REVIEW

Acid stress response in environmental and clinical strains of enteric bacteria

  • Gabriel J. SWENSON , 1,3 ,
  • J. STOCHASTIC 1 ,
  • Franklyn F. BOLANDER, Jr. 1 ,
  • Richard A. LONG 1,2
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  • 1. Biological Sciences, University of South Carolina, Columbia, SC 29208, USA
  • 2. Marine Science Program, University of South Carolina, Columbia, SC 29208, USA
  • 3. Biology Department, Paine College, Augusta, GA 30901, USA

Received date: 18 Oct 2011

Accepted date: 16 Jan 2012

Published date: 01 Dec 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

The success of many enteric bacteria is hinged on the ability to tolerate environmental stress such as extreme acidity. The acid stress response (ASR) has been investigated in many enteric bacteria and has been shown to involve variable expression of a broad spectrum of genes involved in transcriptional regulation, metabolism, colonization and virulence; representing a linkage between acid tolerance and pathogenicity. Though the majority of ASR studies have been conducted in laboratory conditions and from the perspective of pathogenicity, the role of environmental reservoirs on acid adaptation has recently emerged as an important aspect of pathogenic microbial ecology. This mini-review profiles ASR in three opportunistic enteric pathogens and synthesizes recent work pertaining to the study of this dynamic response.

Cite this article

Gabriel J. SWENSON , J. STOCHASTIC , Franklyn F. BOLANDER, Jr. , Richard A. LONG . Acid stress response in environmental and clinical strains of enteric bacteria[J]. Frontiers in Biology, 2012 , 7(6) : 495 -505 . DOI: 10.1007/s11515-012-1191-5

1
Abuaita B H, Withey J H (2009). Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun, 77(9): 4111–4120

DOI PMID

2
Ahmer B M M (2004). Cell-to-cell signaling in Escherichia coli and Salmonella enterica. Mol Microbiol, 52(4): 933–945

3
Angelichio M J, Merrell D S, Camilli A (2004). Spatiotemporal analysis of acid adaptation-mediated Vibrio cholerae hyperinfectivity. Infect Immun, 72(4): 2405–2407

DOI PMID

4
Arnold C N, McElhanon J, Lee A, Leonhart R, Siegele D A (2001). Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J Bacteriol, 183(7): 2178–2186

DOI PMID

5
Assadian N W, Fenn L B, Flores-Ortiz M A, Ali A S (1999). Spatial variability of solutes in a pecan orchard surface-irrigated with untreated effluents in the upper Rio Grande River basin. Agric Water Manag, 42(2): 143–156

6
Bader M W, Navarre W W, Shiau W, Nikaido H, Frye J G, McClelland M, Fang F C, Miller S I (2003). Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol, 50(1): 219–230

DOI PMID

7
Baker-Austin C, Dopson M (2007). Life in acid: pH homeostasis in acidophiles. Trends Microbiol, 15(4): 165–171

DOI PMID

8
Baudart J, Grabulos J, Barusseau J P, Lebaron P (2000). Salmonella spp. and fecal coliform loads in coastal waters from a point vs. nonpoint source of pollution. J Environ Qual, 29(1): 241–250

DOI

9
Beales N (2004). Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: A review. Compr Rev Food Sci F, 3(1): 1–20

DOI

10
Bearson B L, Wilson L, Foster J W (1998). A low pH-Inducible, PhoPQ-Dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress (vol 180, pg 2409, 1998). J Bacteriol, 180(14): 3734–3734

11
Bergholz T M, Vanaja S K, Whittam T S (2009). Gene expression induced in Escherichia coli O157:H7 upon exposure to model apple juice. Appl Environ Microbiol, 75(11): 3542–3553

DOI PMID

12
Beyhan S, Tischler A D, Camilli A, Yildiz F H (2006). Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J Bacteriol, 188(10): 3600–3613

DOI PMID

13
Bhagwat A A (2006). Microbiological Safety of Fresh-cut Produce: Where Are We Now? American Society for Microbiology Press, 121–165

14
Bhagwat A A, Bhagwat M (2008). Methods and tools for comparative genomics of foodborne pathogens. Foodborne Pathog Dis, 5(4): 487–497

DOI PMID

15
Bhagwat A A, Chan L, Han R, Tan J, Kothary M, Jean-Gilles J, Tall B D (2005). Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect Immun, 73(8): 4993–5003

DOI PMID

16
Blokesch M, Schoolnik G K (2007). Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog, 3(6): e81

DOI PMID

17
Brandl M T (2006). Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol, 44(1): 367–392

DOI PMID

18
Butler S M, Nelson E J, Chowdhury N, Faruque S M, Calderwood S B, Camilli A (2006). Cholera stool bacteria repress chemotaxis to increase infectivity. Mol Microbiol, 60(2): 417–426

DOI PMID

19
Capozzi V, Fiocco D, Amodio M L, Gallone A, Spano G (2009). Bacterial stressors in minimally processed food. Int J Mol Sci, 10(7): 3076–3105

DOI PMID

20
Chang Y Y, Cronan J E Jr (1999). Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol, 33(2): 249–259

DOI PMID

21
Cheville A M, Arnold K W, Buchrieser C, Cheng C M, Kaspar C W (1996). rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl Environ Microbiol, 62(5): 1822–1824

22
Chiang S L, Mekalanos J J (1998). Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol Microbiol, 27(4): 797–805

DOI PMID

23
Choi S H, Baumler D J, Kaspar C W (2000). Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl Environ Microbiol, 66(9): 3911–3916

DOI PMID

24
Ciaramella M, Napoli A, Rossi M (2005). Another extreme genome: how to live at pH 0. Trends Microbiol, 13(2): 49–51

DOI PMID

25
Colwell R R (1996). Global climate and infectious disease: the cholera paradigm. Science, 274(5295): 2025–2031

DOI PMID

26
Cotter P D, Hill C (2003). Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev, 67(3): 429–453

DOI PMID

27
De Angelis M, Gobbetti M (2004). Environmental stress responses in Lactobacillus: a review. Proteomics, 4(1): 106–122

DOI PMID

28
Dong T, Schellhorn H E (2010). Role of RpoS in virulence of pathogens. Infect Immun, 78(3): 887–897

DOI PMID

29
Doyle M P, Erickson M C (2008). Summer meeting 2007—the problems with fresh produce: an overview. J Appl Microbiol, 105(2): 317–330

DOI PMID

30
Faruque S M, Biswas K, Udden S M N, Ahmad Q S, Sack D A, Nair G B, Mekalanos J J (2006). Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc Natl Acad Sci USA, 103(16): 6350–6355

DOI PMID

31
Faucher S P, Porwollik S, Dozois C M, McClelland M, Daigle F (2006). Transcriptome of Salmonella enterica Serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci USA, 103(6): 1906–1911

DOI PMID

32
Flahaut S, Hartke A, Giard J C, Benachour A, Boutibonnes P, Auffray Y (1996). Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol Lett, 138(1): 49–54

DOI PMID

33
Foster J W (1991). Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol, 173(21): 6896–6902

PMID

34
Foster J W (1993). The acid tolerance response of Salmonella typhimurium involves transient synthesis of key acid shock proteins. J Bacteriol, 175(7): 1981–1987

PMID

35
Foster J W (1999). When protons attack: microbial strategies of acid adaptation. Curr Opin Microbiol, 2(2): 170–174

DOI PMID

36
Foster J W (2004). Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol, 2(11): 898–907

DOI PMID

37
Foster J W, Hall H K (1990). Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol, 172(2): 771–778

PMID

38
Foster J W, Spector M P (1995). How Salmonella survive against the odds. Annu Rev Microbiol, 49(1): 145–174

DOI PMID

39
Foster P L (2007). Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol, 42(5): 373–397

DOI PMID

40
Frees D, Varmanen P, Ingmer H (2001). Inactivation of a gene that is highly conserved in Gram-positive bacteria stimulates degradation of non-native proteins and concomitantly increases stress tolerance in Lactococcus lactis. Mol Microbiol, 41(1): 93–103

DOI PMID

41
Frees D, Vogensen F K, Ingmer H (2003). Identification of proteins induced at low pH in Lactococcus lactis. Int J Food Microbiol, 87(3): 293–300

DOI PMID

42
Garcia S S, Ake C, Clement B, Huebner H J, Donnelly K C, Shalat S L (2001). Initial results of environmental monitoring in the Texas Rio Grande Valley. Environ Int, 26(7–8): 465–474

DOI PMID

43
Goel A K, Jiang S C (2010). Genetic determinants of virulence, antibiogram and altered biotype among the Vibrio cholerae O1 isolates from different cholera outbreaks in India. Infect Genet Evol, 10(6): 814–819

DOI PMID

44
Goodson M, Rowbury R J (1989). Resistance of acid-habituated Escherichia coli to organic acids and its medical and applied significance. Lett Appl Microbiol, 8(6): 211–214.

45
Greenacre E J, Lucchini S, Hinton J C D, Brocklehurst T F (2006). The lactic acid-induced acid tolerance response in Salmonella enterica Serovar Typhimurium induces sensitivity to hydrogen peroxide. Appl Environ Microbiol, 72(8): 5623–5625

DOI PMID

46
Hanning I B, Nutt J D, Ricke S C (2009). Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathog Dis, 6(6): 635–648

DOI PMID

47
Hayes E T, Wilks J C, Sanfilippo P, Yohannes E, Tate D P, Jones B D, Radmacher M D, BonDurant S S, Slonczewski J L (2006). Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol, 6(1): 89

DOI PMID

48
Heidelberg J F, Eisen J A, Nelson W C, Clayton R A, Gwinn M L, Dodson R J, Haft D H, Hickey E K, Peterson J D, Umayam L, Gill S R, Nelson K E, Read T D, Tettelin H, Richardson D, Ermolaeva M D, Vamathevan J, Bass S, Qin H, Dragoi I, Sellers P, McDonald L, Utterback T, Fleishmann R D, Nierman W C, White O, Salzberg S L, Smith H O, Colwell R R, Mekalanos J J, Venter J C, Fraser C M (2000). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature, 406(6795): 477–483

DOI PMID

49
Hersh B M, Farooq F T, Barstad D N, Blankenhorn D L, Slonczewski J L (1996). A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol, 178(13): 3978–3981

PMID

50
Hommais F, Krin E, Coppée J Y, 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(1): 61–72

DOI PMID

51
Hsieh J L, Fries J S, Noble R T (2007). Vibrio and phytoplankton dynamics during the summer of 2004 in a eutrophying estuary. Ecol Appl, 17(5): S102–S109

DOI

52
Iyer R, Williams C, Miller C (2003). Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J Bacteriol, 185(22): 6556–6561

DOI PMID

53
Johnson M D, Burton N A, Gutierrez B, Painter K, Lund P A (2011). RcsB is required for inducible acid resistance in E. coli and acts at gadE dependent and independent promoters, J Bacteriol online

54
Jiang S C, Louis V, Choopun N, Sharma A, Huq A, Colwell R R (2000). Genetic diversity of Vibrio cholerae in Chesapeake Bay determined by amplified fragment length polymorphism fingerprinting. Appl Environ Microbiol, 66(1): 140–147

DOI PMID

55
Joelsson A, Kan B, Zhu J (2007). Quorum sensing enhances the stress response in Vibrio cholerae. Appl Environ Microbiol, 73(11): 3742–3746

DOI PMID

56
Kamruzzaman M, Udden S M N, Cameron D E, Calderwood S B, Nair G B, Mekalanos J J, Faruque S M (2010). Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc Natl Acad Sci USA, 107(4): 1588–1593

DOI PMID

57
Kang Y S, Weber K D, Qiu Y, Kiley P J, Blattner F R (2005). Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol, 187(3): 1135–1160

DOI PMID

58
King T, Lucchini S, Hinton J C D, Gobius K (2010). Transcriptomic analysis of Escherichia coli O157:H7 and K-12 cultures exposed to inorganic and organic acids in stationary phase reveals acidulant- and strain-specific acid tolerance responses App. Environ Microbiol, 76(19): 6514–6528

DOI

59
Kirkpatrick C, Maurer L M, Oyelakin N E, Yoncheva Y N, Maurer R, Slonczewski J L (2001). Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J Bacteriol, 183(21): 6466–6477

DOI PMID

60
Kirn T J, Jude B A, Taylor R K (2005). A colonization factor links Vibrio cholerae environmental survival and human infection. Nature, 438(7069): 863–866

DOI PMID

61
Kirschner A K T, Schlesinger J, Farnleitner A H, Hornek R, Süss B, Golda B, Herzig A, Reitner B (2008). Rapid growth of planktonic Vibrio cholerae non-O1/non-O139 strains in a large alkaline lake in Austria: dependence on temperature and dissolved organic carbon quality. Appl Environ Microbiol, 74(7): 2004–2015

DOI PMID

62
Kitko R D, Wilks J C, Garduque G M, Slonczewski J L (2010). Osmolytes contribute to pH homeostasis of Escherichia coli. PLoS ONE, 5(4): e10078

DOI PMID

63
Koutsoumanis K P, Kendall P A, Sofos J N (2003). Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Appl Environ Microbiol, 69(12): 7514–7516

DOI PMID

64
Koutsoumanis K P, Sofos J N (2004). Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella Typhimurium after habituation at different pH conditions. Lett Appl Microbiol, 38(4): 321–326

DOI PMID

65
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(16): 4181–4191

DOI PMID

66
Kovacikova G, Skorupski K (2002). Binding site requirements of the virulence gene regulator AphB: differential affinities for the Vibrio cholerae classical and El Tor tcpPH promoters. Mol Microbiol, 44(2): 533–547

DOI PMID

67
Krin E, Danchin A, Soutourina O (2010a). Decrypting the H-NS-dependent regulatory cascade of acid stress resistance in Escherichia coli. BMC Microbiol, 10(1): 273

DOI PMID

68
Krin E, Danchin A, Soutourina O (2010b). RcsB plays a central role in H-NS-dependent regulation of motility and acid stress resistance in Escherichia coli. Res Microbiol, 161(5): 363–371

DOI PMID

69
Leyer G J, Johnson E A (1992). Acid adaptation promotes survival of Salmonella spp. in cheese. Appl Environ Microbiol, 58(6): 2075–2080

PMID

70
Leyer G J, Johnson E A (1993). Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl Environ Microbiol, 59(6): 1842–1847

PMID

71
Li C C, Crawford J A, DiRita V J, Kaper J B (2000). Molecular cloning and transcriptional regulation of ompT, a ToxR-repressed gene in Vibrio cholerae. Mol Microbiol, 35(1): 189–203

DOI PMID

72
Lin J S, Lee I S, Frey J, Slonczewski J L, Foster J W (1995). Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol, 177(14): 4097–4104

PMID

73
Lin J S, Smith M P, Chapin K C, Baik H S, Bennett G N, Foster J W (1996). Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol, 62(9): 3094–3100

PMID

74
López-Solanilla E, García-Olmedo F, Rodríguez-Palenzuela P (1998). Inactivation of the sapA to sapF locus of Erwinia chrysanthemi reveals common features in plant and animal bacterial pathogenesis. Plant Cell, 10(6): 917–924

PMID

75
López-Solanilla E, Llama-Palacios A, Collmer A, García-Olmedo F, Rodríguez-Palenzuela P (2001). Relative effects on virulence of mutations in the sap, pel, and hrp loci of Erwinia chrysanthemi. Mol Plant Microbe Interact, 14(3): 386–393

DOI PMID

76
Ma Z, Gong S M, Richard H, Tucker D L, Conway T, Foster J W (2003). GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol, 49(5): 1309–1320

DOI PMID

77
Ma Z, Masuda N, Foster J W (2004). Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J Bacteriol, 186(21): 7378–7389

DOI PMID

78
Masuda N, Church G M (2003). Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol, 48(3): 699–712

DOI PMID

79
Mathur J, Davis B M, Waldor M K (2007). Antimicrobial peptides activate the Vibrio cholerae sigmaE regulon through an OmpU-dependent signalling pathway. Mol Microbiol, 63(3): 848–858

DOI PMID

80
Mathur J, Waldor M K (2004). The Vibrio cholerae ToxR-regulated porin OmpU confers resistance to antimicrobial peptides. Infect Immun, 72(6): 3577–3583

DOI PMID

81
Matson J S, Withey J H, DiRita V J (2007). Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun, 75(12): 5542–5549

DOI PMID

82
Maurer L M, Yohannes E, Bondurant S S, Radmacher M, Slonczewski J L (2005). pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol, 187(1): 304–319

DOI PMID

83
Merrell D S, Bailey C, Kaper J B, Camilli A (2001). The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J Bacteriol, 183(9): 2746–2754

DOI PMID

84
Merrell D S, Butler S M, Qadri F, Dolganov N A, Alam A, Cohen M B, Calderwood S B, Schoolnik G K, Camilli A (2002a). Host-induced epidemic spread of the cholera bacterium. Nature, 417(6889): 642–645

DOI PMID

85
Merrell D S, Camilli A (1999). The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol Microbiol, 34(4): 836–849

DOI PMID

86
Merrell D S, 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(19): 5342–5350

DOI PMID

87
Merrell D S, Camilli A (2002). Acid tolerance of gastrointestinal pathogens. Curr Opin Microbiol, 5(1): 51–55

DOI PMID

88
Merrell D S, Goodrich M L, Otto G, Tompkins L S, Falkow S (2003). pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect Immun, 71(6): 3529–3539

DOI PMID

89
Merrell D S, Hava D L, Camilli A (2002b). Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol Microbiol, 43(6): 1471–1491

DOI PMID

90
Mols M, van Kranenburg R, Tempelaars M H, van Schaik W, Moezelaar R, Abee T (2010). Comparative analysis of transcriptional and physiological responses of Bacillus cereus to organic and inorganic acid shocks. Int J Food Microbiol, 137(1): 13–21

DOI PMID

91
Nachin L, Barras F (2000). External pH: an environmental signal that helps to rationalize pel gene duplication in Erwinia chrysanthemi. Mol Plant Microbe Interact, 13(8): 882–886

DOI PMID

92
Nalin D R (1976). Cholera, copepods, and chitinase. Lancet, 2(7992): 958–960

DOI PMID

93
Nalin D R, Daya V, Reid A, Levine M M, Cisneros L (1979). Adsorption and growth of Vibrio cholerae on chitin. Infect Immun, 25(2): 768–770

PMID

94
Nutt J D, Pillai S D, Woodward C L, Sternes K L, Zabala-Díaz I B, Kwon Y M, Ricke S C (2003). Use of a Salmonella typhimurium hilA fusion strain to assess effects of environmental fresh water sources on virulence gene expression. Water Res, 37(14): 3319–3326

DOI PMID

95
Nyström T (2004). Stationary-phase physiology. Annu Rev Microbiol, 58(1): 161–181

DOI PMID

96
Padan E, Bibi E, Ito M, Krulwich T A (2005). Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta, 1717(2): 67–88

DOI PMID

97
Parra-Lopez C, Baer M T, Groisman E A (1993). Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J, 12(11): 4053–4062

PMID

98
Peterson K M (2002). Expression of Vibrio cholerae virulence genes in response to environmental signals. Curr Issues Intest Microbiol, 3(2): 29–38

PMID

99
Polen T, Rittmann D, Wendisch V F, Sahm H (2003). DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate. Appl Environ Microbiol, 69(3): 1759–1774

DOI PMID

100
Polo F, Figueras M J, Inza I, Sala J, Fleisher J M, Guarro J (1998). Relationship between presence of Salmonella and indicators of faecal pollution in aquatic habitats. FEMS Microbiol Lett, 160 (2): 253–256

101
Price S B, Cheng C M, Kaspar C W, Wright J C, DeGraves F J, Penfound T A, Castanie-Cornet M P, Foster J W (2000). Role of rpoS in acid resistance and fecal shedding of Escherichia coli O157:H7. Appl Environ Microbiol, 66(2): 632–637

DOI PMID

135
Price S B, Wright J C, DeGraves F J, Castanie-Comet M P, Foster J W (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(8): 4792–4799

DOI PMID

102
Prost L R, Daley M E, Le Sage V, Bader M W, Le Moual H, Klevit R E, Miller S I (2007). Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell, 26(2): 165–174

DOI PMID

103
Provenzano D, Klose K E (2000). Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci USA, 97(18): 10220–10224

DOI PMID

104
Pruzzo C, Vezzulli L, Colwell R R (2008). Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol, 10(6): 1400–1410

DOI PMID

105
Rallu F, Gruss A, Ehrlich S D, Maguin E (2000). Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol Microbiol, 35(3): 517–528

DOI PMID

106
Rehfuss M Y M, Parker C T, Brandl M T (2011). Salmonella transcriptional signature in Tetrahymena phagosomes and role of acid tolerance in passage through the protist. ISME J, 5(2): 262–273

DOI PMID

107
Reidl J, Klose K E (2002). Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev, 26(2): 125–139

DOI PMID

108
Rhee J E, Ju H M, Park U, Park B C, Choi S H (2004). Identification of the Vibrio vulnificus cadC and Evaluation of Its Role in Acid Tolerance. J Microbiol Biotechnol, 14(5): 1093–1098

109
Richard H, Foster J W (2004). Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol, 186(18): 6032–6041

DOI PMID

110
Richards G M, Beuchat L R (2005). Infection of cantaloupe rind with Cladosporium cladosporioides and Penicillium expansum, and associated migration of Salmonella poona into edible tissues. Int J Food Microbiol, 103(1): 1–10

DOI PMID

111
Rowbury R J (1995). An assessment of environmental factors influencing acid tolerance and sensitivity in Escherichia coli, Salmonella spp. and other enterobacteria. Lett Appl Microbiol, 20(6): 333–337

DOI PMID

112
Rutherford S T, van Kessel J C, Shao Y, Bassler B L (2011). AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev, 25(4): 397–408

DOI PMID

113
Schild S, Tamayo R, Nelson E J, Qadri F, Calderwood S B, Camilli A (2007). Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe, 2(4): 264–277

DOI PMID

114
Small P, Blankenhorn D, Welty D, Zinser E, Slonczewski J L (1994). Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol, 176(6): 1729–1737

PMID

115
Song T, Mika F, Lindmark B, Liu Z, Schild S, Bishop A, Zhu J, Camilli A, Johansson J, Vogel J, Wai S N (2008). A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol, 70(1): 100–111

DOI PMID

116
Stincone A, Rahman A S, Antczak P, Henderson I, Cole J, Johnson M D, Lund P (2011). A systems biology approach sheds new light on Escherichia coli acid resistance. Nucl. Acids Res. 39(17): 7512–752

117
Sun Y R, Fukamachi T, Saito H, Kobayashi H (2011). ATP requirement for acidic resistance in Escherichia coli. J Bacteriol, 193(12): 3072–3077

DOI PMID

118
Tamayo R, Patimalla B, Camilli A (2010). Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infect Immun, 78(8): 3560–3569

DOI PMID

119
Tischler A D, Camilli A (2004). Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol, 53(3): 857–869

DOI PMID

120
Tischler A D, Camilli A (2005). Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun, 73(9): 5873–5882

DOI PMID

121
Tucker D L, Tucker N, Conway T (2002). Gene expression profiling of the pH response in Escherichia coli. J Bacteriol, 184(23): 6551–6558

DOI PMID

122
Tucker D L, Tucker N, Ma Z, Foster J W, Miranda R L, Cohen P S, Conway T (2003). Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol, 185(10): 3190–3201

DOI PMID

123
van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich S D, Maguin E (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, 82(1–4): 187–216

DOI PMID

124
Vezzulli L, Guzmán C A, Colwell R R, Pruzzo C (2008). Dual role colonization factors connecting Vibrio cholerae’s lifestyles in human and aquatic environments open new perspectives for combating infectious diseases. Curr Opin Biotechnol, 19(3): 254–259

DOI PMID

125
Wade W N, Beuchat L R (2003). Metabiosis of proteolytic moulds and Salmonella in raw, ripe tomatoes. J Appl Microbiol, 95(3): 437–450

DOI PMID

126
Wade W N, Vasdinnyei R, Deak T, Beuchat L R (2003). Proteolytic yeasts isolated from raw, ripe tomatoes and metabiotic association of Geotrichum candidum with Salmonella. Int J Food Microbiol, 86(1–2): 101–111

DOI PMID

127
Weber H, Polen T, Heuveling J, Wendisch V F, Hengge R (2005). Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and σ factor selectivity. J Bacteriol, 187(5): 1591–1603

DOI PMID

128
Wilmes-Riesenberg M R, Foster J W, Curtiss R 3rd (1997). An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun, 65(1): 203–210

PMID

129
Withey J H, DiRita V J (2005). Activation of both acfA and acfD transcription by Vibrio cholerae ToxT requires binding to two centrally located DNA sites in an inverted repeat conformation. Mol Microbiol, 56(4): 1062–1077

DOI PMID

130
Withey J H, DiRita V J (2006). The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol Microbiol, 59(6): 1779–1789

DOI PMID

131
Xie Y, Chou L S, Cutler A, Weimer B (2004). DNA Macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl Environ Microbiol, 70(11): 6738–6747

DOI PMID

132
Zhu J, Mekalanos J J (2003). Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell, 5(4): 647–656

DOI PMID

133
Zo Y G, Chokesajjawatee N, Grim C, Arakawa E, Watanabe H, Colwell R R (2009). Diversity and seasonality of bioluminescent Vibrio cholerae populations in Chesapeake Bay. Appl Environ Microbiol, 75(1): 135–146

DOI PMID

134
Zwir I, Shin D, Kato A, Nishino K, Latifi T, Solomon F, Hare J M, Huang H, Groisman E A (2005). Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA, 102(8): 2862–2867

DOI PMID

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