wza. J. Biol. Chem. 278:49763-49772.
48. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
49. Parra-Lopez, C., M. T. Baer, and E. A. Groisman. 1993. Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J. 12:4053-4062.
50. Prigent-Combaret, C., G. Prensier, T. T. Le Thi, O. Vidal, P. Lejeune, and C. Dorel. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of fiagella, curli and colanic acid. Environ. Microbiol. 2:450-464.
51. Raina, S., D. Missiakas, L. Baird, S. Kumar, and C. Georgopoulos. 1993. Identification and transcriptional analysis of the Escherichia coli htrE operon which is homologous to pap and related pilin operons. J. Bacteriol. 175:5009-5021.
52. Reid, A. N., and C. Whitfield. 2005. Functional analysis of conserved gene products involved in assembly of Escherichia coli capsules and exopolysaccharides: evidence for molecular recognition between Wza and Wzc for colanic acid biosynthesis. J. Bacteriol. 187:5470-5481.
53. Reisner, A., J. A. Haagensen, M. A. Schembri, E. L. Zechner, and S. Molin. 2003. Development and maturation of Escherichia coli K-12 biofilms. Mol. Microbiol. 48:933-946.
54. Robinson, L. S., E. M. Ashman, S. J. Hultgren, and M. R. Chapman. 2006. Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol. Microbiol. 59:870-881.
55. Sauvonnet, N., P. Gounon, and A. P. Pugsley. 2000. PpdD type IV pilin of Escherichia coli K-12 can be assembled into pili in Pseudomonas aeruginosa. J. Bacteriol. 182:848-854.
56. Sauvonnet, N., G. Vignon, A. P. Pugsley, and P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
57. Sitnikov, D. M., J. B. Schineller, and T. O. Baldwin. 1996. Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and sdiA-mediated autoinduction. Proc. Natl. Acad. Sci. USA 93:336-341.
58. Sledjeski, D., and S. Gottesman. 1995. A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc. Natl. Acad. Sci. USA 92:2003-2007.
59. Sledjeski, D. D., C. Whitman, and A. Zhang. 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 183:1997- 2005.
60. Sonnleitner, E., J. Napetschnig, T. Afonyushkin, K. Ecker, B. Vecerek, I. Moll, V. R. Kaberdin, and U. Blasi. 2004. Functional effects of variants of the RNA chaperone Hfq. Biochem. Biophys. Res. Commun. 323:1017-1023.
61. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003. Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. USA 100:8951-8956.
62. Taga, M. E., S. T. Miller, and B. L. Bassler. 2003. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50:1411-1427.
63. Tetart, F., R. Albigot, A. Conter, E. Mulder, and J. P. Bouche. 1992. Involvement of FtsZ in coupling of nucleoid separation with septation. Mol. Microbiol. 6:621-627.
64. Tetart, F., and J. P. Bouche. 1992. Regulation of the expression of the cell-cycle gene ftsZ by DicF antisense RNA. Division does not require a fixed number of FtsZ molecules. Mol. Microbiol. 6:615-620.
65. Vendeville, A., K. Winzer, K. Heurlier, C. M. Tang, and K. R. Hardie. 2005. Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3:383-396.
66. Ventre, I., A. L. Goodman, I. Vallet-Gely, P. Vasseur, C. Soscia, S. Molin, S. Bleves, A. Lazdunski, S. Lory, and A. Filloux. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. USA 103:171-176.
67. Vicente, M., and A. I. Rico. 2006. The order of the ring: assembly of Escherichia coli cell division components. Mol. Microbiol. 61:5-8.
68. Walters, M., and V. Sperandio. 2006. Quorum sensing in Escherichia coli and Salmonella. Int. J. Med. Microbiol. 296:125-131.
69. Wang, L., Y. Hashimato, C. Y. Tsao, J. J. Valdes, and W. E. Bentley. 2005. Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J. Bacteriol. 187:2066-2076.
70. Wang, L., J. Li, J. C. March, J. J. Valdes, and W. E. Bentley. 2005. luxS-dependent gene regulation in Escherichia coli K-12 revealed by genomic expression profiling. J. Bacteriol. 187:8350-8360.
71. Wassarman, K. M., F. Repoila, C. Rosenow, G. Storz, and S. Gottesman. 2001. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev. 15:1637-1651.
72. Whitfield, C., and A. Paiment. 2003. Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr. Res. 338:2491-2502.
73. Winzer, K., K. R. Hardie, and P. Williams. 2003. LuxS and autoinducer-2: their contribution to quorum sensing and metabolism in bacteria. Adv. Appl. Microbiol. 53:291-396.
74. Xavier, K. B., and B. L. Bassler. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191-197.
75. Xavier, K. B., and B. L. Bassler. 2005. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187:238-248.