Overproduction of exopolysaccharides by an Escherichia coli K-12 rpoS mutant in response to osmotic stress

Applied and Environmental Microbiology

Volumn 75, Issue 2, 2009, Pages 483-492

  Ionescu, Michael ^a   Belkin, Shimshon ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

COLANIC ACIDS; CONSTITUTIVELY ACTIVES; DEPENDENT FUNCTIONS; DNA MICROARRAYS; ENVIRONMENTAL STRESSORS; EXO POLYSACCHARIDES; NEGATIVE SELECTIONS; NUTRIENT UTILIZATIONS; OSMOTIC STRESSES; OVEREXPRESSION; SIGMA FACTORS; STRESS RESPONSES; SYNTHESIS OF; TRANSCRIPTIONAL FUSIONS; WILD TYPES;

BIOASSAY; BIOCHIPS; ESCHERICHIA COLI; GENES; GROWTH (MATERIALS); MICROARRAYS; NUCLEIC ACIDS; ORGANIC ACIDS; POLYSACCHARIDES; STRAIN;

OSMOSIS;

BACTERIUM; ENVIRONMENTAL STRESS; GENE EXPRESSION; GROWTH RESPONSE; MUTATION; OSMOSIS; POLYMERASE CHAIN REACTION; POLYSACCHARIDE;

ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; ESCHERICHIA COLI K12; GENE DELETION; GENE EXPRESSION PROFILING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOTIC PRESSURE; POLYMERASE CHAIN REACTION; POLYSACCHARIDES; SIGMA FACTOR;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI K12;

EID: 58149379960     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01616-08     Document Type: Article

References (66)

1. Bhagwat, A. A., J. Tan, M. Sharma, M. Kothary, S. Low, B. D. Tall, and M. Bhagwat. 2006. Functional heterogeneity of RpoS stress tolerance of enterohemorrhagic Escherichia coli strains. Appl. Environ. Microbiol. 72:4978-4986.
2. Bi, E. F., and J. Lutkenhaus. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-164.
3. Carballes, F., C. Bertrand, J. P. Bouche, and K. Cam. 1999. Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol. Microbiol. 34:442-450.
4. Charette, M., G. W. Henderson, and A. Markovitz. 1981. ATP hydrolysis-dependent activity of the lon(capR) protein of E. coli K12. Proc. Natl. Acad. Sci. USA 78:4728-4732.
5. Chen, G., C. L. Patten, and H. E. Schellhorn. 2004. Positive selection for loss of RpoS function in Escherichia coli. Mutat. Res. 455:193-203.
6. Chen, J., S. M. Lee, and Y. Mao. 2004. Protective effect of exopolysaccharide colanic acid of Escherichia coli to osmotic and oxidative stress. Int. J. Food Microbiol. 93:281-286.
7. Chung, C. H., and A. L. Goldberg. 1981. The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La. Proc. Natl. Acad. Sci. USA 78:4931-4935.
8. Conter, A., R. Sturny, C. Gutierrez, and K. Cam. 2002. The RcsCB His-Asp phosphorelay system is essential to overcome chlorpromazine-induced stress in Escherichia coli. J. Bacteriol. 184:2850-2853.
9. Culham, D. E., A. Lu, M. Jishage, K. A. Krogfelt, A. Ishihama, and J. M. Wood. 2001. The osmotic stress response and virulence in pyelonephritis isolates of Escherichia coli: contributions of RpoS, ProP, ProU and other systems. Microbiology 147:1657-1670.
10. 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.
11. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
12. Dhar, A. K., M. M. Roux, and K. R. Klimpel. 2001. Detection and quantification of infectious hypodermal and hematopoietic necrosis virus and white spot virus in shrimp using real-time quantitative PCR and SYBR green chemistry. J. Clin. Microbiol. 39:2835-2845.
13. Farewell, A., K. Kvint, and T. Nystrom. 1998. Negative regulation by RpoS: a case of sigma factor competition. Mol. Microbiol. 29:1039-1051.
14. Ferenci, T. 2008. The spread of a beneficial mutation in experimental bacterial population: the influence of the environment and genotype on the fixation of rpoS mutations. Heredity 100:446-452.
15. Ferrières, L., and D. J. Clarke. 2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on solid surface. Mol. Microbiol. 50:1665-1682.
16. Ferrières, L., S. N. Aslam, R. M. Cooper, and D. J. Clarke. 2007. The yjbEFGH locus in Escherichia coli K-12 is an operon encoding proteins involved in exopolysaccharide production. Microbiology 153:1070-1080.
17. Francez-Charlot, A., B. Laugel, A. Van Gemert, N. Dubarry, F. Wiorowski, M. P. Castanié-Cornet, C. Gutierrez, and K. Cam. 2003. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49:823-832.
18. Goller, C., X. Wang, Y. Itoh, and T. Romeo. 2006. The cation-responsive protein NhaR of Escherichia coli activates pgaABCD transcription, required for production of the biofilm adhesion poly-β-1,6-N-acetyl-D-glucosamine. J. Bacteriol. 188:8022-8032.
19. Gottesman, S., P. Trisler, and A. Torres-Cabassa. 1985. Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J. Bacteriol. 162:1111-1119.
20. Grant, W. D., I. W. Sutherland, and J. F. Wilkinson. 1969. Exopolysaccharide colanic acid and its occurrence in the Enterobacteriaceae. J. Bacteriol. 100:1187-1193.
21. Hengge-Aronis, R., W. Klein, R. Lange, M. Rimmele, and W. Boos. 1991. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J. Bacteriol. 173:7918-7924.
22. Hengge-Aronis, R., R. Lange, N. Henneberg, and D. Fischer. 1993. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J. Bacteriol. 175:259-265.
23. Higashitani, A., N. Higashitani, and K. Horiuchi. 1995. A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem. Biophys. Res. Commun. 209:198-204.
24. Ionescu, M., A. Franchini, T. Egli, and S. Belkin. 2008. Induction of the yjbEFGH operon is regulated by growth rate and oxygen concentration. Arch. Microbiol. 189:219-226.
25. Jishage, M., and A. Ishihama. 1997. Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J. Bacteriol. 179:959-963.
26. Junkins, A. D., and M. P. Doyle. 1992. Demonstration of exopolysaccharide production by enterohemorrhagic Escherichia coli. Curr. Microbiol. 25:9-17.
27. Kelm, O., C. Kiecker, K. Geider, and F. Bernhard. 1997. Interaction of the regulator proteins RcsA and RcsB with the promoter of the operon for amylovoran biosynthesis in Erwinia amylovora. Mol. Gen. Genet. 256:72-83.
28. King, T., S. Seeto, and T. Ferenci. 2006. Genotyping-by- environment interaction influencing the emergence of rpoS mutations in Escherichia coli population. Genetics 172:2071-2079.
29. Kunin, C. M., T. H. Hua, L. Van Arsdale White, and M. Villarejo. 1992. Growth of Escherichia coli in human urine: role of salt tolerance and accumulation of glycine betaine. J. Infect. Dis. 166:1311-1315.
30. T method. Methods 25:402-408.
31. Loewen, P. C., and B. L. Triggs. 1984. Genetic mapping of katF, a locus that with katE affects the synthesis of a second catalase species in Escherichia coli. J. Bacteriol. 160:668-675.
32. Maeda, H., N. Fujita, and A. Ishihama. 2000. Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase. Nucleic Acids Res. 28:3497-3503.
33. Majdalani, N., and S. Gottesman. 2005. The Rcs phosphorelay: a complex signal transcription system. Annu. Rev. Microbiol. 59:379-405.
34. Mao, Y., M. P. Doyle, and J. Chen. 2006. Role of colanic acid exopolysaccharide in the survival of enterohaemorrhagic Escherichia coli O157:H7 in simulated gastrointestinal fluids. Lett. Appl. Microbiol. 42:642-647.
35. Mao, Y., M. P. Doyle, and J. Chen. 2001. Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:3811-3815.
36. Markovitz, A. 1964. Regulatory mechanisms for synthesis of capsular polysaccharide in mucoid mutants of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 51:239-246.
37. Mizusawa, S., and S. Gottesman. 1983. Protein degradation in Escherichia coli: the lon gene controls the stability of the SulA protein. Proc. Natl. Acad. Sci. USA 80:358-362.
38. Mukherjee, A., C. Cao, and J. Lutkenhaus. 1998. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:2885-2890.
39. Notley-McRobb, L., T. King, and T. Ferenci. 2002. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184:806-811.
40. Peleg, A., Y. Shifrin, O. Ilan, C. Nadler-Yona, S. Nov, S. Koby, K. Baruch, S. Altuvia, M. Elgrably-Weiss, C. M. Abe, S. Knutton, M. A. Saper, and I. Rosenshine. 2005. Identification of an Escherichia coli operon required for formation of O-antigen capsule. J. Bacteriol. 187:5259-5266.
41. 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 flagella, curli and colanic acid. Environ. Microbiol. 2:450-464.
42. Rahn, A., and C. Whitfield. 2003. Transcriptional organization and regulation of the Escherichia coli K30 group 1 capsule biosynthesis (cps) gene cluster. Mol. Microbiol. 47:1045-1060.
43. Robbe-Saule, V., G. Algorta, I. Rouihac, and F. Norel. 2003. Characterization of the RpoS status of clinical isolates of Salmonella enterica. Appl. Environ. Microbiol. 69:4352-4358.
44. Rozen, Y., T. K. Van Dyk, R. A. LaRossa, and S. Belkin. 2001. Seawater activation of Escherichia coli gene promoter elements: dominance of RpoS control. Microbiol. Ecol. 42:635-643.
45. Sagi, E., N. Hever, R. Rosen, A. J. Bartolome, J. Rajan Premkumar, R. Ulber, O. Lev, T. Scheper, and S. Belkin. 2003. Fluorescence and bioluminescence reporter functions in genetically modified bacterial sensor strains. Sens. Actuators 90:2-8.
46. Samuel, S., and P. Reeves. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519.
47. Schoemaker, J. M., R. C. Gayada, and A. Markovitz. 1984. Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death. J. Bacteriol. 158:551-561.
48. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Sledjeski, D., and S. Gottesman. 1996. Osmotic shock induction of capsular synthesis in Escherichia coli K-12. J. Bacteriol. 178:1204-1206.
50. Stout, V. 1996. Identification of the promoter region for the colanic acid polysaccharide biosynthetic genes in Escherichia coli K-12. J. Bacteriol. 178:4273-4280.
51. Stout, V., and S. Gottesman. 1990. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J. Bacteriol. 172:659-669.
52. Sutton, A., W. H. Hsing, K. E. Gibson, and A. Eisenstark. 2000. rpoS mutants in archival cultures of Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:4375-4379.
53. Takeda, S., Y. Fujisawa, M. Matsubara, H. Aiba, and T. Mizuno. 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC → YojN → RcsB signaling pathway implicated in capsular synthesis and swarming behavior. Mol. Microbiol. 40:440-450.
54. Torres-Cabassa, A. S., and S. Gottesman. 1987. Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J. Bacteriol. 169:981-989.
55. Tsilibaris, V., G. Meanhaut-Michel, and L. Van Melderen. 2006. Biological role of the Lon ATP-dependent protease. Res. Microbiol. 157:701-713.
56. Van Dyk, T. K., and R. A. Rosson. 1998. Photorhabdus luminescens luxCDABE probe vector, p. 85-95. In R. A. LaRossa (ed.), Bioluminescence methods and protocols. Humana Press, Totowa, NJ.
57. Van Dyk, T. K., Y. Wei, M. K. Hanafey, M. Dolan, M. I. J. Reeve, J. A. Rafalski, L. B. Rothman-Denes, and R. A. LaRossa. 2001. A genomic approach to gene fusion technology. Proc. Natl. Acad. Sci. USA 98:2555-2560.
58. Virlogeux, I., H. Waxin, C. Ecobichon, J. O. Lee, and M. Y. Popoff. 1996. Characterization of the rcsA and rcsB genes from Salmonella typhi: rcsB through tviA is involved in regulation of Vi antigen synthesis. J. Bacteriol. 178:1691-1698.
59. Wang, X., J. F. Preston, and T. Romeo. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186:2724-2734.
60. Weber, A., and K. Jung. 2002. Profiling early osmostress-dependent gene expression in Escherichia coli using DNA macroarrays. J. Bacteriol. 184:5502-5507.
61. s-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
62. Wehland, M., and F. Bernhard. 2000. The RcsAB box. J. Biol. Chem. 275:7013-7020.
63. Wood, J. M. 2006. Osmosensing by bacteria. Sci. STKE 357:pe43.
64. Yu, D., H. M. Ellis, E. C. Lee, N. A. Jenkins, N. G. Copeland, and D. L. Court. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. USA 97:5978-5983.
65. Yuval, B., R. Kaspi, S. Shloush, and M. S. Warburg. 1998. Nutritional reserves regulate male participation in Mediterranean fruit fly leks. Ecol. Entomol. 23:211-215.
66. Zambrano, M. M., D. A. Siegele, M. Almiron, A. Tormo, and R. Kolter. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760.