Acid- and multistress-resistant mutants of Lactococcus lactis: Identification of intracellular stress signals

Molecular Microbiology

Volumn 35, Issue 3, 2000, Pages 517-528

  Rallu, Fabien ^a   Gruss, Alexandra ^b   Ehrlich, S Dusko ^a   Maguin, Emmanuelle ^a  

^a Lab de Genet Microbienne   (France)

^b CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE; LACTIC ACID; PHOSPHATE;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM MUTANT; LACTOCOCCUS LACTIS; NONHUMAN; PH; PHENOTYPE; PRIORITY JOURNAL;

ACIDS; ADAPTATION, PHYSIOLOGICAL; ATP-BINDING CASSETTE TRANSPORTERS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI PROTEINS; GUANINE NUCLEOTIDES; HEAT-SHOCK RESPONSE; LACTOCOCCUS LACTIS; MUTATION; OXIDATIVE STRESS; PERIPLASMIC BINDING PROTEINS; PHOSPHATE-BINDING PROTEINS; PHOSPHATES; PURINES; SELECTION (GENETICS); SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION;

ANIMALIA; BACTERIA (MICROORGANISMS); LACTOCOCCI; LACTOCOCCI LACTIS; LACTOCOCCUS LACTIS; POSIBACTERIA; STREPTOCOCCUS;

EID: 0033974439     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01711.x     Document Type: Article

References (82)

1. Aizenman, E., Engelberg-Kulka, H., and Glaser, G. (1996) An Escherichia coli chromosomal 'addiction module' regulated by 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc Natl Acad Sci USA 93: 6059-6063.
2. Alonso, J.C., Stiege, A.C., and Luder, G. (1993) Genetic recombination in Bacillus subtilis 168: effect of recN, recF, recH and addAB mutations on DNA repair and recombination. Mol Gen Genet 239: 129-136.
3. Bearson, S.M., Benjamin, Jr, W.H., Swords, W.E., and Foster, J.W. (1996) Acid shock induction of RpoS is mediated by the mouse virulence gene mviA of Salmonella typhimurium. J Bacteriol 178: 2572-2579.
4. Bearson, B.L., Wilson, L., and Foster, J.W. (1998) A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180: 2409-2417.
5. Cashel, M., Gentry, D.R., Hernandez, V.J., and Vinella, D. (1996) The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press, pp. 1458-1496.
6. Casiano-Colon, A., and Marquis, R.E. (1988) Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microbiol 54: 1318-1324.
7. Crow, V.L., and Thomas, T.D. (1982) Arginine metabolism in lactic streptococci. J Bacteriol 150: 1024-1032.
8. Crowley, P.J., Gutierrez, J.A., Hillman, J.D., and Bleiweis, A.S. (1997) Genetic and physiologic analysis of a formyl-tetrahydrofolate synthetase mutant of Streptococcus mutans. J Bacteriol 179: 1563-1572.
9. Curran, T.M., Lieou, J., and Marquis, R.E. (1995) Arginine deiminase system and acid adaptation of oral streptococci. Appl Environ Microbiol 61: 4494-4496.
10. Drici-Cachon, Z., Guzzo, J., Cavin, J.-F., and Diviès, C. (1996) Acid tolerance in Leuconostoc oenos. Isolation and characterization of an acid-resistant mutant. Appl Microbiol Biotechnol 44: 785-789.
11. Duwat, P., Cochu, A., Ehrlich, S.D., and Gruss, A. (1997) Characterization of Lactococcus lactis UV-sensitive mutants obtained by ISS1 transposition. J Bacteriol 179: 4473-4479.
12. Duwat, P., Ehrlich, S.D., and Gruss, A. (1999) Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol Microbiol 31: 845-858.
13. Eymann, C., Mach, H., Harwood, C.R., and Hecker, M. (1996) Phosphate-starvation-inducible proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study. Microbiology 142: 3163-3170.
14. Foster, J.W., and Bearson, B. (1994) Acid-sensitive mutants of Salmonella typhimurium identified through a dinitrophenol lethal screening strategy. J Bacteriol 176: 2596-2602.
15. Foster, J.W., and Hall, H.K. (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173: 5129-5135.
16. Gasson, M. (1983) Plasmid complements of Streptococcus lactis NCDO712 and other lactic streptococci after protoplast induced curing. J Bacteriol 154: 1-9.
17. Hahn, K., Faustoferri, R.C., and Quivey, Jr, R.J. (1999) Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH. Mol Microbiol 31: 1489-1498.
18. Hall, H.K., Karem, K.L., and Foster, J.W. (1995) Molecular responses of microbes to environmental pH stress. Adv Microb Physiol 37: 229-272.
19. Hanahan, D. (1985) Techniques for transformation of E. coli. In DNA Cloning: a Practical Approach. Glover J.M. (ed.). Washington, DC: IRL Press, pp. 109-135.
20. Hartke, A., Bouché, S., Gansel, X., Boutibonnes, P., and Auffray, Y. (1994) Starvation-induced stress resistance in Lactoccocus lactis subsp. lactis IL1403. App Environ Microbiol 60: 3474-3478.
21. Hartke, A., Bouché, S., Giard, J.C., Benachour, A., Boutibonnes, P., and Auffray, Y. (1996) The lactic acid stress response of Lactococcus lactis subsp. lactis. Curr Microbiol 33: 194-199.
22. Hartke, A., Frere, J., Boutibonnes, P., and Auffray, Y. (1997) Differential induction of the chaperonin GroEL and the co-chaperonin GroES by heat, acid, and UV-irradiation in Lactococcus lactis subsp. lactis. Curr Microbiol 34: 23-26.
23. Hecker, M., Völker, U., and Heim, C. (1989) RelA-independent (p)ppGpp accumulation and heat shock protein induction after salt stress in Bacillus subtilis. FEMS Microbiol Lett 58: 125-128.
24. Holo, H., and Nes, I.F. (1989) High frequency transformation by electroporation of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 55: 3119-3123.
25. Hutkins, R.W., and Nannen, N.L. (1993) pH homeostasis in lactic acid bacteria. J Dairy Sci 76: 2354-2365.
26. Ikehara, K., Okada, H., Maeda, K., Ogura, A., and Sugae, K. (1984) Accumulation of reIA gene-independent ppGpp in Bacillus subtilis vegetative cells upon temperature shift-down. J Biochem 95: 895-897.
27. Jensen, P.R., and Hammer, K. (1993) Minimal requirements for exponential growth of Lactococcus lactis. Appl Environ Microbiol 59: 4363-4366.
28. Karimi, R., Pavlov, M.Y., Buckingham, R.H., and Ehrenberg, M. (1999) Novel roles for classical factors at the interface between translation termination and initiation. Mol Cells 3: 601-609.
29. Kim, S.W., Ren, J., and Dunn, N.W. (1999) Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol Lett 171: 57-65.
30. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
31. Langella, P., and Chopin, A. (1989) Effect of restriction-modification system on transfer of foreign DNA in Lactococus lactis subsp. lactis. FEMS Microbiol Lett 60: 149-152.
32. Leenhouts, K. (1995) Integration strategies and vectors. Dev Biol Standards 85: 523-530.
33. Leloup, L., Ehrlich, S.D., Zagorec, M., and Morel-Deville, F. (1997) Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsl and lacL genes. Appl Environ Microbiol 63: 2117-2123.
34. Luchin, S., Putzer, H., Hershey, J.W., Cenatiempo, Y., Grunberg-Manago, M., and Laalami, S. (1999) In vitro study of two dominant inhibitory GTPase mutants of Escherichia coli translation initiation factor IF2. Direct evidence that GTP hydrolysis is necessary for factor recycling. J Biol Chem 274: 6074-6079.
35. Madsen, S.M., Arnau, J., Vrang, A., Givskov, M., and Israelsen, H. (1999) Molecular characterization of the pH-inducible and growth phase-dependent promoter P170 of Lactococcus lactis. Mol Microbiol 32: 75-87.
36. Maguin, E., Prevost, H., Ehrlich, S.D., and Gruss, A. (1996) Efficient insertional mutagenesis in Lactococci and other gram-positive bacteria. J Bacteriol 178: 931-935.
37. Mantsala, P., and Zalkin, H. (1992) Cloning and sequence of Bacillus subtilis pur A and guaA, involved in the conversion of IMP to AMP and GMP. J Bacteriol 174: 1883-1890.
38. Marquis, R.E., Bender, G.R., Murray, D.R., and Wong, A. (1987) Arginine deiminase system and bacterial adaptation to acid environments. Appl Environ Microbiol 53: 198-200.
39. Martinez-Costa, O.H., Fernandez-Moreno, M.A., and Malpartida, F. (1998) The reIA/spoT-homologous gene in Streptomyces coelicolor encodes both ribosome-dependent (p)ppGpp. Synthesizing and degrading activities. J Bacteriol 180: 4123-4132.
40. Mechold, U., and Malke, H. (1997) Characterization of the stringent and relaxed responses of Streptococcus equisimilis. J Bacteriol 179: 2658-2667.
41. Mechold, U., Steiner, K., Vettermann, S., and Malke, H. (1993) Genetic organization of the streptokinase region of the Streptococcus equisimilis H46A chromosome. Mol Gen Genet 241: 129-140.
42. Mechold, U., Cashel, M., Steiner, K., Gentry, D., and Malke, H. (1996) Functional analysis of a reIA/spoT gene homolog from Streptococcus equisimilis. J Bacteriol 178: 1401-1411.
43. Miller, J.H. (1972). Experiments in Molecular Microbiology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Mitani, T., Heinze, J.E., and Freese, E. (1977) Induction of sporulation in Bacillus subtilis by decoyinine or hadacidin. Biochem Biophys Res Commun 77: 1118-1125.
45. Munro, P.M., Flatau, G.N., Clement, R.L., and Gauthier, M.J. (1995) Influence of the RpoS (KatF) sigma factor on maintenance of viability and culturability of Escherichia coli and Salmonella typhimurium in seawater. Appl Environ Microbiol 61: 1853-1858.
46. Nannen, N.L., and Hutkins, R.W. (1991a) Intracellular pH effects in lactic acid bacteria. J Dairy Sci 74: 741-746.
47. Nannen, N.L., and Hutkins, R.W. (1991b) Proton-translocating adenosine triphosphate activity in lactic acid bacteria. J Dairy Sci 74: 747-751.
48. Nilsson, D., and Lauridsen, A.A. (1992) Isolation of purine auxotrophic mutants of Lactococcus lactis and characterization of the gene hpt encoding hypoxanthine guanine phosphoribosyltransferase. Mol Gen Genet 235: 359-364.
49. Nilsson, D., Lauridsen, A.A., Tomoyasu, T., and Ogura, T. (1994) A Lactococcus lactis gene encodes a membrane protein with putative ATPase activity that is homologous to the essential Escherichia coli ftsH gene product. Microbiology 140: 2601-2610.
50. Nyström, T. (1994) Role of guanosine tetraphosphate in gene expression and the survival of glucose or survival of glucose or seryl-tRNA starved cells of Escherichia coli K12. Mol Gen Genet 245: 355-362.
51. O'Sullivan, E., and Condon, S. (1997) Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis. Appl Environ Microbiol 63: 4210-42015.
52. Ostling, J., Flardh, K., and Kjelleberg, S. (1995) Isolation of a carbon starvation regulatory mutant in a marine Vibrio strain. J Bacteriol 177: 6978-6982.
53. Ostling, J., Holmquist, L., and Kjelleberg, S. (1996) Global analysis of the carbon starvation response of a marine Vibrio species with disruptions in genes homologous to reIA and spoT. J Bacteriol 178: 4901-4908.
54. Poolman, B., and Konings, W.N. (1988) Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J Bacteriol 170: 700-707.
55. Poolman, B., Driessen, A.J., and Konings, W.N. (1987a) Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol 169: 5597-5604.
56. Poolman, B., Driessen, A.J., and Konings, W.N. (1987b) Regulation of solute transport in streptococci by external and internal pH values. Microbiol Rev 51: 498-508.
57. Poolman, B., Hellingwerf, K.J., and Konings, W.N. (1987c) Regulation of the glutamate-glutamine transport system by intracellular pH in Streptococcus lactis. J Bacteriol 169: 2272-2276.
58. Poolman, B., Nijssen, R.M., and Konings, W.N. (1987d) Dependence of Streptococcus lactis phosphate transport on internal phosphate concentration and internal pH. J Bacteriol 169: 5373-5378.
59. Projan, S., Carlton, S., and Novick, R.P. (1983) Determination of plasmid copy number by fluorescence densitometry. Plasmid 9: 182-190.
60. Qi, Y., Kobayashi, Y., and Hulett, F.M. (1997) The psf operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the pho regulon. J Bacteriol 179: 2534-2539.
61. Rallu, F., Gruss, A., and Maguin, E. (1996) Lactococcus lactis and stress. Antonie Van Leeuwenhoek 70: 243-251.
62. Rowbury, R.J. (1993) Inducible enterobacterial responses to environmental pollution by sodium ions and alkalinisation. Sci Prog 77: 159-188.
63. Rowbury, R.J. (1997) Regulatory component, including integration host factor, CysB and H-NS, that influence pH responses in Escherichia coli. Lett Appl Microbiol 24: 319-328.
64. Rowbury, R.J., Goodson, M., and Wallace, A.D. (1992) The PhoE porin and transmission of the chemical stimulus for induction of acid resistance (acid habituation) in Escherichia coli. J Appl Bacteriol 72: 233-243.
65. Sambrook, J., Fritsch, E.F., and Maniatis, T.E. (1989) Molecular Cloning, a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
66. Sanders, J.W., Leenhouts, K., Burghoorn, J., Brands, J.R., Venema, G., and Kok, J. (1998) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol 27: 299-310.
67. Schreiber, G., Metzger, S., Aizenman, E., Roza, S., Cashel, M., and Glaser, G. (1991) Overexpression of the reIA gene in Escherichia coli. J Biol Chem 266: 3760-3767.
68. Slonczewski, J.L., and Foster, J.W. (1996) pH-regulated genes and survival at extreme pH. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press, pp. 1539-1549.
69. Spira, B., Silberstein, N., and Yagil, E. (1995) Guanosine 3′,5′-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J Bacteriol 177: 4053-4058.
70. Suzuki, T., Unemoto, T., and Kobayashi, H. (1988) Novel streptococcal mutants defective in the regulation of H+-ATPase biosynthesis and in FO complex. J Biol Chem 263: 11840-11843.
71. Svitil, A.L., Cashel, M., and Zyskind, J.W. (1993) Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. J Biol Chem 268: 2307-2311.
72. Takemaru, K., Mizuno, M., and Kobayashi, Y. (1996) A Bacillus subtilis gene cluster similar to the Escherichia coli phosphate-specific transport (pst) operon: evidence for a tandemly arranged pstB gene. Microbiology 142: 2017-2020.
73. Terzaghy, B.E., and Sandine, W.E. (1975) Improved medium for lactic Streptococci. Curr Microbiol 7: 245-250.
74. Van Hoy, B.E., and Hoch, J.A. (1990) Characterization of the spolVB and recN loci of Bacillus subtilis. J Bacteriol 172: 1306-1311.
75. Walker, G.C. (1996) The SOS response. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press, pp. 1400-1416.
76. Wanner, B.L. (1996) Phosphorus assimilation and control of the phosphate transport. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press, pp. 1357-1381.
77. Wehmeier, L., Schafer, A., Burkovski, A., Kramer, R., Mechold, U., Malke, H., et al. (1998) The role of the Corynebacterium glutamicum rel gene in (p)ppGpp metabolism. Microbiology 144: 1853-1862.
78. Wendrich, T.M., and Marahiel, M.A. (1997) Cloning and characterization of a reIA/spoT homologue from Bacillus subtilis. Mol Microbiol 26: 65-79.
79. Yamashita, Y., Takehara, T., and Kuramitsu, H.K. (1993) Molecular characterization of a Streptococcus mutants mutant altered in environmental stress responses. J Bacteriol 175: 6220-6228.
80. Yokota, A., Amachi, S., Ishii, S., and Tomita, F. (1995) Acid sensitivity of a mutant of Lactococcus lactis subsp. lactis C2 with reduced membrane-bound ATPase activity. Biosci Biotechnol Biochem 59: 2004-2007.
81. Zalkin, H. (1993) De novo purine nucleotide synthesis. In Bacillus subtilis and Other Gram-positive Bacteria. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 335-341.
82. Zalkin, H., and Nygaard, P. (1996) Biosynthesis of purines nucleotides. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press, pp. 561-579.