Acknowledgement
This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning [NRF-2022R1A2B5B02002256, NRF-2022R1A4A1025913, and NRF-2020M3A9H5104235 to E.-J.L. and NRF-2021R1I1A1A01043879 to E.C.] and a grant from Korea University.
References
- Verdu E, Viani F, Armstrong D, Fraser R, Siegrist H, Pignatelli B, et al. 1994. Effect of omeprazole on intragastric bacterial counts, nitrates, nitrites, and N-nitroso compounds. Gut. 35: 455-460. https://doi.org/10.1136/gut.35.4.455
- Zilberstein D, Agmon V, Schuldiner S, Padan E. 1984. Escherichia coli intracellular pH, membrane potential, and cell growth. J. Bacteriol. 158: 246-252. https://doi.org/10.1128/jb.158.1.246-252.1984
- Gorden J, Small P. 1993. Acid resistance in enteric bacteria. Infect. Immun. 61: 364-367. https://doi.org/10.1128/iai.61.1.364-367.1993
- Foster JW, Hall HK. 1990. Adaptive acidification tolerance response of Salmonella Typhimurium. J. Bacteriol. 172: 771-778. https://doi.org/10.1128/jb.172.2.771-778.1990
- Lund P, Tramonti A, De Biase D. 2014. Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol. Rev. 38: 1091-1125. https://doi.org/10.1111/1574-6976.12076
- 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. https://doi.org/10.1128/jb.177.14.4097-4104.1995
- 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. https://doi.org/10.1128/aem.62.9.3094-3100.1996
- Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF, Foster JW. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 3525-3535. https://doi.org/10.1128/JB.181.11.3525-3535.1999
- Small P, Blankenhorn D, Welty D, Zinser E, Slonczewski JL. 1994. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J. Bacteriol. 176: 1729-1737. https://doi.org/10.1128/jb.176.6.1729-1737.1994
- Ma Z, Richard H, Foster JW. 2003. pH-Dependent modulation of cyclic AMP levels and GadW-dependent repression of RpoS affect synthesis of the GadX regulator and Escherichia coli acid resistance. J. Bacteriol. 185: 6852-6859. https://doi.org/10.1128/JB.185.23.6852-6859.2003
- Richard HT, Foster JW. 2003. Acid resistance in Escherichia coli. Adv. Appl. Microbiol. 52: 167-186. https://doi.org/10.1016/S0065-2164(03)01007-4
- Guerra PR, Herrero-Fresno A, Ladero V, Redruello B, Dos Santos TP, Spiegelhauer MR, et al. 2018. Putrescine biosynthesis and export genes are essential for normal growth of avian pathogenic Escherichia coli. BMC Microbiol. 18: 226.
- Kanjee U, Houry WA. 2013. Mechanisms of acid resistance in Escherichia coli. Annu. Rev. Microbiol. 67: 65-81. https://doi.org/10.1146/annurev-micro-092412-155708
- Iyer R, Iverson TM, Accardi A, Miller C. 2002. A biological role for prokaryotic ClC chloride channels. Nature 419: 715-718. https://doi.org/10.1038/nature01000
- 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. https://doi.org/10.1128/JB.186.18.6032-6041.2004
- Foster JW, Hall HK. 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella Typhimurium. J. Bacteriol. 173: 5129-5135. https://doi.org/10.1128/jb.173.16.5129-5135.1991
- 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. https://doi.org/10.1016/S0168-1605(00)00305-6
- Goulbourne Jr E, Matin M, Zychlinsky E, Matin A. 1986. Mechanism of delta pH maintenance in active and inactive cells of an obligately acidophilic bacterium. J. Bacteriol. 166: 59-65. https://doi.org/10.1128/jb.166.1.59-65.1986
- 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. https://doi.org/10.1128/jb.150.2.582-591.1982
- Lim H-H, Miller C. 2009. Intracellular proton-transfer mutants in a CLC Cl-/H+ exchanger. J. Gen. Physiol. 133: 131-138. https://doi.org/10.1085/jgp.200810112
- Chang YY, Cronan JE. 1999. Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 33: 249-259. https://doi.org/10.1046/j.1365-2958.1999.01456.x
- Jentsch TJ, Friedrich T, Schriever A, Yamada H. 1999. The CLC chloride channel family. Pflugers Archiv. 437: 783-795. https://doi.org/10.1007/s004240050847
- Mindell J, Maduke M. 2001. ClC chloride channels. Genome Biol. 2: Reviews3003.
- Middleton RE, Pheasant DJ, Miller C. 1996. Homodimeric architecture of a CIC-type chloride ion channel. Nature 383: 337-340. https://doi.org/10.1038/383337a0
- Jentsch TJ, Steinmeyer K, Schwarz G. 1990. Primary structure of Torpedomarmorata chloride channel isolated by expression cloning in Xenopus oocytes. Nature 348: 510-514. https://doi.org/10.1038/348510a0
- Fodor AA, Aldrich RW. 2006. Statistical limits to the identification of ion channel domains by sequence similarity. J. Gen. Physiol. 127: 755-766. https://doi.org/10.1085/jgp.200509419
- Casalino M, Prosseda G, Barbagallo M, Iacobino A, Ceccarini P, Latella MC, et al. 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. https://doi.org/10.1016/j.ijmm.2009.10.008
- Feng L, Campbell EB, MacKinnon R. 2012. Molecular mechanism of proton transport in CLC Cl-/H+ exchange transporters. Proc. Natl. Acad. Sci. USA 109: 11699-11704. https://doi.org/10.1073/pnas.1205764109
- Maduke M, Pheasant DJ, Miller C. 1999. High-level expression, functional reconstitution, and quaternary structure of a prokaryotic ClC-type chloride channel. J. Gen. Physiol. 114: 713-722. https://doi.org/10.1085/jgp.114.5.713
- Cakar F, Zingl FG, Moisi M, Reidl J, Schild S. 2018. In vivo repressed genes of Vibrio cholerae reveal inverse requirements of an H+/Cl- transporter along the gastrointestinal passage. Proc. Natl. Acad. Sci. USA 115: E2376-E2385. https://doi.org/10.1073/pnas.1716973115
- Ding Y, Waldor MK. 2003. Deletion of a Vibrio cholerae ClC channel results in acid sensitivity and enhanced intestinal colonization. Infect. Immun. 71: 4197-4200. https://doi.org/10.1128/IAI.71.7.4197-4200.2003
- Middleton RE, Pheasant DJ, Miller C. 1994. Purification, reconstitution, and subunit composition of a voltage-gated chloride channel from Torpedo electroplax. Biochemistry 33: 13189-13198. https://doi.org/10.1021/bi00249a005
- Matulef K, Maduke M. 2007. The CLC 'chloride channel'family: revelations from prokaryotes. Mol. Membr. Biol. 24: 342-350. https://doi.org/10.1080/09687680701413874
- Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R. 2002. X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415: 287-294. https://doi.org/10.1038/415287a
- Miller C. 1982. Open-state substructure of single chloride channels from Torpedo electroplax. Philoso. Trans. R. Soc. Lond. B Biol. Sci. 299: 401-411. https://doi.org/10.1098/rstb.1982.0140
- Pusch M. 2004. Structural insights into chloride and proton-mediated gating of CLC chloride channels. Biochemistry 43: 1135-1144. https://doi.org/10.1021/bi0359776
- Miloshevsky GV, Hassanein A, Jordan PC. 2010. Antiport mechanism for Cl(-)/H(+) in ClC-ec1 from normal-mode analysis. Biophys. J. 98: 999-1008. https://doi.org/10.1016/j.bpj.2009.11.035
- Dutzler R, Campbell EB, MacKinnon R. 2003. Gating the selectivity filter in ClC chloride channels. Science 300: 108-112. https://doi.org/10.1126/science.1082708
- Accardi A, Kolmakova-Partensky L, Williams C, Miller C. 2004. Ionic currents mediated by a prokaryotic homologue of CLC Cl- channels. J. Gen. Physiol. 123: 109-119. https://doi.org/10.1085/jgp.200308935
- Lobet S, Dutzler R. 2006. Ion-binding properties of the ClC chloride selectivity filter. EMBO J. 25: 24-33. https://doi.org/10.1038/sj.emboj.7600909
- Accardi A, Walden M, Nguitragool W, Jayaram H, Williams C, Miller C. 2005. Separate ion pathways in a Cl-/H+ exchanger. J. Gen. Physiol. 126: 563-570. https://doi.org/10.1085/jgp.200509417
- Yin J, Kuang Z, Mahankali U, Beck TL. 2004. Ion transit pathways and gating in ClC chloride channels. Proteins 57: 414-421. https://doi.org/10.1002/prot.20208
- Accardi A, Lobet S, Williams C, Miller C, Dutzler R. 2006. Synergism between halide binding and proton transport in a CLC-type exchanger. J. Mol. Biol. 362: 691-699. https://doi.org/10.1016/j.jmb.2006.07.081