Toxin-antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae

Journal of Bacteriology

Volumn 191, Issue 4, 2009, Pages 1258-1267

  Kim, Younghoon ^a   Wang, Xiaoxue ^a   Ma, Qun ^a   Zhang, Xue Song ^a   Wood, Thomas K ^a,b  

^a Texas AandM University   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL TOXIN; HYDROGENASE; COLANIC ACID; ESCHERICHIA COLI PROTEIN; FIMBRIA PROTEIN; POLYSACCHARIDE; YJGK PROTEIN, E COLI;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIOPHAGE; BACTERIUM ADHERENCE; BACTERIUM TRANSDUCTION; BIOFILM; CELL DIVISION; CELL MOTILITY; CHPB GENE; DNA MICROARRAY; ESCHERICHIA COLI; FIMBRIA; GENE EXPRESSION; IRON TRANSPORT; MAZF GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; RELE GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; YAFQ GENE; YJGK GENE; YOEB GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BIOFILMS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; PLASMIDS; POLYSACCHARIDES; SIGNAL TRANSDUCTION;

EID: 60849133892     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01465-08     Document Type: Article

References (51)

1. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:0008.
2. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signalling in Vibrio haiveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9:773-786.
3. Bayles, K. W. 2007. The biological role of death and lysis in biofilm development. Nat. Rev. Microbiol. 5:721-726.
4. Beloin, C, and J.-M. Ghigo. 2005. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 13:16-19.
5. Braun, V., and C. Herrmann. 2007. Docking of the periplasmic FecB binding protein to the FecCD transmembrane proteins in the ferric citrate transport system of Escherichia coli. J. Bacteriol. 189:6913-6918.
6. Carmona, M., C. Balsalobre, F. Muñoa, M. Mouriño, Y. Jubete, F. De la Cruz, and A. Juárez. 1993. Escherichia coli hha mutants. DNA supercoiling and expression of the haemolysin genes from the recombinant plasmid pANN202-312. Mol. Microbiol."9:1011-1018.
7. Christensen, S. K., G. Maenhaut-Miehel, N. Mine, S. Gottesman, K. Gerdes, and L. Van Melderen. 2004. Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: involvement of the yefM-yoeB toxin-antitoxin system. Mol. Microbiol. 51:1705-1717.
8. Domka, J., J. Lee, T. Bansal, and T. K. Wood. 2007. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ. Microbiol. 9:332-346.
9. 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.
10. Engelberg-Kulka, H., S. Amitai, I. Kolodkin-Gal, and R. Hazan. 2006. Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet. 2:el35.
11. García-Contreras, R., X.-S. Zhang, Y. Kim, and T. K. Wood. 2008. Protein translation and cell death: the role of rare tRNAs in biofilm formation and in activating dormant phage killer genes. PLoS ONE 3:e2394.
12. Gerdes, K. 2000. Toxin-antitoxin modules may regulate synthesis of macro-molecules during nutritional stress. J. Bacteriol. 182:561-572.
13. Gerdes, K., S. K. Christensen, and A. Løbner-Olesen. 2005. Prokaiyotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
14. González Barrios, A. F., R. Zuo, Y. Hashimoto, L. Yang, W. E. Bentley, and T. K. Wood. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188:305-316.
15. Jackson, D. W., K. Suzuki, L. Oakford, J. W. Simecka, M. E. Hart, and T. Romeo. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184:290-301.
16. Kang, Y, T. Durfee, J. D. Glasner, Y. Qiu, D. Frisch, K. M. Winterberg, and F. R. Blattner. 2004. Systematic mutagenesis of the Escherichia coli genome. J. Bacteriol. 186:4921-4930.
17. Kitagawa, M., T. Ara, M. Arifuzzaman, T. Ioka-Nakamichi, E. Inamoto, H. Toyonaga, and H. Mori. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299.
18. Klemm, P. 1984. The fimA gene encoding the type-1 fimbrial subunit of Escherichia coli. Eur. J. Biochem. 143:395-399.
19. Landini, P., and A. J. B. Zehnder. 2002. The global regulatory hns gene negatively affects adhesion to solid surfaces by anaerobically grown Escherichia coli by modulating expression of flagellar genes and lipopolysaccharide production. J. Bacteriol. 184:1522-1529.
20. Lee, J., A. Jayaraman, and T. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7:42.
21. Lee, J., X.-S. Zhang, M. Hegde, W. E. Bentley, A. Jayaraman, and T. K. Wood. 2008. Indole cell signaling occurs primarily at low temperatures in Escherichia coli. ISME J. 2:1007-1023.
22. Lemos, J. A. C., J. T. A. Brown, J. Abranches, and R. A. Burne. 2005. Characteristics of Streptococcus mutans strains lacking the MazEF and RelBE toxin-antitoxin modules. FEMS Microbiol. Lett. 253:251-257.
23. Maeda, T., V. Sanchez-Torres, and T. K. Wood. 2008. Metabolic engineering to enhance bacterial hydrogen production. Microb. Biotechnol. 1:30-39.
24. Magnuson, R. D. 2007. Hypothetical functions of toxin-antitoxin systems. J. Bacteriol. 189:6089-6092.
25. Mai-Prochnow, A., J. S. Webb, B. C. Ferrari, and S. Kjelleberg. 2006. Ecological advantages of autolysis during the development and dispersal of Pseudoalteromonas tunicata biofilms. Appl. Environ. Microbiol. 72:5414-5420.
26. Mikulskis, A. V., and G. R. Cornetis. 1994. A new class of proteins regulating gene expression in enterobacteria. Mol. Microbiol. 11:77-86.
27. Morgan, R., S. Kohn, S.-H. Hwang, D. J. Hassett, and K. Sauer. 2006. BdlA, a Chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J. Bacteriol. 188:7335-7343.
28. Pecota, D. C, and T. K. Wood. 1996. Exclusion of T4 phage by the hok/sok killer locus from plasmid Rl. J. Bacteriol. 178:2044-2050.
29. Pedersen, K,, and K. Gerdes. 1999. Multiple hok genes on the chromosome of Escherichia coli. Mol. Microbiol. 32:1090-1102.
30. 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.
31. Ren, D., L. A. Bedzyk, S. M. Thomas, R. W. Ye, and T. K. Wood. 2004. Gene expression in Escherichia coli biofilms. Appl. Microbiol. Biotechnol. 64:515-524.
32. Ren, D., L. A. Bedzyk, R. W. Ye, S. M. Thomas, and T. K. Wood. 2004. Stationary-phase quorum-sensing signals affect autoinducer-2 and gene expression in Escherichia coli. Appl. Environ. Microbiol. 70:2038-2043.
33. Ren, D., L. A. Bedzyk, R. W. Ye, S. M. Thomas, and T. K. Wood. 2004. Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol. Bioeng. 88:630-642.
34. Rodionov, D. A., M. S. Gelfand, and N. Hugouvieux-Cotte-Pattat. 2004. Comparative genomics of the KdgR regulon in Erwinia chrysanthemi 3937 and other gamma-proteobacteria. Microbiology 150:3571-3590.
35. Romeo, T. 2006. When the parly is over: a signal for dispersal of Pseudomonas aeruginosa biofilms. J. Bacteriol. 188:7325-7327.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press. Cold Spring Harbor. NY.
37. Schembri, M. A., and P. Klemm. 2001. Biofilm formation in a hydrodynamic environment by novel FimH variants and ramifications for virulence. Infect. Immun. 69:1322-1328.
38. Shah, D., Z. Zhang, A. Khodursky, N. Kaldalu, K. Kurg, and K. Lewis. Persisters: a distinct physiological state of Escherichia coli. BMC Microbiol. 6:53, 2006.
39. Teplyakov, A., G. Obmolova, J. Toedt, M. Y. Galperin, and G. L. Gilliland. 2005. Crystal structure of the bacterial YhcH protein indicates a role in sialic acid catabolism. J. Bacteriol. 187:5520-5527.
40. Tsilibaris, V., G. Maenhaut-Michel, N. Mine, and L. Van Melderen. 2007. What is the benefit to Escherichia coli of having multiple toxin-antitoxin systems in its genome? J. Bacteriol. 189:6101-6108.
41. Valenski, M. L., S. L. Harris, P. A. Spears, J. R. Horton, and P. E. Orndorff. 2003. The product of the fiml gene is necessary for Escherichia coli type 1 pilus biosynthesis. J. Bacteriol. 185:5007-5011.
42. van Houdt, R., and C. W. Michiels. 2005. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 156:626-633.
43. Vogel, J., V. Bartels, T. H. Tang, G. Churakov, J. G. Slagter-Jäger, A. Hüttenhofer, and E. G. H. Wagner. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31:6435-6443.
44. Wang, L., Y. Hashimoto, 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.
45. Wang, X., A. K. Dubey, K. Suzuki, C. S. Baker, P. Babitzke, and T. Romeo. 2005. CsrA posttranscriptionally represses pgaABCD. responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol. Microbiol. 56:1648-1663.
46. Webb, J. S., L. S. Thompson, S, James, T. Charlton, T. Tolker-Nielsen, B. Koch, M. Givskov, and S. Kjelleberg. 2003. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185:4585-4592.
47. Wood, T. K., and S. W. Peretti. 1991. Effect of chemically-induced, cloned-gene expression on protein synthesis in E. coli. Biotechnol. Bioeng. 38:397-412.
48. Yew, W. S., and J. A. Gerlt. 2002. Utilization of l- ascorbate by Escherichia coli K-12: assignments of functions to products of the yjf-sga and yia-sgb operons. J. Bacteriol. 184:302-306.
49. Zhang, X.-S., R. García-Contreras, and T. K. Wood. 2008. Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA). ISME J, 2:615-631.
50. Zhang, X.-S., R. García-Contreras, and T. K. Wood. 2007. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J. Bacteriol. 189:3051-3062.
51. Zheng, M., X. Wang, L. J. Templeton, D. R. Smulski, R. A. LaRossa, and G. Storz. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562-4570.