Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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ClC Chloride Channels in Gram-Negative Bacteria and Its Role in the Acid Resistance Systems

  • Minjeong Kim (Department of Life Sciences, College of Life Sciences and Biotechnology, Korea University) ;
  • Nakjun Choi (Department of Life Sciences, College of Life Sciences and Biotechnology, Korea University) ;
  • Eunna Choi (Department of Life Sciences, College of Life Sciences and Biotechnology, Korea University) ;
  • Eun-Jin Lee (Department of Life Sciences, College of Life Sciences and Biotechnology, Korea University)
  • Received : 2023.03.09
  • Accepted : 2023.04.06
  • Published : 2023.07.28
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Abstract

Pathogenic bacteria that colonize the human intestinal tract have evolved strategies to overcome acidic conditions when they pass through the gastrointestinal tract. Amino acid-mediated acid resistance systems are effective survival strategies in a stomach that is full of amino acid substrate. The amino acid antiporter, amino acid decarboxylase, and ClC chloride antiporter are all engaged in these systems, and each one plays a role in protecting against or adapting to the acidic environment. The ClC chloride antiporter, a member of the ClC channel family, eliminates negatively charged intracellular chloride ions to avoid inner membrane hyperpolarization as an electrical shunt of the acid resistance system. In this review, we will discuss the structure and function of the prokaryotic ClC chloride antiporter of amino acid-mediated acid resistance system.

Keywords

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

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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.
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. Mindell J, Maduke M. 2001. ClC chloride channels. Genome Biol. 2: Reviews3003.
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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