Coping with low pH: Molecular strategies in neutralophilic bacteria

FEMS Microbiology Reviews

Volumn 38, Issue 6, 2014, Pages 1091-1125

  Lund, Peter ^a   Tramonti, Angela ^b   De Biase, Daniela ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Acid tolerance response; Extreme acid resistance; Glutamate dependent acid resistance; Pathogenic bacteria; Two component systems; Virulence

Indexed keywords

ACID; AMINO ACID; AMMONIA; BACTERIAL PROTEIN; CARBOXYLIC ACID; DEAMINASE; INORGANIC ACID; LIPID; PROTON; UREA;

ACIDIFICATION; ACIDITY; BACILLUS CEREUS; BIFIDOBACTERIUM; BRUCELLA; CELL MEMBRANE; CELL PH; CLOSTRIDIUM; DECARBOXYLATION; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HEALTH STATUS; HELICOBACTER PYLORI; HUMAN; LACTOBACILLUS; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; MACROMOLECULE; MEMBRANE; NONHUMAN; PATHOGENICITY; PH; PHYSIOLOGICAL PROCESS; REVIEW; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STREPTOCOCCUS; VIBRIO CHOLERAE; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; ENVIRONMENT; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS;

ANIMALIA; ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; ENVIRONMENT; HYDROGEN-ION CONCENTRATION; STRESS, PHYSIOLOGICAL;

EID: 84924930823     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/1574-6976.12076     Document Type: Review

References (298)

1. Abe H, Miyahara A, Oshima T, Tashiro K, Ogura Y, Kuhara S, Ogasawara N, Hayashi T & Tobe T (2008) Global regulation by horizontally transferred regulators establishes the pathogenicity of Escherichia coli. DNA Res 15: 25-38.
2. Alsaker KV, Paredes C & Papoutsakis ET (2010) Metabolite stress and tolerance in the production of biofuels and chemicals: gene-expression-based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum. Biotechnol Bioeng 105: 1131-1147.
3. Alvarez-Ordonez A, Fernandez A, Lopez M & Bernardo A (2009) Relationship between membrane fatty acid composition and heat resistance of acid and cold stressed Salmonella senftenberg CECT 4384. Food Microbiol 26: 347-353.
4. Alvarez-Ordonez A, Fernandez A, Bernardo A & Lopez M (2010) Arginine and lysine decarboxylases and the acid tolerance response of Salmonella Typhimurium. Int J Food Microbiol 136: 278-282.
5. Amachi S, Ishikawa K, Toyoda S, Kagawa Y, Yokota A & Tomita F (1998) Characterization of a mutant of Lactococcus lactis with reduced membrane-bound ATPase activity under acidic conditions. Biosci Biotechnol Biochem 62: 1574-1580.
6. Arnold CN, McElhanon J, Lee A, Leonhart R & Siegele DA (2001) Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J Bacteriol 183: 2178-2186.
7. Azcarate-Peril MA, Altermann E, Hoover-Fitzula RL, Cano RJ & Klaenhammer TR (2004) Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl Environ Microbiol 70: 5315-5322.
8. Bandara AB, Contreras A, Contreras-Rodriguez A, Martins AM, Dobrean V, Poff-Reichow S, Rajasekaran P, Sriranganathan N, Schurig GG & Boyle SM (2007) Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7: 57.
9. Bearson S, Bearson B & Foster JW (1997) Acid stress responses in enterobacteria. FEMS Microbiol Lett 147: 173-180.
10. Bearson BL, Wilson L & Foster JW (1998) A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180: 2409-2417.
11. Bearson SM, Bearson BL & Rasmussen MA (2006) Identification of Salmonella enterica serovar Typhimurium genes important for survival in the swine gastric environment. Appl Environ Microbiol 72: 2829-2836.
12. Bekhit A, Fukamachi T, Saito H & Kobayashi H (2011) The role of OmpC and OmpF in acidic resistance in Escherichia coli. Biol Pharm Bull 34: 330-334.
13. Belli WA & Marquis RE (1991) Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microbiol 57: 1134-1138.
14. Bender GR, Sutton SV & Marquis RE (1986) Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infect Immun 53: 331-338.
15. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ & Rabinowitz JD (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5: 593-599.
16. Berk PA, Jonge R, Zwietering MH, Abee T & Kieboom J (2005) Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. J Appl Microbiol 99: 859-866.
17. Bhagwat AA, Chan L, Han R, Tan J, Kothary M, Jean-Gilles J & Tall BD (2005) Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect Immun 73: 4993-5003.
18. Blankenhorn D, Phillips J & Slonczewski JL (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.
19. Blethen SL, Boeker EA & Snell EE (1968) Argenine decarboxylase from Escherichia coli. I. Purification and specificity for substrates and coenzyme. J Biol Chem 243: 1671-1677.
20. Bock A & Gross R (2002) The unorthodox histidine kinases BvgS and EvgS are responsive to the oxidation status of a quinone electron carrier. Eur J Biochem 269: 3479-3484.
21. Booth IR, Cash P & O'Byrne C (2002) Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81: 33-42.
22. Borden JR, Jones SW, Indurthi D, Chen Y & Papoutsakis ET (2010) A genomic-library based discovery of a novel, possibly synthetic, acid-tolerance mechanism in Clostridium acetobutylicum involving non-coding RNAs and ribosomal RNA processing. Metab Eng 12: 268-281.
23. Broadbent JR, Larsen RL, Deibel V & Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192: 2445-2458.
24. Brown JL, Ross T, McMeekin TA & Nichols PD (1997) Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37: 163-173.
25. Browne N & Dowds BC (2002) Acid stress in the food pathogen Bacillus cereus. J Appl Microbiol 92: 404-414.
26. Budin-Verneuil A, Maguin E, Auffray Y, Ehrlich SD & Pichereau V (2005) Transcriptional analysis of the cyclopropane fatty acid synthase gene of Lactococcus lactis MG1363 at low pH. FEMS Microbiol Lett 250: 189-194.
27. Budin-Verneuil A, Maguin E, Auffray Y, Ehrlich DS & Pichereau V (2006) Genetic structure and transcriptional analysis of the arginine deiminase (ADI) cluster in Lactococcus lactis MG1363. Can J Microbiol 52: 617-622.
28. Burton NA, Johnson MD, Antczak P, Robinson A & Lund PA (2010) Novel aspects of the acid response network of E. coli K-12 are revealed by a study of transcriptional dynamics. J Mol Biol 401: 726-742.
29. Capitani G, De Biase D, Aurizi C, Gut H, Bossa F & Grutter MG (2003) Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J 22: 4027-4037.
30. Casalino M, Prosseda G, Barbagallo M, Iacobino A, Ceccarini P, Latella MC, Nicoletti M & Colonna B (2010) Interference of the CadC regulator in the arginine-dependent acid resistance system of Shigella and enteroinvasive E. coli. Int J Med Microbiol 300: 289-295.
31. Casiano-Colon A & Marquis RE (1988) Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microbiol 54: 1318-1324.
32. Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF & Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181: 3525-3535.
33. Castanie-Cornet MP, Treffandier H, Francez-Charlot A, Gutierrez C & Cam K (2007) The glutamate-dependent acid resistance system in Escherichia coli: essential and dual role of the His-Asp phosphorelay RcsCDB/AF. Microbiology 153: 238-246.
34. Castanie-Cornet MP, Cam K, Bastiat B, Cros A, Bordes P & Gutierrez C (2010) Acid stress response in Escherichia coli: mechanism of regulation of gadA transcription by RcsB and GadE. Nucleic Acids Res 38: 3546-3554.
35. Champomier Verges MC, Zuniga M, Morel-Deville F, Perez-Martinez G, Zagorec M & Ehrlich SD (1999) Relationships between arginine degradation, pH and survival in Lactobacillus sakei. FEMS Microbiol Lett 180: 297-304.
36. Chang YY & Cronan JE Jr (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33: 249-259.
37. Chen YY, Clancy KA & Burne RA (1996) Streptococcus salivarius urease: genetic and biochemical characterization and expression in a dental plaque streptococcus. Infect Immun 64: 585-592.
38. Chen YY, Weaver CA & Burne RA (2000) Dual functions of Streptococcus salivarius urease. J Bacteriol 182: 4667-4669.
39. Chen J, Cheng C, Xia Y, Zhao H, Fang C, Shan Y, Wu B & Fang W (2011) Lmo0036, an ornithine and putrescine carbamoyltransferase in Listeria monocytogenes, participates in arginine deiminase and agmatine deiminase pathways and mediates acid tolerance. Microbiology 157: 3150-3161.
40. Choi SH, Baumler DJ & Kaspar CW (2000) Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 66: 3911-3916.
41. Cid SB, Miguelez-Arrizado MJ, Becker B, Holzapfel WH & Vidal-Carou MC (2008) Amino acid decarboxylation by Lactobacillus curvatus CTC273 affected by the pH and glucose availability. Food Microbiol 25: 269-277.
42. Clarke DJ (2010) The Rcs phosphorelay: more than just a two-component pathway. Future Microbiol 5: 1173-1184.
43. Conte MP, Petrone G, Di Biase AM, Longhi C, Penta M, Tinari A, Superti F, Fabozzi G, Visca P & Seganti L (2002) Effect of acid adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon. Infect Immun 70: 4369-4378.
44. Cotter PD & Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67: 429-453, table of contents.
45. Cotter PD, Gahan CG & Hill C (2000) Analysis of the role of the Listeria monocytogenes F0F1 -AtPase operon in the acid tolerance response. Int J Food Microbiol 60: 137-146.
46. Cotter PD, Gahan CG & Hill C (2001) A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol 40: 465-475.
47. Cotter PD, Ryan S, Gahan CG & Hill C (2005) Presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains is associated with an ability to grow at low pH. Appl Environ Microbiol 71: 2832-2839.
48. Cozzani I, Misuri A & Santoni C (1970) Purification and general properties of glutamate decarboxylase from Clostridium perfringens. Biochem J 118: 135-141.
49. Cozzani I, Barsacchi R, Dibenedetto G, Saracchi L & Falcone G (1975) Regulation of breakdown and synthesis of L-glutamate decarboxylase in Clostridium perfringens. J Bacteriol 123: 1115-1123.
50. Croxen MA & Finlay BB (2010) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8: 26-38.
51. Cui S, Meng J & Bhagwat AA (2001) Availability of glutamate and arginine during acid challenge determines cell density-dependent survival phenotype of Escherichia coli strains. Appl Environ Microbiol 67: 4914-4918.
52. Cunin R, Glansdorff N, Pierard A & Stalon V (1986) Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev 50: 314-352.
53. Davis MJ, Coote PJ & O'Byrne CP (1996) Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance. Microbiology 142(Pt 10): 2975-2982.
54. De Biase D & Pennacchietti E (2012) Glutamate decarboxylase-dependent acid resistance in orally acquired bacteria: function, distribution and biomedical implications of the gadBC operon. Mol Microbiol 86: 770-786.
55. De Biase D, Tramonti A, Bossa F & Visca P (1999) The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol 32: 1198-1211.
56. Deamer DW (1987) Proton permeation of lipid bilayers. J Bioenerg Biomembr 19: 457-479.
57. Degnan BA, Fontaine MC, Doebereiner AH, Lee JJ, Mastroeni P, Dougan G, Goodacre JA & Kehoe MA (2000) Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. Infect Immun 68: 2441-2448.
58. Dell CL, Neely MN & Olson ER (1994) Altered pH and lysine signalling mutants of cadC, a gene encoding a membrane-bound transcriptional activator of the Escherichia coli cadBA operon. Mol Microbiol 14: 7-16.
59. Deng Z, Shan Y, Pan Q, Gao X & Yan A (2013) Anaerobic expression of the gadE-mdtEF multidrug efflux operon is primarily regulated by the two-component system ArcBA through antagonizing the H-NS mediated repression. Front Microbiol 4: 194.
60. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A & Wade WG (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
61. Diez-Gonzalez F & Karaibrahimoglu Y (2004) Comparison of the glutamate-, arginine- and lysine-dependent acid resistance systems in Escherichia coli O157:H7. J Appl Microbiol 96: 1237-1244.
62. Diez-Gonzalez F, Callaway TR, Kizoulis MG & Russell JB (1998) Grain feeding and the dissemination of acid-resistant Escherichia coli from cattle. Science 281: 1666-1668.
63. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE & Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
64. Eguchi Y, Itou J, Yamane M, Demizu R, Yamato F, Okada A, Mori H, Kato A & Utsumi R (2007) B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. P Natl Acad Sci USA 104: 18712-18717.
65. Eguchi Y, Ishii E, Hata K & Utsumi R (2011) Regulation of acid resistance by connectors of two-component signal transduction systems in Escherichia coli. J Bacteriol 193: 1222-1228.
66. Eguchi Y, Ishii E, Yamane M & Utsumi R (2012) The connector SafA interacts with the multi-sensing domain of PhoQ in Escherichia coli. Mol Microbiol 85: 299-313.
67. Eriksson S, Lucchini S, Thompson A, Rhen M & Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
68. Feehily C & Karatzas KA (2013) Role of glutamate metabolism in bacterial responses towards acid and other stresses. J Appl Microbiol 114: 11-24.
69. Ferenci T, Galbiati HF, Betteridge T, Phan K & Spira B (2011) The constancy of global regulation across a species: the concentrations of ppGpp and RpoS are strain-specific in Escherichia coli. BMC Microbiol 11: 62.
70. Ferreira A, Sue D, O'Byrne CP & Boor KJ (2003) Role of Listeria monocytogenes sigma(B) in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl Environ Microbiol 69: 2692-2698.
71. Fletcher KA (2012) Metabolomic Analysis of Escherichia coli O157:H7 under Acid Stress using Two-Dimensional Gas Chromatography-Time-of-Flight Mass Spectrometry. PhD Thesis. http://www.lib.ncsu.edu/resolver/1840.16/7898.
72. Flint HJ, Duncan SH, Scott KP & Louis P (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9: 1101-1111.
73. Flint HJ, Bayer EA, Rincon MT, Lamed R & White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6: 121-131.
74. Foit L, George JS, Zhang BW, Brooks CL 3rd & Bardwell JC (2013) Chaperone activation by unfolding. P Natl Acad Sci USA 110: E1254-E1262.
75. Foster JW (1993) The acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. J Bacteriol 175: 1981-1987.
76. Foster JW (2001) Acid stress responses of Salmonella and E. coli: survival mechanisms, regulation, and implications for pathogenesis. J Microbiol 39: 89-94.
77. Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2: 898-907.
78. Foster JW & Hall HK (1990) Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol 172: 771-778.
79. Foster JW & Hall HK (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173: 5129-5135.
80. Fozo EM & Quivey RG Jr (2004a) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70: 929-936.
81. Fozo EM & Quivey RG Jr (2004b) The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol 186: 4152-4158.
82. Fozo EM, Kajfasz JK & Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238: 291-295.
83. Frank C, Werber D, Cramer JPet al. (2011) Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365: 1771-1780.
84. Frees D, Vogensen FK & Ingmer H (2003) Identification of proteins induced at low pH in Lactococcus lactis. Int J Food Microbiol 87: 293-300.
85. Gajiwala KS & Burley SK (2000) HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295: 605-612.
86. Gale EF (1940) The production of amines by bacteria: the decarboxylation of amino-acids by strains of Bacterium coli. Biochem J 34: 392-413.
87. Gale EF (1946) The bacterial amino acid decarboxylases. Adv Enzymol 6: 1-31.
88. Garcia-del Portillo F, Foster JW & Finlay BB (1993) Role of acid tolerance response genes in Salmonella typhimurium virulence. Infect Immun 61: 4489-4492.
89. Georgellis D, Kwon O & Lin EC (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science 292: 2314-2316.
90. Giannella RA, Broitman SA & Zamcheck N (1972) Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13: 251-256.
91. Gong S, Richard H & Foster JW (2003) YjdE (AdiC) is the arginine:agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J Bacteriol 185: 4402-4409.
92. Gorden J & Small PL (1993) Acid resistance in enteric bacteria. Infect Immun 61: 364-367.
93. Goto Y, Calciano LJ & Fink AL (1990) Acid-induced folding of proteins. P Natl Acad Sci USA 87: 573-577.
94. Gould GW (1996) Methods for preservation and extension of shelf life. Int J Food Microbiol 33: 51-64.
95. Griswold AR, Chen YY & Burne RA (2004) Analysis of an agmatine deiminase gene cluster in Streptococcus mutans UA159. J Bacteriol 186: 1902-1904.
96. Gruening P, Fulde M, Valentin-Weigand P & Goethe R (2006) Structure, regulation, and putative function of the arginine deiminase system of Streptococcus suis. J Bacteriol 188: 361-369.
97. Gut H, Pennacchietti E, John RA, Bossa F, Capitani G, De Biase D & Grutter MG (2006) Escherichia coli acid resistance: pH-sensing, activation by chloride and autoinhibition in GadB. EMBO J 25: 2643-2651.
98. Gutknecht J & Walter A (1981) Transport of protons and hydrochloric acid through lipid bilayer membranes. Biochim Biophys Acta 641: 183-188.
99. Hahn K, Faustoferri RC & Quivey RG Jr (1999) Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH. Mol Microbiol 31: 1489-1498.
100. Hall HK & Foster JW (1996) The role of fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol 178: 5683-5691.
101. Haneburger I, Eichinger A, Skerra A & Jung K (2011) New insights into the signaling mechanism of the pH-responsive, membrane-integrated transcriptional activator CadC of Escherichia coli. J Biol Chem 286: 10681-10689.
102. Haneburger I, Fritz G, Jurkschat N, Tetsch L, Eichinger A, Skerra A, Gerland U & Jung K (2012) Deactivation of the E. coli pH stress sensor CadC by cadaverine. J Mol Biol 424: 15-27.
103. Hanna MN, Ferguson RJ, Li YH & Cvitkovitch DG (2001) uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans. J Bacteriol 183: 5964-5973.
104. Haque M, Hirai Y, Yokota K, Mori N, Jahan I, Ito H, Hotta H, Yano I, Kanemasa Y & Oguma K (1996) Lipid profile of Helicobacter spp.: presence of cholesteryl glucoside as a characteristic feature. J Bacteriol 178: 2065-2070.
105. Hayes ET, Wilks JC, Sanfilippo P, Yohannes E, Tate DP, Jones BD, Radmacher MD, BonDurant SS & Slonczewski JL (2006) Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol 6: 89.
106. Heithoff DM, Conner CP, Hanna PC, Julio SM, Hentschel U & Mahan MJ (1997) Bacterial infection as assessed by in vivo gene expression. P Natl Acad Sci USA 94: 934-939.
107. Hengge R (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160: 667-676.
108. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: 373-395, table of contents.
109. Hersh BM, Farooq FT, Barstad DN, Blankenhorn DL & Slonczewski JL (1996) A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178: 3978-3981.
110. Heuveling J, Possling A & Hengge R (2008) A role for Lon protease in the control of the acid resistance genes of Escherichia coli. Mol Microbiol 69: 534-547.
111. Heyde M & Portalier R (1990) Acid shock proteins of Escherichia coli. FEMS Microbiol Lett 57: 19-26.
112. Higuchi T, Hayashi H & Abe K (1997) Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. J Bacteriol 179: 3362-3364.
113. Hinsinger P, Plassard C, Tang C & Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248: 43-59.
114. Hirshfield IN, Terzulli S & O'Byrne C (2003) Weak organic acids: a panoply of effects on bacteria. Sci Prog 86: 245-269.
115. Ho NAT, Hou CY, Kim WH & Kang TJ (2013) Expanding the active pH range of Escherichia coli glutamate decarboxylase by breaking the cooperativeness. J Biosci Bioeng 115: 154-158.
116. Hommais F, Krin E, Coppee JY, Lacroix C, Yeramian E, Danchin A & Bertin P (2004) GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150: 61-72.
117. Hong W, Wu YE, Fu X & Chang Z (2012) Chaperone-dependent mechanisms for acid resistance in enteric bacteria. Trends Microbiol 20: 328-335.
118. Howden CW & Hunt RH (1987) Relationship between gastric secretion and infection. Gut 28: 96-107.
119. Hughes DT, Terekhova DA, Liou L, Hovde CJ, Sahl JW, Patankar AV, Gonzalez JE, Edrington TS, Rasko DA & Sperandio V (2010) Chemical sensing in mammalian host-bacterial commensal associations. P Natl Acad Sci USA 107: 9831-9836.
120. Hutkins RW (2008) Microbiology and Technology of Fermented Foods. IFT Press Series, Vol. 22. John Wiley & Sons, Oxford, UK.
121. Itou J, Eguchi Y & Utsumi R (2009) Molecular mechanism of transcriptional cascade initiated by the EvgS/EvgA system in Escherichia coli K-12. Biosci Biotechnol Biochem 73: 870-878.
122. Ivy RA, Wiedmann M & Boor KJ (2012) Listeria monocytogenes grown at 7 degrees C shows reduced acid survival and an altered transcriptional response to acid shock compared to L. monocytogenes grown at 37 degrees C. Appl Environ Microbiol 78: 3824-3836.
123. Iyer R, Williams C & Miller C (2003) Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J Bacteriol 185: 6556-6561.
124. Jayaraman GC, Penders JE & Burne RA (1997) 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 25: 329-341.
125. Jenkinson HF (2011) Beyond the oral microbiome. Environ Microbiol 13: 3077-3087.
126. Jeong KC, Hung KF, Baumler DJ, Byrd JJ & Kaspar CW (2008) Acid stress damage of DNA is prevented by Dps binding in Escherichia coli O157:H7. BMC Microbiol 8: 181.
127. Jin J, Liu S, Zhao L, Ge K, Mao X & Ren F (2011) Changes in ffh, uvrA, groES and dnaK mRNA abundance as a function of acid-adaptation and growth phase in Bifidobacterium longum BBMN68 isolated from healthy centenarians. Curr Microbiol 62: 612-617.
128. Jobin MP, Clavel T, Carlin F & Schmitt P (2002) Acid tolerance response is low-pH and late-stationary growth phase inducible in Bacillus cereus TZ415. Int J Food Microbiol 79: 65-73.
129. Johnson DB & Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338: 3-14.
130. Johnson MD, Burton NA, Gutierrez B, Painter K & Lund PA (2011) RcsB is required for inducible acid resistance in Escherichia coli and acts at gadE-dependent and -independent promoters. J Bacteriol 193: 3653-3656.
131. Jones JE, Dreyton CJ, Flick H, Causey CP & Thompson PR (2010) Mechanistic studies of agmatine deiminase from multiple bacterial species. Biochemistry 49: 9413-9423.
132. Kailasan Vanaja S, Bergholz TM & Whittam TS (2009) Characterization of the Escherichia coli O157:H7 Sakai GadE regulon. J Bacteriol 191: 1868-1877.
133. Kajfasz JK, Martinez AR, Rivera-Ramos I, Abranches J, Koo H, Quivey RG Jr & Lemos JA (2009) Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J Bacteriol 191: 2060-2068.
134. Kanjee U & Houry WA (2013) Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol 67: 65-81.
135. Karatzas KA, Brennan O, Heavin S, Morrissey J & O'Byrne CP (2010) Intracellular accumulation of high levels of gamma-aminobutyrate by Listeria monocytogenes 10403S in response to low pH: uncoupling of gamma-aminobutyrate synthesis from efflux in a chemically defined medium. Appl Environ Microbiol 76: 3529-3537.
136. Karatzas KA, Suur L & O'Byrne CP (2012) Characterization of the intracellular glutamate decarboxylase system: analysis of its function, transcription, and role in the acid resistance of various strains of Listeria monocytogenes. Appl Environ Microbiol 78: 3571-3579.
137. Kern R, Malki A, Abdallah J, Tagourti J & Richarme G (2007) Escherichia coli HdeB is an acid stress chaperone. J Bacteriol 189: 603-610.
138. Kieboom J & Abee T (2006) Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. J Bacteriol 188: 5650-5653.
139. Kim JR & Cho KH (2006) The multi-step phosphorelay mechanism of unorthodox two-component systems in E. coli realizes ultrasensitivity to stimuli while maintaining robustness to noises. Comput Biol Chem 30: 438-444.
140. Kim BH, Kim S, Kim HG, Lee J, Lee IS & Park YK (2005) The formation of cyclopropane fatty acids in Salmonella enterica serovar Typhimurium. Microbiology 151: 209-218.
141. Kitko RD, Cleeton RL, Armentrout EI, Lee GE, Noguchi K, Berkmen MB, Jones BD & Slonczewski JL (2009) Cytoplasmic acidification and the benzoate transcriptome in Bacillus subtilis. PLoS One 4: e8255.
142. Kobayashi H, Suzuki T & Unemoto T (1986) Streptococcal cytoplasmic pH is regulated by changes in amount and activity of a proton-translocating ATPase. J Biol Chem 261: 627-630.
143. Koelz HR (1992) Gastric acid in vertebrates. Scand J Gastroenterol Suppl 193: 2-6.
144. Koponen J, Laakso K, Koskenniemi K, Kankainen M, Savijoki K, Nyman TA, de Vos WM, Tynkkynen S, Kalkkinen N & Varmanen P (2012) Effect of acid stress on protein expression and phosphorylation in Lactobacillus rhamnosus GG. J Proteomics 75: 1357-1374.
145. Kovacikova G, Lin W & Skorupski K (2010) The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J Bacteriol 192: 4181-4191.
146. Krin E, Danchin A & Soutourina O (2010) Decrypting the H-NS-dependent regulatory cascade of acid stress resistance in Escherichia coli. BMC Microbiol 10: 273.
147. Krulwich TA, Sachs G & Padan E (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9: 330-343.
148. Kuhnert WL, Quivey RG Jr & Jr (2003) Genetic and biochemical characterization of the F-ATPase operon from Streptococcus sanguis 10904. J Bacteriol 185: 1525-1533.
149. Kuhnert WL, Zheng G, Faustoferri RC & Quivey RG Jr (2004) The F-ATPase operon promoter of Streptococcus mutans is transcriptionally regulated in response to external pH. J Bacteriol 186: 8524-8528.
150. Kullen MJ & Klaenhammer TR (1999) Identification of the pH-inducible, proton-translocating F1F0-ATPase (atpBEFHAGDC) operon of Lactobacillus acidophilus by differential display: gene structure, cloning and characterization. Mol Microbiol 33: 1152-1161.
151. Lee YH, Kim BH, Kim JH, Yoon WS, Bang SH & Park YK (2007) CadC has a global translational effect during acid adaptation in Salmonella enterica serovar Typhimurium. J Bacteriol 189: 2417-2425.
152. Lee K, Lee HG, Pi K & Choi YJ (2008a) The effect of low pH on protein expression by the probiotic bacterium Lactobacillus reuteri. Proteomics 8: 1624-1630.
153. Lee YH, Kim JH, Bang IS & Park YK (2008b) The membrane-bound transcriptional regulator CadC is activated by proteolytic cleavage in response to acid stress. J Bacteriol 190: 5120-5126.
154. Len AC, Harty DW & Jacques NA (2004a) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology 150: 1353-1366.
155. Len AC, Harty DW & Jacques NA (2004b) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150: 1339-1351.
156. Li H & Cao Y (2010) Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39: 1107-1116.
157. Li Y & Zamble DB (2009) pH-responsive DNA-binding activity of Helicobacter pylori NikR. Biochemistry 48: 2486-2496.
158. Li YH, Chen YY & Burne RA (2000) Regulation of urease gene expression by Streptococcus salivarius growing in biofilms. Environ Microbiol 2: 169-177.
159. Lin J, Lee IS, Frey J, Slonczewski JL & Foster JW (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177: 4097-4104.
160. Lin J, Smith MP, Chapin KC, Baik HS, Bennett GN & Foster JW (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62: 3094-3100.
161. Lindahl T & Nyberg B (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11: 3610-3618.
162. Liu Y & Burne RA (2009) Multiple two-component systems of Streptococcus mutans regulate agmatine deiminase gene expression and stress tolerance. J Bacteriol 191: 7363-7366.
163. Liu Y, Zeng L & Burne RA (2009) AguR is required for induction of the Streptococcus mutans agmatine deiminase system by low pH and agmatine. Appl Environ Microbiol 75: 2629-2637.
164. Loesche WJ (1986) The identification of bacteria associated with periodontal disease and dental caries by enzymatic methods. Oral Microbiol Immunol 1: 65-72.
165. Lorca GL, Font de Valdez G & Ljungh A (2002) Characterization of the protein-synthesis dependent adaptive acid tolerance response in Lactobacillus acidophilus. J Mol Microbiol Biotechnol 4: 525-532.
166. Lu J, Chen T, Wu J, Wilson PC, Hao X & Qian J (2011) Acid tolerance of an acid mine drainage bioremediation system based on biological sulfate reduction. Bioresour Technol 102: 10401-10406.
167. Lu P, Ma D, Chen Y, Guo Y, Chen GQ, Deng H & Shi Y (2013) L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23: 635-644.
168. Lucas PM, Blancato VS, Claisse O, Magni C, Lolkema JS & Lonvaud-Funel A (2007) Agmatine deiminase pathway genes in Lactobacillus brevis are linked to the tyrosine decarboxylation operon in a putative acid resistance locus. Microbiology 153: 2221-2230.
169. Ma Z, Masuda N & Foster JW (2004) Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J Bacteriol 186: 7378-7389.
170. Ma D, Lu P, Yan C, Fan C, Yin P, Wang J & Shi Y (2012) Structure and mechanism of a glutamate-GABA antiporter. Nature 483: 632-636.
171. Ma D, Lu P & Shi Y (2013) Substrate selectivity of the acid-activated glutamate/gamma-aminobutyric acid (GABA) antiporter GadC from Escherichia coli. J Biol Chem 288: 15148-15153.
172. Majdalani N, Hernandez D & Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46: 813-826.
173. Malpica R, Franco B, Rodriguez C, Kwon O & Georgellis D (2004) Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. P Natl Acad Sci USA 101: 13318-13323.
174. Marcus EA, Moshfegh AP, Sachs G & Scott DR (2005) The periplasmic alpha-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J Bacteriol 187: 729-738.
175. Marcus EA, Sachs G, Wen Y, Feng J & Scott DR (2012) Role of the Helicobacter pylori sensor kinase ArsS in protein trafficking and acid acclimation. J Bacteriol 194: 5545-5551.
176. Marshall BJ & Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1: 1311-1315.
177. Martinelle K & Haggstrom L (1997) On the dissociation constant of ammonium: effects of using an incorrect pK(a) in calculations of the ammonia concentration in animal cell cultures. Biotechnol Tech 11: 549-551.
178. Martinez AR, Abranches J, Kajfasz JK & Lemos JA (2010) Characterization of the Streptococcus sobrinus acid-stress response by interspecies microarrays and proteomics. Mol Oral Microbiol 25: 331-342.
179. Martinez KA 2nd, Kitko RD, Mershon JP, Adcox HE, Malek KA, Berkmen MB & Slonczewski JL (2012) Cytoplasmic pH response to acid stress in individual cells of Escherichia coli and Bacillus subtilis observed by fluorescence ratio imaging microscopy. Appl Environ Microbiol 78: 3706-3714.
180. Masuda N & Church GM (2002) Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 184: 6225-6234.
181. Matin A, Wilson B, Zychlinsky E & Matin M (1982) Proton motive force and the physiological basis of delta pH maintenance in thiobacillus acidophilus. J Bacteriol 150: 582-591.
182. Matsumoto M, Ohishi H & Benno Y (2004) H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93: 109-113.
183. Maurer LM, Yohannes E, Bondurant SS, Radmacher M & Slonczewski JL (2005) pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187: 304-319.
184. Maus JE & Ingham SC (2003) Employment of stressful conditions during culture production to enhance subsequent cold- and acid-tolerance of bifidobacteria. J Appl Microbiol 95: 146-154.
185. McLaggan D, Naprstek J, Buurman ET & Epstein W (1994) Interdependence of K+ and glutamate accumulation during osmotic adaptation of Escherichia coli. J Biol Chem 269: 1911-1917.
186. Meng SY & Bennett GN (1992a) Regulation of the Escherichia coli cad operon: location of a site required for acid induction. J Bacteriol 174: 2670-2678.
187. Meng SY & Bennett GN (1992b) Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol 174: 2659-2669.
188. Merrell DS & Camilli A (1999) The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol Microbiol 34: 836-849.
189. Merrell DS & Camilli A (2000) Regulation of Vibrio cholerae genes required for acid tolerance by a member of the "ToxR-like" family of transcriptional regulators. J Bacteriol 182: 5342-5350.
190. Merrell DS & Camilli A (2002) Acid tolerance of gastrointestinal pathogens. Curr Opin Microbiol 5: 51-55.
191. Merrell DS, Bailey C, Kaper JB & Camilli A (2001) The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J Bacteriol 183: 2746-2754.
192. Merrell DS, Goodrich ML, Otto G, Tompkins LS & Falkow S (2003) pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect Immun 71: 3529-3539.
193. Miller SI, Kukral AM & Mekalanos JJ (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. P Natl Acad Sci USA 86: 5054-5058.
194. Mobley HL, Island MD & Hausinger RP (1995) Molecular biology of microbial ureases. Microbiol Rev 59: 451-480.
195. Molenaar D, Bosscher JS, ten Brink B, Driessen AJ & Konings WN (1993) Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J Bacteriol 175: 2864-2870.
196. Mols M, van Kranenburg R, van Melis CC, Moezelaar R & Abee T (2010a) Analysis of acid-stressed Bacillus cereus reveals a major oxidative response and inactivation-associated radical formation. Environ Microbiol 12: 873-885.
197. Mols M, van Kranenburg R, Tempelaars MH, van Schaik W, Moezelaar R & Abee T (2010b) Comparative analysis of transcriptional and physiological responses of Bacillus cereus to organic and inorganic acid shocks. Int J Food Microbiol 137: 13-21.
198. Moreau PL (2007) The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 189: 2249-2261.
199. Mujacic M & Baneyx F (2007) Chaperone Hsp31 contributes to acid resistance in stationary-phase Escherichia coli. Appl Environ Microbiol 73: 1014-1018.
200. Muller S, Gotz M & Beier D (2009) Histidine residue 94 is involved in pH sensing by histidine kinase ArsS of Helicobacter pylori. PLoS One 4: e6930.
201. Muller C, Bahlawane C, Aubert S, Delay CM, Schauer K, Michaud-Soret I & De Reuse H (2011) Hierarchical regulation of the NikR-mediated nickel response in Helicobacter pylori. Nucleic Acids Res 39: 7564-7575.
202. Nakajo K, Takahashi N & Beighton D (2010) Resistance to acidic environments of caries-associated bacteria: Bifidobacterium dentium and Bifidobacterium longum. Caries Res 44: 431-437.
203. Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136: 65-80.
204. Neumann G & Martinoia E (2002) Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci 7: 162-167.
205. Nguyen Y & Sperandio V (2012) Enterohemorrhagic E. coli (EHEC) pathogenesis. Front Cell Infect Microbiol 2: 90.
206. Nye PH (1981) Changes of pH across the rhizosphere induced by roots. Plant Soil 61: 7-26.
207. Occhialini A, Jimenez de Bagues MP, Saadeh B, Bastianelli D, Hanna N, De Biase D & Kohler S (2012) The glutamic acid decarboxylase system of the new species Brucella microti contributes to its acid resistance and to oral infection of mice. J Infect Dis 206: 1424-1432.
208. Ogahara T, Ohno M, Takayama M, Igarashi K & Kobayashi H (1995) Accumulation of glutamate by osmotically stressed Escherichia coli is dependent on pH. J Bacteriol 177: 5987-5990.
209. O'Sullivan E & 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: 4210-4215.
210. O'Sullivan E & Condon S (1999) Relationship between acid tolerance, cytoplasmic pH, and ATP and H+-ATPase levels in chemostat cultures of Lactococcus lactis. Appl Environ Microbiol 65: 2287-2293.
211. Ottemann KM & Lowenthal AC (2002) Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect Immun 70: 1984-1990.
212. Park YK, Bearson B, Bang SH, Bang IS & Foster JW (1996) Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol Microbiol 20: 605-611.
213. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N & Sibley RK (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325: 1127-1131.
214. Pennacchietti E, Lammens TM, Capitani G, Franssen MC, John RA, Bossa F & De Biase D (2009) Mutation of His465 alters the pH-dependent spectroscopic properties of Escherichia coli glutamate decarboxylase and broadens the range of its activity toward more alkaline pH. J Biol Chem 284: 31587-31596.
215. Pflock M, Kennard S, Delany I, Scarlato V & Beier D (2005) Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori. Infect Immun 73: 6437-6445.
216. Pflock M, Finsterer N, Joseph B, Mollenkopf H, Meyer TF & Beier D (2006) Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J Bacteriol 188: 3449-3462.
217. Planamente S, Mondy S, Hommais F, Vigouroux A, Morera S & Faure D (2012) Structural basis for selective GABA binding in bacterial pathogens. Mol Microbiol 86: 1085-1099.
218. Porsch K, Meier J, Kleinsteuber S & Wendt-Potthoff K (2009) Importance of different physiological groups of iron reducing microorganisms in an acidic mining lake remediation experiment. Microb Ecol 57: 701-717.
219. Porte F, Liautard JP & Kohler S (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect Immun 67: 4041-4047.
220. Price SB, Cheng CM, Kaspar CW, Wright JC, DeGraves FJ, Penfound TA, Castanie-Cornet MP & Foster JW (2000) Role of rpoS in acid resistance and fecal shedding of Escherichia coli O157:H7. Appl Environ Microbiol 66: 632-637.
221. Price SB, Wright JC, DeGraves FJ, Castanie-Cornet MP & Foster JW (2004) Acid resistance systems required for survival of Escherichia coli O157:H7 in the bovine gastrointestinal tract and in apple cider are different. Appl Environ Microbiol 70: 4792-4799.
222. Prost LR & Miller SI (2008) The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol 10: 576-582.
223. Prost LR, Daley ME, Le Sage V, Bader MW, Le Moual H, Klevit RE & Miller SI (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26: 165-174.
224. Quiocho FA & Ledvina PS (1996) Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol Microbiol 20: 17-25.
225. Quivey RG Jr, Faustoferri RC, Clancy KA & Marquis RE (1995) Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency. FEMS Microbiol Lett 126: 257-261.
226. Quivey RG Jr, Faustoferri R, Monahan K & Marquis R (2000) Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett 189: 89-92.
227. Ramond J-B, Welz PJ, Le Roes-Hill M, Tuffin MI, Burton SG & Cowan DA (2013) Selection of Clostridium spp. in biological sand filters neutralizing synthetic acid mine drainage. FEMS Microbiol Ecol 87: 678-690.
228. Rasko DA, Rosovitz MJ, Myers GS et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881-6893.
229. Richard H & Foster JW (2004) Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol 186: 6032-6041.
230. Riggins DP, Narvaez MJ, Martinez KA, Harden MM & Slonczewski JL (2013) Escherichia coli K-12 survives anaerobic exposure at pH 2 without RpoS, Gad, or hydrogenases, but shows sensitivity to autoclaved broth products. PLoS One 8: e56796.
231. Rollan G, Lorca GL & de Valdez GF (2003) Arginine catabolism and acid tolerance response in Lactobacillus reuteri isolated from sourdough. Food Microbiol 20: 313-319.
232. Russell JB, Diez-Gonzalez F & Jarvis GN (2000) Potential effect of cattle diets on the transmission of pathogenic Escherichia coli to humans. Microbes Infect 2: 45-53.
233. Ryan S, Begley M, Gahan CG & Hill C (2009) Molecular characterization of the arginine deiminase system in Listeria monocytogenes: regulation and role in acid tolerance. Environ Microbiol 11: 432-445.
234. Sachs G, Weeks DL, Melchers K & Scott DR (2003) The gastric biology of Helicobacter pylori. Annu Rev Physiol 65: 349-369.
235. Sachs G, Weeks DL, Wen Y, Marcus EA, Scott DR & Melchers K (2005) Acid acclimation by Helicobacter pylori. Physiology (Bethesda) 20: 429-438.
236. Salmond CV, Kroll RG & Booth IR (1984) The effect of food preservatives on pH homeostasis in Escherichia coli. J Gen Microbiol 130: 2845-2850.
237. Sanchez B, Champomier-Verges MC, Collado Mdel C, Anglade P, Baraige F, Sanz Y, de los Reyes-Gavilan CG, Margolles A & Zagorec M (2007) Low-pH adaptation and the acid tolerance response of Bifidobacterium longum biotype longum. Appl Environ Microbiol 73: 6450-6459.
238. Sanchez-Andrea I, Rodriguez N, Amils R & Sanz JL (2011) Microbial diversity in anaerobic sediments at Rio Tinto, a naturally acidic environment with a high heavy metal content. Appl Environ Microbiol 77: 6085-6093.
239. Sanders JW, Leenhouts K, Burghoorn J, Brands JR, Venema G & Kok J (1998) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol 27: 299-310.
240. Sangari FJ, Seoane A, Rodriguez MC, Aguero J & Garcia Lobo JM (2007) Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infect Immun 75: 774-780.
241. Sangari FJ, Cayon AM, Seoane A & Garcia-Lobo JM (2010) Brucella abortus ure2 region contains an acid-activated urea transporter and a nickel transport system. BMC Microbiol 10: 107.
242. Santiago B, MacGilvray M, Faustoferri RC & Quivey RG Jr (2012) The branched-chain amino acid aminotransferase encoded by ilvE is involved in acid tolerance in Streptococcus mutans. J Bacteriol 194: 2010-2019.
243. Schmidt MA (2010) LEEways: tales of EPEC, ATEC and EHEC. Cell Microbiol 12: 1544-1552.
244. Scott DR, Marcus EA, Wen Y, Singh S, Feng J & Sachs G (2010) Cytoplasmic histidine kinase (HP0244)-regulated assembly of urease with UreI, a channel for urea and its metabolites, CO2, NH3, and NH4(+), is necessary for acid survival of Helicobacter pylori. J Bacteriol 192: 94-103.
245. Senouci-Rezkallah K, Schmitt P & Jobin MP (2011) Amino acids improve acid tolerance and internal pH maintenance in Bacillus cereus ATCC14579 strain. Food Microbiol 28: 364-372.
246. Shabala L & Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159: 458-461.
247. Shin S, Castanie-Cornet MP, Foster JW, Crawford JA, Brinkley C & Kaper JB (2001) An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol 41: 1133-1150.
248. Shioi JI, Matsuura S & Imae Y (1980) Quantitative measurements of proton motive force and motility in Bacillus subtilis. J Bacteriol 144: 891-897.
249. Shukuya R & Schwert GW (1960) Glutamic acid decarboxylase. I. Isolation procedures and properties of the enzyme. J Biol Chem 235: 1649-1652.
250. Slonczewski JL, Rosen BP, Alger JR & Macnab RM (1981) pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. P Natl Acad Sci USA 78: 6271-6275.
251. Slonczewski JL, Fujisawa M, Dopson M & Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 55(1-79): 317.
252. Smolka AJ, Lacy ER, Luciano L & Reale E (1994) Identification of gastric H, K-ATPase in an early vertebrate, the Atlantic stingray Dasyatis sabina. J Histochem Cytochem 42: 1323-1332.
253. Su MS, Schlicht S & Ganzle MG (2011) Contribution of glutamate decarboxylase in Lactobacillus reuteri to acid resistance and persistence in sourdough fermentation. Microb Cell Fact 10(Suppl 1): S8.
254. Sun Y, Fukamachi T, Saito H & Kobayashi H (2012a) Respiration and the F(1)Fo-ATPase enhance survival under acidic conditions in Escherichia coli. PLoS One 7: e52577.
255. Sun Y, Fukamachi T, Saito H & Kobayashi H (2012b) Adenosine deamination increases the survival under acidic conditions in Escherichia coli. J Appl Microbiol 112: 775-781.
256. Swanson JM & Simons J (2009) Role of charge transfer in the structure and dynamics of the hydrated proton. J Phys Chem B 113: 5149-5161.
257. Tam NK, Uyen NQ, Hong HA, le Duc H, Hoa TT, Serra CR, Henriques AO & Cutting SM (2006) The intestinal life cycle of Bacillus subtilis and close relatives. J Bacteriol 188: 2692-2700.
258. Tapley TL, Franzmann TM, Chakraborty S, Jakob U & Bardwell JC (2010) Protein refolding by pH-triggered chaperone binding and release. P Natl Acad Sci USA 107: 1071-1076.
259. Tatsuno I, Nagano K, Taguchi K, Rong L, Mori H & Sasakawa C (2003) Increased adherence to Caco-2 cells caused by disruption of the yhiE and yhiF genes in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 71: 2598-2606.
260. Teixeira-Gomes AP, Cloeckaert A & Zygmunt MS (2000) Characterization of heat, oxidative, and acid stress responses in Brucella melitensis. Infect Immun 68: 2954-2961.
261. Tennant SM, Hartland EL, Phumoonna T, Lyras D, Rood JI, Robins-Browne RM & van Driel IR (2008) Influence of gastric acid on susceptibility to infection with ingested bacterial pathogens. Infect Immun 76: 639-645.
262. Tetsch L, Koller C, Haneburger I & Jung K (2008) The membrane-integrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol Microbiol 67: 570-583.
263. Tetsch L, Koller C, Donhofer A & Jung K (2011) Detection and function of an intramolecular disulfide bond in the pH-responsive CadC of Escherichia coli. BMC Microbiol 11: 74.
264. Theron MM & Lues JFR (2010) Organic Acids and Food Preservation. CRC Press, USA.
265. Thomassin S, Jobin MP & Schmitt P (2006) The acid tolerance response of Bacillus cereus ATCC14579 is dependent on culture pH, growth rate and intracellular pH. Arch Microbiol 186: 229-239.
266. Touchon M, Hoede C, Tenaillon O et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344.
267. Tree JJ, Roe AJ, Flockhart A et al. (2011) Transcriptional regulators of the GAD acid stress island are carried by effector protein-encoding prophages and indirectly control type III secretion in enterohemorrhagic Escherichia coli O157:H7. Mol Microbiol 80: 1349-1365.
268. Tsai MF & Miller C (2013) Substrate selectivity in arginine-dependent acid resistance in enteric bacteria. P Natl Acad Sci USA 110: 5893-5897.
269. Tsai MF, McCarthy P & Miller C (2013) Substrate selectivity in glutamate-dependent acid resistance in enteric bacteria. P Natl Acad Sci USA 110: 5898-5902.
270. Tucker DL, Tucker N & Conway T (2002) Gene expression profiling of the pH response in Escherichia coli. J Bacteriol 184: 6551-6558.
271. Tucker DL, Tucker N, Ma Z, Foster JW, Miranda RL, Cohen PS & Conway T (2003) Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185: 3190-3201.
272. Ugurbil K, Rottenberg H, Glynn P & Shulman RG (1978) 31P nuclear magnetic resonance studies of bioenergetics and glycolysis in anaerobic Escherichia coli cells. P Natl Acad Sci USA 75: 2244-2248.
273. Valderas MW, Alcantara RB, Baumgartner JE, Bellaire BH, Robertson GT, Ng WL, Richardson JM, Winkler ME & Roop RM 2nd (2005) Role of HdeA in acid resistance and virulence in Brucella abortus 2308. Vet Microbiol 107: 307-312.
274. van Vliet AHM, Poppelaars SW, Davies BJ, Stoof J, Bereswill S, Kist M, Penn CW, Kuipers EJ & Kusters JG (2002) NikR mediates nickel-responsive transcriptional induction of urease expression in Helicobacter pylori. Infect Immun 70: 2846-2852.
275. van Vliet AHM, Ernst FD & Kusters JG (2004) NikR-mediated regulation of Helicobacter pylori acid adaptation. Trends Microbiol 12: 489-494.
276. Ventura M, Canchaya C, van Sinderen D, Fitzgerald GF & Zink R (2004) Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Appl Environ Microbiol 70: 3110-3121.
277. Ventura M, Turroni F, Zomer A et al. (2009) The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5: e1000785.
278. Viala JP, Meresse S, Pocachard B, Guilhon AA, Aussel L & Barras F (2011) Sensing and adaptation to low pH mediated by inducible amino acid decarboxylases in Salmonella. PLoS One 6: e22397.
279. Vilain S, Luo Y, Hildreth MB & Brozel VS (2006) Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl Environ Microbiol 72: 4970-4977.
280. Villarreal L, Heredia NL & Garcia S (2000) Changes in protein synthesis and acid tolerance in Clostridium perfringens type A in response to acid shock. Int Microbiol 3: 113-116.
281. Waddington L, Cyr T, Hefford M, Hansen LT & Kalmokoff M (2010) Understanding the acid tolerance response of bifidobacteria. J Appl Microbiol 108: 1408-1420.
282. Wall T, Bath K, Britton RA, Jonsson H, Versalovic J & Roos S (2007) The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl Environ Microbiol 73: 3924-3935.
283. Waterman SR & Small PL (1996) Identification of sigma S-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri. Mol Microbiol 21: 925-940.
284. Waterman SR & Small PL (2003) The glutamate-dependent acid resistance system of Escherichia coli and Shigella flexneri is inhibited in vitro by L-trans-pyrrolidine-2, 4-dicarboxylic acid. FEMS Microbiol Lett 224: 119-125.
285. Watson N, Dunyak DS, Rosey EL, Slonczewski JL & Olson ER (1992) Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH. J Bacteriol 174: 530-540.
286. Weber H, Polen T, Heuveling J, Wendisch VF & Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187: 1591-1603.
287. Weeks DL, Eskandari S, Scott DR & Sachs G (2000) A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287: 482-485.
288. Wemekamp-Kamphuis HH, Wouters JA, de Leeuw PP, Hain T, Chakraborty T & Abee T (2004) Identification of sigma factor sigma B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl Environ Microbiol 70: 3457-3466.
289. Wen Y, Marcus EA, Matrubutham U, Gleeson MA, Scott DR & Sachs G (2003) Acid-adaptive genes of Helicobacter pylori. Infect Immun 71: 5921-5939.
290. Wen Y, Feng J, Scott DR, Marcus EA & Sachs G (2009) The pH-responsive regulon of HP0244 (FlgS), the cytoplasmic histidine kinase of Helicobacter pylori. J Bacteriol 191: 449-460.
291. Wen Y, Feng J & Sachs G (2013) Helicobacter pylori 5′ureB-sRNA, a cis-encoded antisense small RNA, negatively regulates ureAB expression by transcription termination. J Bacteriol 195: 444-452.
292. Wilks JC & Slonczewski JL (2007) pH of the cytoplasm and periplasm of Escherichia coli: Rapid measurement by green fluorescent protein fluorimetry. J Bacteriol 189: 5601-5607.
293. Wilks JC, Kitko RD, Cleeton SH, Lee GE, Ugwu CS, Jones BD, BonDurant SS & Slonczewski JL (2009) Acid and base stress and transcriptomic responses in Bacillus subtilis. Appl Environ Microbiol 75: 981-990.
294. Wilmes-Riesenberg MR, Foster JW & Curtiss R 3rd (1997) An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun 65: 203-210.
295. Young GM, Amid D & Miller VL (1996) A bifunctional urease enhances survival of pathogenic Yersinia enterocolitica and Morganella morganii at low pH. J Bacteriol 178: 6487-6495.
296. Zanotti G & Cendron L (2010) Functional and structural aspects of Helicobacter pylori acidic stress response factors. IUBMB Life 62: 715-723.
297. Zhang M, Lin S, Song X, Liu J, Fu Y, Ge X, Fu X, Chang Z & Chen PR (2011) A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat Chem Biol 7: 671-677.
298. Zhao B & Houry WA (2010) Acid stress response in enteropathogenic gammaproteobacteria: an aptitude for survival. Biochem Cell Biol 88: 301-314.