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PMID: 12966143 Published · ppublish English Journal Article Review

Surviving the acid test: responses of gram-positive bacteria to low pH.

Microbiology and molecular biology reviews : MMBR ·Vol. 67 ·No. 3 ·2003-09-00 ·Pages 429-53, table of contents

Cotter PD, Hill C

Abstract

Gram-positive bacteria possess a myriad of acid resistance systems that can help them to overcome the challenge posed by different acidic environments. In this review the most common mechanisms are described: i.e., the use of proton pumps, the protection or repair of macromolecules, cell membrane changes, production of alkali, induction of pathways by transcriptional regulators, alteration of metabolism, and the role of cell density and cell signaling. We also discuss the responses of Listeria monocytogenes, Rhodococcus, Mycobacterium, Clostridium perfringens, Staphylococcus aureus, Bacillus cereus, oral streptococci, and lactic acid bacteria to acidic environments and outline ways in which this knowledge has been or may be used to either aid or prevent bacterial survival in low-pH environments.

MeSH Terms
Bacillus cereus/growth & development,physiology Clostridium perfringens/growth & development,physiology Food Microbiology Gram-Positive Bacteria/growth & development,physiology Hydrogen-Ion Concentration Lactobacillus/growth & development,physiology Listeria monocytogenes/growth & development,physiology Mycobacterium/growth & development,physiology Proton Pumps/metabolism Rhodococcus equi/growth & development,physiology Staphylococcus aureus/growth & development,physiology
Chemicals
Proton Pumps
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cotter Paul D
Department of Microbiology and National Food Biotechnology Centre, University College Cork, Cork, Ireland.
Hill Colin
References (243)
243 references, click to expand
  1. The citrate transport system of Lactococcus lactis subsp. lactis biovar diacetylactis is induced by acid stress.
    Appl Environ Microbiol. 1998 Mar;64(3):850-7 PMID: 9501425
  2. Defects in D-alanyl-lipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity.
    J Bacteriol. 2000 Nov;182(21):6055-65 PMID: 11029425
  3. Characterization of a mutant of Lactococcus lactis with reduced membrane-bound ATPase activity under acidic conditions.
    Biosci Biotechnol Biochem. 1998 Aug;62(8):1574-80 PMID: 9757564
  4. Quantitative assessment of urea, glucose and ammonia changes in human dental plaque and saliva following rinsing with urea and glucose.
    Arch Oral Biol. 1983;28(10):923-9 PMID: 6580848
  5. Energy coupling to potassium transport in Streptococcus faecalis. Interplay of ATP and the protonmotive force.
    J Biol Chem. 1980 Jan 25;255(2):433-40 PMID: 6766127
  6. Transcriptional regulation of the Streptococcus salivarius 57.I urease operon.
    J Bacteriol. 1998 Nov;180(21):5769-75 PMID: 9791132
  7. Molecular characterization of a STreptococcus mutans mutant altered in environmental stress responses.
    J Bacteriol. 1993 Oct;175(19):6220-8 PMID: 8407794
  8. Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans.
    J Bacteriol. 2001 Oct;183(20):6074-84 PMID: 11567008
  9. Lactococcus lactis contains only one glutamate decarboxylase gene.
    Microbiology. 1999 Jun;145 ( Pt 6):1375-80 PMID: 10411264
  10. Plaque sampling and telemetry for monitoring acid production on human buccal tooth surfaces.
    Arch Oral Biol. 1982;27(1):21-31 PMID: 6951525
  11. Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria.
    Int J Med Microbiol. 2001 May;291(2):97-106 PMID: 11437344
  12. A glutamate-dependent acid resistance gene in Escherichia coli.
    J Bacteriol. 1996 Jul;178(13):3978-81 PMID: 8682809
  13. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS).
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11554-9 PMID: 10500215
  14. Stress responses in lactic acid bacteria.
    Antonie Van Leeuwenhoek. 2002 Aug;82(1-4):187-216 PMID: 12369188
  15. Crohn's disease and the mycobacterioses: a review and comparison of two disease entities.
    Clin Microbiol Rev. 1989 Jan;2(1):90-117 PMID: 2644025
  16. Rapid procedure for acid adaptation of oral lactic-acid bacteria and further characterization of the response.
    Can J Microbiol. 1997 Feb;43(2):143-8 PMID: 9090104
  17. Acid survival of Helicobacter pylori: how does urease activity trigger cytoplasmic pH homeostasis?
    Trends Microbiol. 2002 Feb;10(2):70-4 PMID: 11827807
  18. Survival of Mycobacterium avium and Mycobacterium tuberculosis in acidified vacuoles of murine macrophages.
    Infect Immun. 1999 Jul;67(7):3199-206 PMID: 10377091
  19. Multiple sigma factor genes in Brevibacterium lactofermentum: characterization of sigA and sigB.
    J Bacteriol. 1996 Jan;178(2):550-3 PMID: 8550480
  20. Structural and functional analysis of the gene cluster encoding the enzymes of the arginine deiminase pathway of Lactobacillus sake.
    J Bacteriol. 1998 Aug;180(16):4154-9 PMID: 9696763
  21. Effect of carbon starvation and proteolytic activity on stationary-phase acid tolerance of Streptococcus mutans.
    Microbiology. 2001 Nov;147(Pt 11):2971-9 PMID: 11700348
  22. Proton ATPases in bacteria: comparison to Escherichia coli F1F0 as the prototype.
    Novartis Found Symp. 1999;221:218-29; discussion 229-34 PMID: 10207922
  23. cis-Acting elements that regulate the low-pH-inducible urease operon of Streptococcus salivarius.
    Microbiology. 2002 Nov;148(Pt 11):3599-608 PMID: 12427950
  24. uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans.
    J Bacteriol. 2001 Oct;183(20):5964-73 PMID: 11566996
  25. The importance of repairing stalled replication forks.
    Nature. 2000 Mar 2;404(6773):37-41 PMID: 10716434
  26. Acid stress in the food pathogen Bacillus cereus.
    J Appl Microbiol. 2002;92(3):404-14 PMID: 11872115
  27. A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the sigmaB transcription factor of Bacillus subtilis.
    Mol Microbiol. 2000 Jan;35(1):180-8 PMID: 10632888
  28. Influence of the natural microbial flora on the acid tolerance response of Listeria monocytogenes in a model system of fresh meat decontamination fluids.
    Appl Environ Microbiol. 2001 Jun;67(6):2410-20 PMID: 11375145
  29. Mechanism of citrate metabolism in Lactococcus lactis: resistance against lactate toxicity at low pH.
    J Bacteriol. 1999 Mar;181(5):1451-7 PMID: 10049375
  30. Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans.
    J Bacteriol. 2002 Nov;184(22):6333-42 PMID: 12399503
  31. Cloning and nucleotide sequence analysis of the Streptococcus mutans membrane-bound, proton-translocating ATPase operon.
    Gene. 1996 Dec 12;183(1-2):87-96 PMID: 8996091
  32. Immunology of tuberculosis.
    Annu Rev Immunol. 2001;19:93-129 PMID: 11244032
  33. Acid sensitivity of neomycin-resistant mutants of Oenococcus oeni: a relationship between reduction of ATPase activity and lack of malolactic activity.
    FEMS Microbiol Lett. 1999 Sep 15;178(2):319-26 PMID: 10499282
  34. Arginine deiminase system and bacterial adaptation to acid environments.
    Appl Environ Microbiol. 1987 Jan;53(1):198-200 PMID: 3103530
  35. Stress-induced membrane association of the Streptococcus mutans GTP-binding protein, an essential G protein, and investigation of its physiological role by utilizing an antisense RNA strategy.
    Infect Immun. 1999 Sep;67(9):4510-6 PMID: 10456893
  36. Glutamic acid decarboxylase in Mycobacterium leprae.
    Arch Microbiol. 1983 Jul;134(4):320-3 PMID: 6137201
  37. Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes.
    Infect Immun. 2002 Jul;70(7):3948-52 PMID: 12065541
  38. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci.
    J Bacteriol. 1992 Sep;174(18):5820-6 PMID: 1522060
  39. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence.
    Nature. 1998 Jun 11;393(6685):537-44 PMID: 9634230
  40. Dependence of Streptococcus lactis phosphate transport on internal phosphate concentration and internal pH.
    J Bacteriol. 1987 Dec;169(12):5373-8 PMID: 3119562
  41. Strain-related acid production by oral streptococci.
    Caries Res. 2000 Nov-Dec;34(6):486-90 PMID: 11093023
  42. Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic.
    Infect Immun. 1991 May;59(5):1823-31 PMID: 1902198
  43. Novel RNA polymerase sigma factor from Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7000-4 PMID: 6784117
  44. Identification of 15- to 17-kilodalton antigens associated with virulent Rhodococcus equi.
    J Clin Microbiol. 1991 Mar;29(3):439-43 PMID: 2037660
  45. Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions.
    Appl Environ Microbiol. 2002 May;68(5):2382-90 PMID: 11976112
  46. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase.
    Science. 1994 Feb 4;263(5147):678-81 PMID: 8303277
  47. Regulation of breakdown and synthesis of L-glutamate decarboxylase in Clostridium perfringens.
    J Bacteriol. 1975 Sep;123(3):1115-23 PMID: 239920
  48. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase.
    Nature. 2000 Aug 17;406(6797):735-8 PMID: 10963599
  49. pH regulation of urease levels in Streptococcus salivarius.
    J Dent Res. 1990 May;69(5):1131-7 PMID: 2110582
  50. Expression of virulence-associated antigens of Rhodococcus equi is regulated by temperature and pH.
    Microbiol Immunol. 1996;40(8):591-4 PMID: 8887354
  51. Identification of stress-responsive genes in Streptococcus mutans by differential display reverse transcription-PCR.
    Infect Immun. 2001 Apr;69(4):2493-501 PMID: 11254612
  52. Effect of acid-adaptation on Listeria monocytogenes survival and translocation in a murine intragastric infection model.
    FEMS Microbiol Lett. 2000 Dec 1;193(1):155-9 PMID: 11094295
  53. Association of free arginine and lysine concentrations in human parotid saliva with caries experience.
    J Dent Res. 1995 Feb;74(2):686-90 PMID: 7722066
  54. A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase.
    Lett Appl Microbiol. 1997 May;24(5):393-6 PMID: 9172446
  55. Inhibition of human peripheral blood mononuclear cell proliferation by Streptococcus pyogenes cell extract is associated with arginine deiminase activity.
    Infect Immun. 1998 Jul;66(7):3050-8 PMID: 9632565
  56. Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria.
    Cell Microbiol. 2001 Aug;3(8):551-66 PMID: 11488816
  57. Acid tolerance in Listeria monocytogenes influences invasiveness of enterocyte-like cells and macrophage-like cells.
    Microb Pathog. 2000 Sep;29(3):137-44 PMID: 10968945
  58. Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract.
    J Appl Microbiol. 1998 May;84(5):759-68 PMID: 9674129
  59. Effect of acid adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon.
    Infect Immun. 2002 Aug;70(8):4369-78 PMID: 12117947
  60. Complementation of an Enterococcus hirae (Streptococcus faecalis) mutant in the alpha subunit of the H(+)-ATPase by cloned genes from the same and different species.
    Mol Microbiol. 1993 Jul;9(1):111-8 PMID: 8412656
  61. A parallel intraphagosomal survival strategy shared by mycobacterium tuberculosis and Salmonella enterica.
    Mol Microbiol. 2000 Mar;35(6):1375-82 PMID: 10760138
  62. Characterization of anaerobic bacteria by using a commercially available rapid tube test for glutamic acid decarboxylase.
    J Clin Microbiol. 1989 Feb;27(2):361-3 PMID: 2644301
  63. Production of gamma-aminobutyric acid by cheese starters during cheese ripening.
    J Dairy Sci. 1998 Jun;81(6):1486-91 PMID: 9684157
  64. Factors controlling acid tolerance of Listeria monocytogenes: effects of nisin and other ionophores.
    Appl Environ Microbiol. 1997 Oct;63(10):4123-6 PMID: 9327581
  65. Identification of the pH-inducible, proton-translocating F1F0-ATPase (atpBEFHAGDC) operon of Lactobacillus acidophilus by differential display: gene structure, cloning and characterization.
    Mol Microbiol. 1999 Sep;33(6):1152-61 PMID: 10510230
  66. Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation.
    J Bacteriol. 1991 Oct;173(19):6199-206 PMID: 1917854
  67. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells.
    J Cell Biol. 2002 Mar 18;156(6):1029-38 PMID: 11901168
  68. The subtilisin E gene of Bacillus subtilis is transcribed from a sigma 37 promoter in vivo.
    Proc Natl Acad Sci U S A. 1984 Feb;81(4):1184-8 PMID: 6322190
  69. Purification and general properties of glutamate decarboxylase from Clostridium perfringens.
    Biochem J. 1970 Jun;118(1):135-41 PMID: 4319539
  70. The relationship between acid stress responses and virulence in Salmonella typhimurium and Listeria monocytogenes.
    Int J Food Microbiol. 1999 Sep 15;50(1-2):93-100 PMID: 10488846
  71. A transmembrane pH gradient in Streptococcus faecalis: origin, and dissipation by proton conductors and N,N'-dicyclohexylcarbodimide.
    Biochim Biophys Acta. 1970;196(2):235-44 PMID: 4244306
  72. Characterization of the sat operon in Streptococcus mutans: evidence for a role of Ffh in acid tolerance.
    J Bacteriol. 2001 Apr;183(8):2543-52 PMID: 11274114
  73. HtrA protease and processing of extracellular proteins of Streptococcus mutans.
    FEMS Microbiol Lett. 2001 Oct 16;204(1):23-8 PMID: 11682172
  74. The anaerobic pathogen Clostridium perfringens can escape the phagosome of macrophages under aerobic conditions.
    Cell Microbiol. 2000 Dec;2(6):505-19 PMID: 11207604
  75. Interactions between a Bacillus subtilis anti-sigma factor (RsbW) and its antagonist (RsbV).
    J Bacteriol. 1994 Apr;176(7):1813-20 PMID: 8144446
  76. The tolerances of unclassified mycobacteria. I. Limits of pH tolerance.
    Am Rev Respir Dis. 1962 Oct;86:582-3 PMID: 14020151
  77. Purification and characterization of Listeria monocytogenes phosphatidylinositol-specific phospholipase C.
    Infect Immun. 1992 Oct;60(10):4059-67 PMID: 1398918
  78. Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans.
    FEMS Microbiol Lett. 2000 Aug 1;189(1):89-92 PMID: 10913871
  79. Expression of the sigmaB-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis.
    J Bacteriol. 1999 Jul;181(13):3942-8 PMID: 10383961
  80. Cloning and transcriptional characterization of two sigma factor genes, sigA and sigB, from Brevibacterium flavum.
    Curr Microbiol. 2001 Oct;43(4):249-54 PMID: 11683358
  81. Identification and characterization of two temperature-induced surface-associated proteins of Streptococcus suis with high homologies to members of the Arginine Deiminase system of Streptococcus pyogenes.
    J Bacteriol. 2002 Dec;184(24):6768-76 PMID: 12446626
  82. Mycobacterium avium-Mycobacterium intracellulare from the intestinal tracts of patients with the acquired immunodeficiency syndrome: concepts regarding acquisition and pathogenesis.
    J Infect Dis. 1985 Jan;151(1):179-81 PMID: 3965590
  83. A mutant of Listeria monocytogenes LO28 unable to induce an acid tolerance response displays diminished virulence in a murine model.
    Appl Environ Microbiol. 1997 Dec;63(12):4945-7 PMID: 9406415
  84. The final pH of bacteria comprising the predominant flora on sound and carious human root and enamel surfaces.
    J Dent Res. 1996 Apr;75(4):1008-14 PMID: 8708129
  85. Acidogenicity and acidurance of fluoride-resistant Streptococcus sobrinus in vitro.
    Chin J Dent Res. 2000 Aug;3(2):7-14 PMID: 11314523
  86. sigma(B) activity in Staphylococcus aureus is controlled by RsbU and an additional factor(s) during bacterial growth.
    Infect Immun. 2001 Dec;69(12):7858-65 PMID: 11705968
  87. Microbial interference and colonization of the murine gastrointestinal tract by Listeria monocytogenes.
    Infect Immun. 1979 Jan;23(1):168-74 PMID: 106003
  88. Purification and characterization of glutamate decarboxylase from Lactobacillus brevis IFO 12005.
    Biosci Biotechnol Biochem. 1997 Jul;61(7):1168-71 PMID: 9255981
  89. Extracellular sensing components and extracellular induction component alarmones give early warning against stress in Escherichia coli.
    Adv Microb Physiol. 2001;44:215-57 PMID: 11407114
  90. The sgp gene modulates stress responses of Streptococcus mutans: utilization of an antisense RNA strategy to investigate essential gene functions.
    FEMS Microbiol Lett. 1998 Feb 15;159(2):241-5 PMID: 9503617
  91. Responses of Listeria monocytogenes to acid stress and glucose availability revealed by a novel combination of fluorescence microscopy and microelectrode ion-selective techniques.
    Appl Environ Microbiol. 2002 Apr;68(4):1794-802 PMID: 11916698
  92. Six putative two-component regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363.
    Microbiology. 2000 Apr;146 ( Pt 4):935-47 PMID: 10784052
  93. Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms.
    J Bacteriol. 2001 Dec;183(23):6875-84 PMID: 11698377
  94. Barotolerant variant of Streptococcus faecalis with reduced sensitivity to glucose catabolite repression.
    Can J Microbiol. 1985 Jul;31(7):644-50 PMID: 3928124
  95. Analysis of Streptococcus salivarius urease expression using continuous chemostat culture.
    FEMS Microbiol Lett. 1996 Jan 15;135(2-3):223-9 PMID: 8595861
  96. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes.
    Infect Immun. 1987 Jul;55(7):1641-6 PMID: 3110067
  97. Catalytic mechanism of F1-ATPase.
    Biochim Biophys Acta. 1997 Mar 28;1319(1):19-58 PMID: 9107315
  98. Oral streptococci... products of their environment.
    J Dent Res. 1998 Mar;77(3):445-52 PMID: 9496917
  99. Control of enzyme synthesis in the arginine deiminase pathway of Streptococcus faecalis.
    J Bacteriol. 1982 Jun;150(3):1085-90 PMID: 6281235
  100. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation.
    Appl Environ Microbiol. 1996 Sep;62(9):3128-32 PMID: 8795199
  101. Turning on and turning off the arginine deiminase system in oral streptococci.
    Can J Microbiol. 1998 Nov;44(11):1078-85 PMID: 10030002
  102. Acid stress responses in enterobacteria.
    FEMS Microbiol Lett. 1997 Feb 15;147(2):173-80 PMID: 9119190
  103. Caries resistance in children with chronic renal failure: plaque pH, salivary pH, and salivary composition.
    Pediatr Res. 1985 Aug;19(8):796-9 PMID: 3898000
  104. Novel streptococcal mutants defective in the regulation of H+-ATPase biosynthesis and in F0 complex.
    J Biol Chem. 1988 Aug 25;263(24):11840-3 PMID: 2900247
  105. Second system for potassium transport in Streptococcus faecalis.
    J Bacteriol. 1982 May;150(2):506-11 PMID: 6279560
  106. Sodium bicarbonate enhances the severity of infection in neutropenic mice orally inoculated with Listeria monocytogenes EGD.
    Clin Diagn Lab Immunol. 2002 Mar;9(2):477-81 PMID: 11874896
  107. Isolation and molecular analysis of the gene cluster for the arginine deiminase system from Streptococcus gordonii DL1.
    Appl Environ Microbiol. 2002 Nov;68(11):5549-53 PMID: 12406748
  108. Characterization of recombinant, ureolytic Streptococcus mutans demonstrates an inverse relationship between dental plaque ureolytic capacity and cariogenicity.
    Infect Immun. 2000 May;68(5):2621-9 PMID: 10768953
  109. Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH.
    Mol Microbiol. 1999 Mar;31(5):1489-98 PMID: 10200967
  110. Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus.
    Electrophoresis. 2000 Jul;21(12):2557-61 PMID: 10939472
  111. The promoter of the operon encoding the F0F1 ATPase of Streptococcus pneumoniae is inducible by pH.
    Mol Microbiol. 2001 Sep;41(6):1327-38 PMID: 11580837
  112. Rhodococcus equi infection in HIV-infected patients.
    AIDS. 1996 Apr;10(4):359-62 PMID: 8728038
  113. A model of food-borne Listeria monocytogenes infection in the Sprague-Dawley rat using gastric inoculation: development and effect of gastric acidity on infective dose.
    Int J Food Microbiol. 1993 Mar;18(1):15-24 PMID: 8466809
  114. Killing of Listeria monocytogens by conventional and germfree rat sera.
    Infect Immun. 1981 Aug;33(2):348-54 PMID: 6792076
  115. Isolation and characterization of Staphylococcus aureus starvation-induced, stationary-phase mutants defective in survival or recovery.
    Microbiology. 1998 Nov;144 ( Pt 11):3159-69 PMID: 9846752
  116. Mycobacterium tuberculosis: here today, and here tomorrow.
    Nat Rev Mol Cell Biol. 2001 Aug;2(8):569-77 PMID: 11483990
  117. Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147.
    J Food Prot. 1999 May;62(5):536-9 PMID: 10340677
  118. Rhodococcus equi: an animal and human pathogen.
    Clin Microbiol Rev. 1991 Jan;4(1):20-34 PMID: 2004346
  119. Listeria monocytogenes response regulators important for stress tolerance and pathogenesis.
    FEMS Microbiol Lett. 2001 Oct 16;204(1):111-5 PMID: 11682188
  120. Survival of osmotic and acid stress by Listeria monocytogenes strains of clinical or meat origin.
    Int J Food Microbiol. 2000 Jun 1;56(2-3):161-6 PMID: 10857542
  121. Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis.
    Appl Environ Microbiol. 1997 Nov;63(11):4210-5 PMID: 9361406
  122. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid.
    Mol Microbiol. 2001 Apr;40(2):465-75 PMID: 11309128
  123. Streptococcal cytoplasmic pH is regulated by changes in amount and activity of a proton-translocating ATPase.
    J Biol Chem. 1986 Jan 15;261(2):627-30 PMID: 2416756
  124. Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence.
    Infect Immun. 2002 Apr;70(4):1991-6 PMID: 11895963
  125. Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification.
    Mol Microbiol. 1997 Jul;25(2):329-41 PMID: 9282745
  126. Stress resistance in Staphylococcus aureus.
    Trends Microbiol. 1999 Nov;7(11):458-62 PMID: 10542426
  127. Changes in protein synthesis and acid tolerance in Clostridium perfringens type A in response to acid shock.
    Int Microbiol. 2000 Jun;3(2):113-6 PMID: 11001541
  128. Bacillus subtilis sigma B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2330-4 PMID: 8460143
  129. Intestinal infection with Mycobacterium avium in acquired immune deficiency syndrome (AIDS). Histological and clinical comparison with Whipple's disease.
    Dig Dis Sci. 1985 May;30(5):497-504 PMID: 2580679
  130. Mammalian and Escherichia coli signal recognition particles.
    Mol Microbiol. 1994 Jan;11(1):9-13 PMID: 8145649
  131. Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria.
    Infect Immun. 1994 Feb;62(2):543-53 PMID: 8300212
  132. Arginine deiminase system and acid adaptation of oral streptococci.
    Appl Environ Microbiol. 1995 Dec;61(12):4494-6 PMID: 8534118
  133. New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigma(B) of Bacillus subtilis.
    J Bacteriol. 2001 Feb;183(4):1329-38 PMID: 11157946
  134. Response of Mycobacterium smegmatis to acid stress.
    FEMS Microbiol Lett. 1996 May 15;139(1):11-7 PMID: 8647369
  135. Role of the glutamate decarboxylase acid resistance system in the survival of Listeria monocytogenes LO28 in low pH foods.
    J Food Prot. 2001 Sep;64(9):1362-8 PMID: 11563513
  136. The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins.
    Antimicrob Agents Chemother. 2002 Sep;46(9):2784-90 PMID: 12183229
  137. Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes.
    J Bacteriol. 1999 Nov;181(21):6840-3 PMID: 10542190
  138. Resistance of Rhodococcus equi to acid pH.
    Int J Food Microbiol. 2000 Apr 10;55(1-3):295-8 PMID: 10791761
  139. Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance.
    Appl Environ Microbiol. 1988 Jun;54(6):1318-24 PMID: 2843090
  140. Identification of the gene encoding the alternative sigma factor sigmaB from Listeria monocytogenes and its role in osmotolerance.
    J Bacteriol. 1998 Sep;180(17):4547-54 PMID: 9721294
  141. Deletion of the alternative sigma factor sigmaB in Staphylococcus aureus reveals its function as a global regulator of virulence genes.
    J Bacteriol. 1998 Sep;180(18):4814-20 PMID: 9733682
  142. Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy.
    J Bacteriol. 1991 Oct;173(19):6030-7 PMID: 1917837
  143. Involvement of molecular chaperonins in nucleotide excision repair. Dnak leads to increased thermal stability of UvrA, catalytic UvrB loading, enhanced repair, and increased UV resistance.
    J Biol Chem. 1998 May 22;273(21):12887-92 PMID: 9582319
  144. The Garrod Lecture. Understanding the chemotherapy of tuberculosis--current problems.
    J Antimicrob Chemother. 1992 May;29(5):477-93 PMID: 1624388
  145. Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein.
    Infect Immun. 2000 May;68(5):2441-8 PMID: 10768929
  146. The arcABC gene cluster encoding the arginine deiminase pathway of Oenococcus oeni, and arginine induction of a CRP-like gene.
    Res Microbiol. 2001 Sep;152(7):653-61 PMID: 11605985
  147. Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses.
    J Bacteriol. 1995 Jul;177(13):3771-80 PMID: 7601843
  148. Lactococcus lactis and stress.
    Antonie Van Leeuwenhoek. 1996 Oct;70(2-4):243-51 PMID: 8879409
  149. Catalytic function of an alpha/beta hydrolase is required for energy stress activation of the sigma(B) transcription factor in Bacillus subtilis.
    J Bacteriol. 2001 Nov;183(21):6422-8 PMID: 11591687
  150. L-Glutamate decarboxylase from bacteria.
    Methods Enzymol. 1985;113:11-6 PMID: 3910996
  151. The proton motive force generated in Leuconostoc oenos by L-malate fermentation.
    J Bacteriol. 1996 Jun;178(11):3127-32 PMID: 8655490
  152. A mycobacterial extracytoplasmic function sigma factor involved in survival following stress.
    J Bacteriol. 1997 May;179(9):2922-9 PMID: 9139909
  153. Mycobacterium avium resists exposure to the acidic conditions of the stomach.
    FEMS Microbiol Lett. 2000 Jan 1;182(1):45-9 PMID: 10612729
  154. Mutans streptococci and non-mutans streptococci acidogenic at low pH, and in vitro acidogenic potential of dental plaque in two different areas of the human dentition.
    J Dent Res. 1991 Dec;70(12):1503-7 PMID: 1774381
  155. Electron microscopic investigation of intracellular events after ingestion of Rhodococcus equi by foal alveolar macrophages.
    Vet Microbiol. 1987 Aug;14(3):295-305 PMID: 3672872
  156. Streptococcus salivarius urease: genetic and biochemical characterization and expression in a dental plaque streptococcus.
    Infect Immun. 1996 Feb;64(2):585-92 PMID: 8550211
  157. Comparative genomics of Listeria species.
    Science. 2001 Oct 26;294(5543):849-52 PMID: 11679669
  158. Inactivation of the glutamate decarboxylase gene in Lactococcus lactis subsp. cremoris.
    Appl Environ Microbiol. 2000 May;66(5):2235-7 PMID: 10788408
  159. Response of a Streptococcus sanguis strain to arginine-containing peptides.
    Infect Immun. 1988 Mar;56(3):687-92 PMID: 3343053
  160. Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency.
    FEMS Microbiol Lett. 1995 Mar 1;126(3):257-61 PMID: 7729669
  161. Dynamic response of catabolic pathways to autoacidification in Lactococcus lactis: transcript profiling and stability in relation to metabolic and energetic constraints.
    Mol Microbiol. 2002 Aug;45(4):1143-52 PMID: 12180931
  162. Inorganic cation transport and energy transduction in Enterococcus hirae and other streptococci.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1021-45 PMID: 9841664
  163. Streptococcus salivarius urease expression: involvement of the phosphoenolpyruvate:sugar phosphotransferase system.
    FEMS Microbiol Lett. 1998 Aug 1;165(1):117-22 PMID: 9711847
  164. Two-Dimensional Polyacrylamide Gel Electrophoresis Analysis of the Acid Tolerance Response in Listeria monocytogenes LO28.
    Appl Environ Microbiol. 1997 Jul;63(7):2679-85 PMID: 16535645
  165. Stress activation of Bacillus subtilis sigma B can occur in the absence of the sigma B negative regulator RsbX.
    J Bacteriol. 1997 Mar;179(6):1980-4 PMID: 9068644
  166. Acid-induced acid tolerance and acidogenicity of non-mutans streptococci.
    Oral Microbiol Immunol. 1999 Feb;14(1):43-8 PMID: 10204479
  167. Analysis of the role of the Listeria monocytogenes F0F1 -AtPase operon in the acid tolerance response.
    Int J Food Microbiol. 2000 Sep 25;60(2-3):137-46 PMID: 11016603
  168. Activity of H(+)-ATPase in ruminal bacteria with special reference to acid tolerance.
    Appl Environ Microbiol. 1997 Jun;63(6):2155-8 PMID: 9172333
  169. The effects of inhibitors of vacuolar acidification on the release of Listeria monocytogenes from phagosomes of Caco-2 cells.
    J Med Microbiol. 1996 Jun;44(6):418-24 PMID: 8636958
  170. Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses.
    FEMS Microbiol Lett. 1999 Feb 1;171(1):57-65 PMID: 9987842
  171. Acid- and multistress-resistant mutants of Lactococcus lactis : identification of intracellular stress signals.
    Mol Microbiol. 2000 Feb;35(3):517-28 PMID: 10672175
  172. Intracellular pH regulation by Mycobacterium smegmatis and Mycobacterium bovis BCG.
    Microbiology. 2001 Apr;147(Pt 4):1017-24 PMID: 11283297
  173. Urea content of gingival crevicular fluid and its relation to periodontal diseases in humans.
    J Periodontal Res. 1971;6(4):243-51 PMID: 4272018
  174. Changes in acid tolerance of Lactococcus lactis during growth at constant pH.
    Int J Food Microbiol. 2000 Apr 10;55(1-3):215-21 PMID: 10791746
  175. Virulence-associated 15- to 17-kilodalton antigens in Rhodococcus equi: temperature-dependent expression and location of the antigens.
    Infect Immun. 1992 Jul;60(7):2995-7 PMID: 1612765
  176. Molecular characterization of a lipid-modified virulence-associated protein of Rhodococcus equi and its potential in protective immunity.
    Can J Vet Res. 1995 Jan;59(1):51-9 PMID: 7704843
  177. Physiologic homeostasis and stress responses in oral biofilms.
    Methods Enzymol. 1999;310:441-60 PMID: 10547811
  178. Effects of potassium ions on the electrical and pH gradients across the membrane of Streptococcus lactis cells.
    J Bacteriol. 1977 Jun;130(3):1017-23 PMID: 16864
  179. Ribosomes as sensors of heat and cold shock in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5589-93 PMID: 2198567
  180. Homologous pairs of regulatory proteins control activity of Bacillus subtilis transcription factor sigma(b) in response to environmental stress.
    J Bacteriol. 1996 Jul;178(13):3846-53 PMID: 8682789
  181. Mycobacterium avium infection and AIDS: a therapeutic dilemma in rapid evolution.
    J Infect Dis. 1991 Jun;163(6):1326-35 PMID: 2037799
  182. Molecular biology of microbial ureases.
    Microbiol Rev. 1995 Sep;59(3):451-80 PMID: 7565414
  183. Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance.
    Microbiology. 1996 Oct;142 ( Pt 10):2975-82 PMID: 8885415
  184. Acid responses of Listeria monocytogenes.
    Int J Food Microbiol. 2000 Apr 10;55(1-3):121-6 PMID: 10791729
  185. DNA excision repair.
    Annu Rev Biochem. 1996;65:43-81 PMID: 8811174
  186. The association of mutans streptococci and non-mutans streptococci capable of acidogenesis at a low pH with dental caries on enamel and root surfaces.
    J Dent Res. 1993 Feb;72(2):508-16 PMID: 8423248
  187. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes.
    J Bacteriol. 2002 Jul;184(14):4025-32 PMID: 12081975
  188. Monolaurin and acetic acid inactivation of Listeria monocytogenes attached to stainless steel.
    J Food Prot. 1996 Mar;59(3):249-52 PMID: 10463441
  189. The widely conserved Era G-protein contains an RNA-binding domain required for Era function in vivo.
    Mol Microbiol. 1999 Sep;33(6):1118-31 PMID: 10510227
  190. General stress transcription factor sigmaB and its role in acid tolerance and virulence of Listeria monocytogenes.
    J Bacteriol. 1998 Jul;180(14):3650-6 PMID: 9658010
  191. A proteomic approach to study the acid response in Listeria monocytogenes.
    Electrophoresis. 1999 Aug;20(11):2214-24 PMID: 10493126
  192. Improved acid tolerance of a recombinant strain of Escherichia coli expressing genes from the acidophilic bacterium Oenococcus oeni.
    Lett Appl Microbiol. 2001 Aug;33(2):126-30 PMID: 11472520
  193. The Lactic Acid Stress Response of Lactococcus lactis subsp. lactis
    Curr Microbiol. 1996 Sep;33(3):194-9 PMID: 8672097
  194. Amplification of the Streptococcus faecalis proton-translocating ATPase by a decrease in cytoplasmic pH.
    J Bacteriol. 1984 Jun;158(3):1157-60 PMID: 6202676
  195. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions.
    DNA Res. 1996 Jun 30;3(3):109-36 PMID: 8905231
  196. Role of malolactic fermentation in lactic acid bacteria.
    Biochimie. 1988 Mar;70(3):375-9 PMID: 3139055
  197. Rate of depurination of native deoxyribonucleic acid.
    Biochemistry. 1972 Sep 12;11(19):3610-8 PMID: 4626532
  198. Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci.
    Infect Immun. 1986 Aug;53(2):331-8 PMID: 3015800
  199. Hijacking the host: survival of pathogenic mycobacteria inside macrophages.
    Trends Microbiol. 2002 Mar;10(3):142-6 PMID: 11864824
  200. Arginine catabolism by sourdough lactic acid bacteria: purification and characterization of the arginine deiminase pathway enzymes from Lactobacillus sanfranciscensis CB1.
    Appl Environ Microbiol. 2002 Dec;68(12):6193-201 PMID: 12450844
  201. Role of sigma(B) in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes.
    Appl Environ Microbiol. 2001 Oct;67(10):4454-7 PMID: 11571142
  202. The Staphylococcus aureus alternative sigma factor sigmaB controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model.
    J Bacteriol. 1998 Dec;180(23):6082-9 PMID: 9829915
  203. The Product of arcR, the sixth gene of the arc operon of Lactobacillus sakei, is essential for expression of the arginine deiminase pathway.
    Appl Environ Microbiol. 2002 Dec;68(12):6051-8 PMID: 12450828
  204. Increased prevalence of Listeria monocytogenes in the faeces of patients receiving long-term H2-antagonists.
    Eur J Gastroenterol Hepatol. 1996 Nov;8(11):1071-4 PMID: 8944368
  205. Growth of Mycobacterium tuberculosis in a defined medium is very restricted by acid pH and Mg(2+) levels.
    Infect Immun. 2000 Aug;68(8):4518-22 PMID: 10899850
  206. Comparative acid tolerances and inhibitor sensitivities of isolated F-ATPases of oral lactic acid bacteria.
    Appl Environ Microbiol. 1992 Jul;58(7):2287-91 PMID: 1386211
  207. The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis.
    J Bacteriol. 2003 Jan;185(1):60-70 PMID: 12486041
  208. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing.
    J Bacteriol. 1996 Oct;178(20):6036-42 PMID: 8830703
  209. Phosphate-starvation-inducible proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study.
    Microbiology. 1996 Nov;142 ( Pt 11):3163-70 PMID: 8969513
  210. Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis.
    J Bacteriol. 1999 Dec;181(23):7161-7 PMID: 10572116
  211. Arginine metabolism in lactic streptococci.
    J Bacteriol. 1982 Jun;150(3):1024-32 PMID: 6281231
  212. Lactobacillus sakei: recent developments and future prospects.
    Res Microbiol. 2001 Dec;152(10):839-48 PMID: 11766959
  213. Influence of starvation and biofilm formation on acid resistance of Streptococcus mutans.
    Oral Microbiol Immunol. 2001 Feb;16(1):24-7 PMID: 11169135
  214. The influence of specific foods and oral hygiene on the microflora of fissures and smooth surfaces of molar teeth: A 5-day study.
    Caries Res. 1999 Sep-Oct;33(5):349-56 PMID: 10460958
  215. pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes.
    J Exp Med. 1997 Oct 6;186(7):1159-63 PMID: 9314564
  216. Streptococcus mutans ffh, a gene encoding a homologue of the 54 kDa subunit of the signal recognition particle, is involved in resistance to acid stress.
    Microbiology. 1999 Feb;145 ( Pt 2):357-66 PMID: 10075418
  217. Modulator protein RsbR regulates environmental signalling in the general stress pathway of Bacillus subtilis.
    Mol Microbiol. 1997 May;24(3):567-78 PMID: 9179850
  218. Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells.
    Mol Microbiol. 1992 Nov;6(22):3289-97 PMID: 1484485
  219. Role of Listeria monocytogenes exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C in activation of human neutrophils.
    Infect Immun. 1999 Mar;67(3):1125-30 PMID: 10024552
  220. The Brevibacterium flavum sigma factor SigB has a role in the environmental stress response.
    FEMS Microbiol Lett. 2002 Oct 29;216(1):77-84 PMID: 12423756
  221. Altered protein expression of Streptococcus oralis cultured at low pH revealed by two-dimensional gel electrophoresis.
    Appl Environ Microbiol. 2001 Aug;67(8):3396-405 PMID: 11472910
  222. Regulation of the gtfBC and ftf genes of Streptococcus mutans in biofilms in response to pH and carbohydrate.
    Microbiology. 2001 Oct;147(Pt 10):2841-8 PMID: 11577162
  223. Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides.
    J Bacteriol. 1996 Apr;178(8):2178-85 PMID: 8636016
  224. Protein expression by planktonic and biofilm cells of Streptococcus mutans.
    FEMS Microbiol Lett. 2001 Nov 27;205(1):139-46 PMID: 11728728
  225. Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain.
    J Bacteriol. 1997 May;179(10):3362-4 PMID: 9150237
  226. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13855-60 PMID: 12370433
  227. Killed cultures of Escherichia coli can protect living organisms from acid stress.
    Microbiology. 2000 Aug;146 ( Pt 8):1759-60 PMID: 10931881
  228. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence.
    Appl Environ Microbiol. 1996 May;62(5):1693-8 PMID: 8633868
  229. Gene structure, organization, expression, and potential regulatory mechanisms of arginine catabolism in Enterococcus faecalis.
    J Bacteriol. 2002 Nov;184(22):6289-300 PMID: 12399499
  230. Genotypic heterogeneity of Streptococcus oralis and distinct aciduric subpopulations in human dental plaque.
    Appl Environ Microbiol. 2000 Aug;66(8):3330-6 PMID: 10919787
  231. Identification of sigma S-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri.
    Mol Microbiol. 1996 Sep;21(5):925-40 PMID: 8885264
  232. Enzyme level of enterococcal F1Fo-ATPase is regulated by pH at the step of assembly.
    Eur J Biochem. 1999 Jan;259(1-2):262-8 PMID: 9914501
  233. Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli.
    Trends Microbiol. 1998 Jun;6(6):214-6 PMID: 9675796
  234. Analysis of human T cell responses to group A streptococci using fractionated Streptococcus pyogenes proteins.
    FEMS Immunol Med Microbiol. 1997 Mar;17(3):161-70 PMID: 9093837
  235. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation.
    Mol Microbiol. 1998 Jan;27(2):299-310 PMID: 9484886
  236. Biosynthesis and metabolism of arginine in bacteria.
    Microbiol Rev. 1986 Sep;50(3):314-52 PMID: 3534538
  237. pH regulation by Streptococcus mutans.
    J Dent Res. 1992 May;71(5):1159-65 PMID: 1607433
  238. Composition of pooled resting plaque fluid from caries-free and caries-susceptible individuals.
    J Dent Res. 1988 Dec;67(12):1468-75 PMID: 3198844
  239. Genetics of acid adaptation in oral streptococci.
    Crit Rev Oral Biol Med. 2001;12(4):301-14 PMID: 11603503
  240. Problems of adverse pH and bacterial strategies to combat it.
    Novartis Found Symp. 1999;221:4-14, discussion 14-8 PMID: 10207910
  241. Cell density dependent acid sensitivity in stationary phase cultures of enterohemorrhagic Escherichia coli O157:H7.
    FEMS Microbiol Lett. 1999 Dec 15;181(2):289-95 PMID: 10585551
  242. SOS-regulated proteins in translesion DNA synthesis and mutagenesis.
    Trends Biochem Sci. 1995 Oct;20(10):416-20 PMID: 8533155
  243. Activation of Bacillus subtilis transcription factor sigma B by a regulatory pathway responsive to stationary-phase signals.
    J Bacteriol. 1992 Jun;174(11):3695-706 PMID: 1592822
Article Info
Journal
Microbiology and molecular biology reviews : MMBR
Abbr.
Microbiol Mol Biol Rev
ISSN
1092-2172
DOI
10.1128/MMBR.67.3.429-453.2003
Published
2003-09-00
Pages
429-53, table of contents
Language
English
Region
United States
NLM ID
9706653
PMCID
PMC193868
Subset
IM
External Links
PubMed source DOI: 10.1128/MMBR.67.3.429-453.2003 PMC Full Text View journal details
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