Acid stress response in environmental and clinical strains of enteric bacteria

Gabriel J. SWENSON, J. STOCHASTIC, Franklyn F. BOLANDER, Jr., Richard A. LONG

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Front. Biol. ›› 2012, Vol. 7 ›› Issue (6) : 495-505. DOI: 10.1007/s11515-012-1191-5
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REVIEW

Acid stress response in environmental and clinical strains of enteric bacteria

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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.

Keywords

acid stress response / enteric bacteria / microbial ecology / transcriptional regulation / virulence

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Gabriel J. SWENSON, J. STOCHASTIC, Franklyn F. BOLANDER, Jr., Richard A. LONG. Acid stress response in environmental and clinical strains of enteric bacteria. Front Biol, 2012, 7(6): 495‒505 https://doi.org/10.1007/s11515-012-1191-5

References

[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[7]
Baker-Austin C, Dopson M (2007). Life in acid: pH homeostasis in acidophiles. Trends Microbiol, 15(4): 165–171
CrossRef Pubmed Google scholar
[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
CrossRef Google scholar
[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
CrossRef Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[16]
Blokesch M, Schoolnik G K (2007). Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog, 3(6): e81
CrossRef Pubmed Google scholar
[17]
Brandl M T (2006). Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol, 44(1): 367–392
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[24]
Ciaramella M, Napoli A, Rossi M (2005). Another extreme genome: how to live at pH 0. Trends Microbiol, 13(2): 49–51
CrossRef Pubmed Google scholar
[25]
Colwell R R (1996). Global climate and infectious disease: the cholera paradigm. Science, 274(5295): 2025–2031
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[27]
De Angelis M, Gobbetti M (2004). Environmental stress responses in Lactobacillus: a review. Proteomics, 4(1): 106–122
CrossRef Pubmed Google scholar
[28]
Dong T, Schellhorn H E (2010). Role of RpoS in virulence of pathogens. Infect Immun, 78(3): 887–897
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[33]
Foster J W (1991). Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol, 173(21): 6896–6902
Pubmed
[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
Pubmed
[35]
Foster J W (1999). When protons attack: microbial strategies of acid adaptation. Curr Opin Microbiol, 2(2): 170–174
CrossRef Pubmed Google scholar
[36]
Foster J W (2004). Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol, 2(11): 898–907
CrossRef Pubmed Google scholar
[37]
Foster J W, Hall H K (1990). Adaptive acidification tolerance response of Salmonella typhimurium. J Bacteriol, 172(2): 771–778
Pubmed
[38]
Foster J W, Spector M P (1995). How Salmonella survive against the odds. Annu Rev Microbiol, 49(1): 145–174
CrossRef Pubmed Google scholar
[39]
Foster P L (2007). Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol, 42(5): 373–397
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Google scholar
[52]
Iyer R, Williams C, Miller C (2003). Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J Bacteriol, 185(22): 6556–6561
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[55]
Joelsson A, Kan B, Zhu J (2007). Quorum sensing enhances the stress response in Vibrio cholerae. Appl Environ Microbiol, 73(11): 3742–3746
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[69]
Leyer G J, Johnson E A (1992). Acid adaptation promotes survival of Salmonella spp. in cheese. Appl Environ Microbiol, 58(6): 2075–2080
Pubmed
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
Pubmed
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[78]
Masuda N, Church G M (2003). Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol, 48(3): 699–712
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[87]
Merrell D S, Camilli A (2002). Acid tolerance of gastrointestinal pathogens. Curr Opin Microbiol, 5(1): 51–55
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[92]
Nalin D R (1976). Cholera, copepods, and chitinase. Lancet, 2(7992): 958–960
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[95]
Nyström T (2004). Stationary-phase physiology. Annu Rev Microbiol, 58(1): 161–181
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[98]
Peterson K M (2002). Expression of Vibrio cholerae virulence genes in response to environmental signals. Curr Issues Intest Microbiol, 3(2): 29–38
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[104]
Pruzzo C, Vezzulli L, Colwell R R (2008). Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol, 10(6): 1400–1410
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[119]
Tischler A D, Camilli A (2004). Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol, 53(3): 857–869
CrossRef Pubmed Google scholar
[120]
Tischler A D, Camilli A (2005). Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun, 73(9): 5873–5882
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[132]
Zhu J, Mekalanos J J (2003). Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell, 5(4): 647–656
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar

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