Polyphosphate kinase protects Salmonella enterica from weak organic acid stress

Journal of Bacteriology

Volumn 187, Issue 9, 2005, Pages 3088-3099

  Price Carter, Marian ^a   Fazzio, Thomas G ^a,c   Vallbona, Ester Ibañez ^a,d   Roth, John R ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACID; HOMOSERINE; METHIONINE; PHOSPHOTRANSFERASE; POLYPHOSPHATE KINASE; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GROWTH INHIBITION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN EXPRESSION; SALMONELLA ENTERICA;

ACIDS; ACYLTRANSFERASES; ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; CLONING, MOLECULAR; ENZYME STABILITY; GENE DELETION; HOMOSERINE O-SUCCINYLTRANSFERASE; HYDROGEN PEROXIDE; METHIONINE; MUTAGENESIS, INSERTIONAL; PHOSPHOTRANSFERASES (PHOSPHATE GROUP ACCEPTOR); POLYPHOSPHATES; PROTEIN DENATURATION; SALMONELLA ENTERICA; SIGMA FACTOR;

SALMONELLA ENTERICA;

EID: 17644423441     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.9.3088-3099.2005     Document Type: Article

References (64)

1. Aikiyama, M., E. Crook, and A. Kornberg. 1992. The polyphosphate gene of Escherichia coli. Isolation and sequence of the ppk gene and membrane localization of the protein. J. Biol. Chem. 267:22556-22561.
2. Arnold, C. N., J. McElhanon, A. Lee, R. Leonhart, and D. A. Siegele. 2001. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J. Bacteriol. 183:2178-2186.
3. Audia, J. P., C. C. Webb, and J. W. Foster. 2001. Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int. J. Med. Microbiol. 291:97-106.
4. Ault-Riche, D., C. D. Fraley, C. Tzeng, and A. Kornberg. 1998. Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180:1841-1847.
5. Biran, D., E. Gur, L. Gollan, and E. Z. Ron. 2000. Control of methionine biosynthesis in Escherichia coli by proteolysis. Mol. Microbiol. 37:1436-1443.
6. Blankenhorn, D., J. Phillips, and J. L. Slonczewski. 1999. Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J. Bacteriol. 181:2209-2216.
7. 12 synthesis and propanediol degradation. J. Bacteriol. 174:2253-2266.
8. 12-dependent 1,2-propanediol degradation. J. Bacteriol. 181:5967-5975.
9. Born, T. L., and J. S. Blanchard. 1999. Enzyme-catalyzed acylation of homoserine: mechanistic characterization of the Escherichia coli metA-encoded homoserine transsuccinylase. Biochemistry 38:14416-14423.
10. Brinsmade, S. R., and J. C. Escalante-Semerena. 2004. The eutD gene of Salmonella enterica encodes a protein with phosphotransacetylase enzyme activity. J. Bacteriol. 186:1890-1892.
11. Brown, L., and T. Elliott. 1996. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J. Bacteriol. 178:3763-3770.
12. Brown, M., and A. Kornberg. 2004. Inorganic phosphate in the origin and survival of species. Proc. Natl. Acad. Sci. USA 101:16085-16087.
13. Creighton, T. E. 1993. Proteins: structure and molecular properties, 2nd ed. W.H. Freeman and Co., New York, N.Y.
14. Crook, E., M. Aikiyama, N. N. Rao, and A. Kornberg. 1994. Genetically altered levels of inorganic polyphosphate in Escherichia coli. S. Biol. Chem. 269:6290-6295.
15. Davis, R. W. 1980. A manual for genetic engineering: advanced bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
16. Dukan, S., A. Farewell, M. Ballestros, F. Taddei, M. Radman, and T. Nystrom. 2000. Protein oxidation in response to increased transcriptional or translational errors. Proc. Natl. Acad. Sci. USA 97:5746-5749.
17. Dukan, S., and T. Nystrom. 1998. Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev. 12:3431-3441.
18. Dukan, S., and T. Nystrom. 1999. Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells. J. Biol. Chem. 274:26027-26032.
19. Fazzio, T., and J. Roth. Unpublished data.
20. Ferguson, G. P., D. McLaggan, and I. R. Booth. 1995. Potassium channel activation by glutathione-S-conjugates in Escherichia coli: protection against methylglyoxal is mediated by cytoplasmic acidification. Mol. Microbiol. 17:1025-1033.
21. Giandomenico, A. R., G. E. Cerniglia, J. E. Biaglow, C. W. Stevens, and C. J. Koch. 1997. The importance of sodium pyruvate in assessing the damage produced by hydrogen peroxide. Free Radical Biol. Med. 23:426-434.
22. Greene, R. C. 1996. Biosynthesis of methionine, p. 542-560. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
23. Gur, E., D. Biran, E. Gazit, and E. Z. Ron. 2002. In vivo aggregation of a single enzyme limits growth of Escherichia coli at elevated temperatures. Mol. Microbiol. 46:1391-1397.
24. 12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar Typhimurium LT2. J. Bacteriol. 184:1253-1261.
25. Hondorp, E., and R. Matthews. 2004. Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol. 2:1738-1753.
26. Horswill, A. R., A. R. Dudding, and J. C. Escalante-Semerena. 2001. Studies of propionate toxicity in Salmonella enterica identify 2-methylcitrate as a potent inhibitor of cell growth. J. Biol. Chem. 276:19094-19101.
27. Hughes, K. T., and J. R. Roth. 1988. Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics 119:9-12.
28. Imlay, J. A., S. M. Chin, and S. Linn. 1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640-642.
29. Kim, K., N. N. Rao, C. D. Fraley, and A. Kornberg. 2002. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc. Natl. Acad. Sci. USA 99:7675-7680.
30. Kofoid, E. C., C. Rappleye, I. Stojiljkovic, and J. R. Roth. 1999. The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologs of carboxysome shell proteins. J. Bacteriol. 181:5317-5329.
31. Kornberg, A., N. N. Rao, and D. Ault-Riche. 1999. Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68:89-125.
32. Kuroda, A., K. Nomura, R. Ohtomo, J. Kato, T. Ikeda, N. Takiguchi, H. Ohtake, and A. Kornberg. 2001. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293:705-708.
33. Kuroda, A., S. Tanaka, T. Ikeda, J. Kato, N. Takiguchi, and H. Ohtake. 1999. Inorganic polyphosphate kinase is required to stimulate protein degradation and for adaptation to amino acid starvation in Escherichia coli. Proc. Natl. Acad. Sci. USA 96:14264-14269.
34. Kwon, Y. M., and S. C. Ricke. 1998. Induction of acid resistance of Salmonella typhimurium by exposure to short-chain fatty acids. Appl. Environ. Microbiol. 64:3458-3463.
35. Lambert, L. A., K. Abshire, D. Blankenhorn, and J. L. Slonczewski. 1997. Proteins induced in Escherichia coli by benzoic acid. J. Bacteriol. 179:7595-7599.
36. Loewen, P. C., B. Hu, J. Strutinsky, and R. Sparling. 1998. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44:707-717.
37. Mori, K., R. Bando, N. Hieda, and T. Toraya. 2004. Identification of a reactivating factor for adenosylcobalamin-dependent ethanolamine ammonia lyase. 186:6845-6854.
38. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
39. Oikawa, S., and S. Kawanishi. 1996. Site-specific damage induced by NADH in the presence of copper(II): role of active oxygen species. Biochemistry 35:4584-4590.
40. Penrod, J., T. Fazzio, C. Mace, E. C. Kofoid, and J. R. Roth. Unpublished data.
41. 12-dependent anaerobic growth of Salmonella enterica serovar Typhimurium on ethanolamine or 1,2-propanediol. J. Bacteriol. 183:2463-2475.
42. Rao, N. N., and A. Kornberg. 1996. Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J. Bacteriol. 178:1394-1400.
43. Rappleye, C., and J. R. Roth. 1997. A Tn10 derivative (TPOP) for isolation of insertions with conditional (tetracycline-dependent) phenotypes. J. Bacteriol. 179:5827-5834.
44. Roe, A. J., D. McLaggan, I. Davidson, C. O'Byrne, and I. R. Booth. 1998. Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J. Bacteriol. 180:767-772.
45. Roe, A. J., C. O'Byrne, D. McLaggan, and I. R. Booth. 2002. Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity. Microbiology 148:2215-2222.
46. Ron, E. Z. 1975. Growth rate of Enterobacteriaceae at elevated temperatures: limitation by methionine. J. Bacteriol. 124:243-246.
47. Ron, E. Z., and B. D. Davis. 1971. Growth rate of Escherichia coli at elevated temperatures: limitation by methionine. J. Bacteriol. 107:391-396.
48. Ron, E. Z., and M. Shani. 1971. Growth rate of Escherichia coli at elevated temperatures: reversible inhibition of homoserine trans-succinylase. J. Bacteriol. 107:397-400.
49. Roof, D. M., and J. R. Roth. 1988. Ethanolamine utilization in Salmonella typhimunum. J. Bacteriol. 170:3855-3863.
50. Russell, J. B., and F. Diez-Gonzalez. 1998. The effects of fermentation acids on bacterial growth. Adv. Microb. Physiol. 39:205-234.
51. Salmond, C. V., R. Kroll, and I. R. Booth. 1984. The effect of food preservatives on pH homeostasis in Escherichia coli. J. Gen. Microbiol. 130:2845-2850.
52. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
53. Schellhorn, H. E., and V. L. Stones. 1992. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J. Bacteriol. 174:4769-4776.
54. Schmieger, H. 1971. A method of detection of phage mutants with altered transducing ability. Mol. Gen. Genet. 110:378-381.
55. Seaver, L. C., and J. A. Imlay. 2001. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183:7182-7189.
56. 12-adenosyl transferase is encoded within the ethanolamine operon of Salmonella enterica. J. Bacteriol. 186:7635-7644.
57. Shiba, T., K. Tsutsumi, H. Yano, Y. Ihara, A. Kameda, S. Tanaka, H. Takahashi, M. Munekata, N. N. Rao, and A. Kornberg. 1997. Inorganic polyphosphate and the induction of rpoS expression. Proc. Natl. Acad. Sci. USA 94:11210-11215.
58. Shively, J., and R. English. 1991. The carboxysome, a prokaryotic organelle: a mini review. Can. J. Bot. 69:957-963.
59. Stadtman, E. R. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62:797-821.
60. Tomoyasu, T., A. Mogk, H. Langen, P. Goloubinoff, and B. Bukau. 2001. Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol. Microbiol. 40:397-413.
61. Tsutsumi, K., M. Munekata, and T. Shiba. 2000. Involvement of inorganic polyphosphate in expression of SOS genes. Biochim. Biophys. Acta 1493:73-81.
62. Van Dien, S. J., S. Keyhani, C. Yang, and J. D. Keasling. 1997. Manipulation of independent synthesis and degradation of polyphosphate in Escherichia coli for investigation of phosphate secretion from the cell. Appl. Environ. Microbiol. 63:1689-1695.
63. Van Niel, E. W. J., K. Hofvendahl, and B. Hahn-Hägerdal. 2002. Formation and conversion of oxygen metabolites by Lactococcus lactis subsp. lactis ATCC 19435 under different growth conditions. Appl. Environ. Microbiol. 68:4350-4356.
64. Wickner, S., M. R. Maurizi, and S. Gottesman. 1999. Posttranslational quality control: folding, refolding, and degrading proteins. Science 286:1888-1893.