1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 3:

Metabolism

Bacterial Ion Channels

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy article
Choose downloadable ePub or PDF files.
Buy this Chapter
Digital (?) $30.00
  • Authors: Emma L. R. Compton1, and Joseph A. Mindell2
  • Editor: Valley Stewart3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Membrane Transport Biophysics Unit, Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892; 2: Membrane Transport Biophysics Unit, Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892; 3: University of California, Davis, Davis, CA
  • Received 04 June 2009 Accepted 10 August 2009 Published 01 June 2010
  • Address correspondence to Joseph A. Mindell mindellj@ninds.nih.gov
image of Bacterial Ion Channels
    Preview this reference work article:
    Zoom in
    Zoomout

    Bacterial Ion Channels, Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/4/1/3_3_2_module-1.gif /docserver/preview/fulltext/ecosalplus/4/1/3_3_2_module-2.gif
  • Abstract:

    Bacterial ion channels were known, but only in special cases, such as outer membrane porins in and bacterial toxins that form pores in their target (bacterial or mammalian) membranes. The exhaustive coverage provided by a decade of bacterial genome sequencing has revealed that ion channels are actually widespread in bacteria, with homologs of a broad range of mammalian channel proteins coded throughout the bacterial and archaeal kingdoms. This review discusses four groups of bacterial channels: porins, mechano-sensitive (MS) channels, channel-forming toxins, and bacterial homologs of mammalian channels. The outer membrane (OM) of gram-negative bacteria blocks access of essential nutrients; to survive, the cell needs to provide a mechanism for nutrients to penetrate the OM. Porin channels provide this access by forming large, nonspecific aqueous pores in the OM that allow ions and vital nutrients to cross it and enter the periplasm. MS channels act as emergency release valves, allowing solutes to rapidly exit the cytoplasm and to dissipate the large osmotic disparity between the internal and external environments. MS channels are remarkable in that they do this by responding to forces exerted by the membrane itself. Some bacteria produce toxic proteins that form pores in , attacking and killing other organisms by virtue of their pore formation. The review focuses on those bacterial toxins that kill other bacteria, specifically the class of proteins called colicins. Colicins reveal the dangers of channel formation in the plasma membrane, since they kill their targets with exactly that approach.

  • Citation: Compton E, Mindell J. 2010. Bacterial Ion Channels, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.2

Key Concept Ranking

Bacterial Proteins
0.4789189
Fourier Transform Infrared Spectroscopy
0.43236154
Bacterial Toxins
0.40158698
0.4789189

References

1. Nikaido H, Vaara M. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49:1–32.[PubMed]
2. Benz R. 1994. Uptake of solutes through bacterial outer membranes, p 397–424. In Ghuysen J-M and Hakenbeck R (ed), Bacterial Cell Wall, vol. 27. Elsevier, Amsterdam, The Netherlands.
3. Delcour AH. 1997. Function and modulation of bacterial porins: insights from electrophysiology. FEMS Microbiol Lett 151:115–123. [PubMed][CrossRef]
4. Jeanteur D, Lakey JH, Pattus F. 1994. The porin superfamily: diversity and common features, p 363–380. In Ghuysen J-M and Hakenbeck R (ed), Bacterial Cell Wall, vol. 27. Elsevier, Amsterdam, The Netherlands.
5. Koebnik R, Locher KP, Van Gelder P. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253. [PubMed][CrossRef]
6. Nikaido H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656. [PubMed][CrossRef]
7. Pratt LA, Hsing W, Gibson KE, Silhavy TJ. 1996. From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 20:911–917. [PubMed][CrossRef]
8. Schulz GE. 2002. The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565:308–317. [PubMed][CrossRef]
9. Decad GM, Nikaido H. 1976. Outer membrane of gram-negative bacteria. XII. Molecular-sieving function of cell wall. J Bacteriol 128:325–336.[PubMed]
10. Nakae T. 1975. Outer membrane of Salmonella typhimurium: reconstitution of sucrose-permeable membrane vesicles. Biochem Biophys Res Commun 64:1224–1230. [PubMed][CrossRef]
11. Nakae T. 1976. Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J Biol Chem 251:2176–2178.[PubMed]
12. Lutkenhaus JF. 1977. Role of a major outer membrane protein in Escherichia coli. J Bacteriol 131:631–637.[PubMed]
13. Beacham IR, Haas D, Yagil E. 1977. Mutants of Escherichia coli “cryptic” for certain periplasmic enzymes: evidence for an alteration of the outer membrane. J Bacteriol 129:1034–1044.[PubMed]
14. Guillier M, Gottesman S, Storz G. 2006. Modulating the outer membrane with small RNAs. Genes Dev 20:2338–2348. [PubMed][CrossRef]
15. Nikaido H, Rosenberg EY. 1983. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. J Bacteriol 153:241–252.[PubMed]
16. Harder KJ, Nikaido H, Matsuhashi M. 1981. Mutants of Escherichia coli that are resistant to certain beta-lactam compounds lack the ompF porin. Antimicrob Agents Chemother 20:549–552.[PubMed]
17. Nikaido I, Saito C, Mizuno Y, Meguro M, Bono H, Kadomura M, Kono T, Morris GA, Lyons PA, Oshimura M, Hayashizaki Y, Okazaki Y, RIKEN GER Group, GSL Members. 2003. Discovery of imprinted transcripts in the mouse transcriptome using large-scale expression profiling. Genome Res 13:1402–1409. [PubMed][CrossRef]
18. Lamarche MG, Wanner BL, Crépin S, Harel J. 2008. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32:461–473. [PubMed][CrossRef]
19. Benz R, Janko K, Lauger P. 1979. Ionic selectivity of pores formed by the matrix protein (porin) of Escherichia coli. Biochim Biophys Acta 551:238–247.[PubMed]
20. Benz R, Schmid A, Hancock RE. 1985. Ion selectivity of gram-negative bacterial porins. J Bacteriol 162:722–727.[PubMed]
21. Lakey JH, Watts JP, Lea EJ. 1985. Characterisation of channels induced in planar bilayer membranes by detergent solubilised Escherichia coli porins. Biochim Biophys Acta 817:208–216. [PubMed][CrossRef]
22. Berrier C, Coulombe A, Houssin C, Ghazi A. 1992. Fast and slow kinetics of porin channels from Escherichia coli reconstituted into giant liposomes and studied by patch-clamp. FEBS Lett 306:251–256. [PubMed][CrossRef]
23. Delcour AH, Martinac B, Adler J, Kung C. 1989. Voltage-sensitive ion channel of Escherichia coli. J Membr Biol 112:267–275.[PubMed]
24. Dargent B, Hofmann W, Pattus F, Rosenbusch JP. 1986. The selectivity filter of voltage-dependent channels formed by phosphoporin (PhoE protein) from E. coli. EMBO J 5:773–778.[PubMed]
25. Delcour AH. 2003. Solute uptake through general porins. Front Biosci 8:d1055–d1071. [PubMed][CrossRef]
26. delaVega AL, Delcour AH. 1995. Cadaverine induces closing of E. coli porins. EMBO J 14:6058–6065.[PubMed]
27. Samartzidou H, Mehrazin M, Xu Z, Benedik MJ, Delcour AH. 2003. Cadaverine inhibition of porin plays a role in cell survival at acidic pH. J Bacteriol 185:13–19. [PubMed][CrossRef]
28. Inokuchi K, Mutoh N, Matsuyama S, Mizushima S. 1982. Primary structure of the ompF gene that codes for a major outer membrane protein of Escherichia coli K-12. Nucleic Acids Res 10:6957–6968. [PubMed][CrossRef]
29. Mizuno T, Chou MY, Inouye M. 1983. A comparative study on the genes for three porins of the Escherichia coli outer membrane. DNA sequence of the osmoregulated ompC gene. J Biol Chem 258:6932–6940.[PubMed]
30. Overbeeke N, Bergmans H, van Mansfeld F, Lugtenberg B. 1983. Complete nucleotide sequence of phoE, the structural gene for the phosphate limitation inducible outer membrane pore protein of Escherichia coli K12. J Mol Biol 163:513–532. [PubMed][CrossRef]
31. Rosenbusch JP. 1974. Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulfate binding. J Biol Chem 249:8019–8029.[PubMed]
32. Weiss MS, Kreusch A, Schiltz E, Nestel U, Welte W, Weckesser J, Schulz GE. 1991. The structure of porin from Rhodobacter capsulatus at 1.8 Å resolution. FEBS Lett 280:379–382. [PubMed][CrossRef]
33. Weiss MS, Schulz GE. 1992. Structure of porin refined at 1.8 Å resolution. J Mol Biol 227:493–509. [PubMed][CrossRef]
34. Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP. 1992. Crystal structures explain functional properties of two E. coli porins. Nature 358:727–733. [PubMed][CrossRef]
35. Schulz GE. 2000. beta-Barrel membrane proteins. Curr Opin Struct Biol 10:443–447. [PubMed][CrossRef]
36. Cowan S, Schirmer T. 1994. Structures of non-specific diffusion pores in Escherichia coli, p 353–362. In Ghuysen J-M and Hakenbeck R (ed), Bacterial Cell Wall, vol. 27. Elsevier, Amsterdam, The Netherlands.
37. Yamashita E, Zhalnina MV, Zakharov SD, Sharma O, Cramer WA. 2008. Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J 27:2171–2180. [PubMed][CrossRef]
38. Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC. 1998. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226. [PubMed][CrossRef]
39. Wang W, Black SS, Edwards MD, Miller S, Morrison EL, Bartlett W, Dong C, Naismith JH, Booth IR. 2008. The structure of an open form of an E. coli mechanosensitive channel at 3.45 Å resolution. Science 321:1179–1183. [PubMed][CrossRef]
40. Corry B, Martinac B. 2008. Bacterial mechanosensitive channels: experiment and theory. Biochim Biophys Acta 1778:1859–1870. [PubMed][CrossRef]
41. Hamill OP, Martinac B. 2001. Molecular basis of mechanotransduction in living cells. Physiol Rev 81:685–740.[PubMed]
42. Martinac B. 2004. Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 117(pt. 12):2449–2460. [PubMed][CrossRef]
43. Martinac B. 2005. Structural plasticity in MS channels. Nat Struct Mol Biol 12:104–105. [PubMed][CrossRef]
44. Oakley AJ, Martinac B, Wilce MC. 1999. Structure and function of the bacterial mechanosensitive channel of large conductance. Protein Sci 8:1915–1921. [PubMed][CrossRef]
45. Martinac B, Buechner M, Delcour AH, Adler J, Kung C. 1987. Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci USA 84:2297–2301. [PubMed][CrossRef]
46. Berrier C, Besnard M, Ajouz B, Coulombe A, Ghazi A. 1996. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J Membr Biol 151:175–187. [PubMed][CrossRef]
47. Levina N, Tötemeyer S, Stokes NR, Louis P, Jones MA, Booth IR. 1999. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18:1730–1737. [PubMed][CrossRef]
48. McLaggan D, Jones MA, Gouesbet G, Levina N, Lindey S, Epstein W, Booth IR. 2002. Analysis of the kefA2 mutation suggests that KefA is a cation-specific channel involved in osmotic adaptation in Escherichia coli. Mol Microbiol 43:521–536.[PubMed]
49. Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C. 1994. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368:265–268. [PubMed][CrossRef]
50. Yang XC, Sachs F. 1989. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243(pt. 1):1068–1071. [PubMed][CrossRef]
51. Berrier C, Coulombe A, Szabo I, Zoratti M, Ghazi A. 1992. Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. Eur J Biochem 206:559–565. [PubMed][CrossRef]
52. Blount P, Sukharev SI, Moe PC, Schroeder MJ, Guy HR, Kung C. 1996. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J 15:4798–4805.[PubMed]
53. Stokes NR, Murray HD, Subramaniam C, Gourse RL, Louis P, Bartlett W, Miller S, Booth IR. 2003. A role for mechanosensitive channels in survival of stationary phase: regulation of channel expression by RpoS. Proc Natl Acad Sci USA 100:15959–15964. [PubMed][CrossRef]
54. Vasquez V, Sotomayor M, Cortes DM, Roux B, Schulten K, Perozo E. 2008. Three-dimensional architecture of membrane-embedded MscS in the closed conformation. J Mol Biol 378:55–70. [PubMed][CrossRef]
55. Martinac B, Adler J, Kung C. 1990. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261–263. [PubMed][CrossRef]
56. Perozo E, Kloda A, Cortes DM, Martinac B. 2002. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9:696–703. [PubMed][CrossRef]
57. Li Y, Moe PC, Chandrasekaran S, Booth IR, Blount P. 2002. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J 21:5323–5330. [PubMed][CrossRef]
58. Sukharev SI, Martinac B, Arshavsky VY, Kung C. 1993. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J 65:177–183. [PubMed][CrossRef]
59. Bass RB, Strop P, Barclay M, Rees DC. 2002. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298:1582–1587. [PubMed][CrossRef]
60. Kloda A, Ghazi A, Martinac B. 2006. C-terminal charged cluster of MscL, RKKEE, functions as a pH sensor. Biophys J 90:1992–1998. [PubMed][CrossRef]
61. Vasquez V, Sotomayor M, Cordero-Morales J, Schulten K, Perozo E. 2008. A structural mechanism for MscS gating in lipid bilayers. Science 321:1210–1214. [PubMed][CrossRef]
62. Cruickshank CC, Minchin RF, Le Dain AC, Martinac B. 1997. Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys J 73:1925–1931. [PubMed][CrossRef]
63. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B. 2002. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 418:942–948. [PubMed][CrossRef]
64. Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubès R, Postle K, Riley M, Slatin S, Cavard D. 2007. Colicin biology. Microbiol Mol Biol Rev 71:158–229. [PubMed][CrossRef]
65. Jacob F, Siminovitch L, Wollman E. 1952. [Biosynthesis of a colicin and its mode of action.]. Ann Inst Pasteur (Paris) 83:295–315.[PubMed]
66. Luria SE. 1964. On the mechanisms of action of colicins. Ann Inst Pasteur (Paris) 107(Suppl.):67–73.[PubMed]
67. Fields KL, Luria SE. 1969. Effects of colicins E1 and K on transport systems. J Bacteriol 97:57–63.[PubMed]
68. Fields KL, Luria SE. 1969. Effects of colicins E1 and K on cellular metabolism. J Bacteriol 97:64–77.[PubMed]
69. Wendt L. 1970. Mechanism of colicin action: early events. J Bacteriol 104:1236–1241.[PubMed]
70. Schein SJ, Kagan BL, Finkelstein A. 1978. Colicin K acts by forming voltage-dependent channels in phospholipid bilayer membranes. Nature 276:159–163. [PubMed][CrossRef]
71. Elkins P, Bunker A, Cramer WA, Stauffacher CV. 1997. A mechanism for toxin insertion into membranes is suggested by the crystal structure of the channel-forming domain of colicin E1. Structure 5:443–458. [PubMed][CrossRef]
72. Parker MW, Pattus F, Tucker AD, Tsernoglou D. 1989. Structure of the membrane-pore-forming fragment of colicin A. Nature 337:93–96. [PubMed][CrossRef]
73. Wiener M, Freymann D, Ghosh P, Stroud RM. 1997. Crystal structure of colicin Ia. Nature 385:461–464. [PubMed][CrossRef]
74. Merrill AR, Cohen FS, Cramer WA. 1990. On the nature of the structural change of the colicin E1 channel peptide necessary for its translocation-competent state. Biochemistry 29:5829–5836. [PubMed][CrossRef]
75. van der Goot FG, González-Mañas JM, Lakey JH, Pattus F. 1991. A ‘molten-globule’ membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354:408–410. [PubMed][CrossRef]
76. Rath P, Bousché O, Merrill AR, Cramer WA, Rothschild KJ. 1991. Fourier transform infrared evidence for a predominantly alpha-helical structure of the membrane bound channel forming COOH-terminal peptide of colicin E1. Biophys J 59:516–522. [PubMed][CrossRef]
77. Song HY, Cohen FS, Cramer WA. 1991. Membrane topography of ColE1 gene products: the hydrophobic anchor of the colicin E1 channel is a helical hairpin. J Bacteriol 173:2927–2934.[PubMed]
78. Kienker PK, Qiu X, Slatin SL, Finkelstein A, Jakes KS. 1997. Transmembrane insertion of the colicin Ia hydrophobic hairpin. J Membr Biol 157:27–37. [PubMed][CrossRef]
79. Slatin SL, Raymond L, Finkelstein A. 1986. Gating of a voltage-dependent channel (colicin E1) in planar lipid bilayers: the role of protein translocation. J Membr Biol 92:247–254. [PubMed][CrossRef]
80. Abrams CK, Jakes KS, Finkelstein A, Slatin SL. 1991. Identification of a translocated gating charge in a voltage-dependent channel. Colicin E1 channels in planar phospholipid bilayer membranes. J Gen Physiol 98:77–93. [PubMed][CrossRef]
81. Qiu XQ, Jakes KS, Kienker PK, Finkelstein A, Slatin SL. 1996. Major transmembrane movement associated with colicin Ia channel gating. J Gen Physiol 107:313–328. [PubMed][CrossRef]
82. Slatin SL, Qiu XQ, Jakes KS, Finkelstein A. 1994. Identification of a translocated protein segment in a voltage-dependent channel. Nature 371:158–161. [PubMed][CrossRef]
83. Jakes K, Kienker PK, Slatin SL, Finkelstein A. 1998. Translocation of inserted foreign epitopes by a channel-forming protein. Proc Natl Acad Sci USA 95:4321–4326. [CrossRef]
84. Kienker PK, Jakes KS, Blaustein RO, Miller C, Finkelstein A. 2003. Sizing the protein translocation pathway of colicin Ia channels. J Gen Physiol 122:161–176. [PubMed][CrossRef]
85. Slatin SL, Nardi A, Jakes KS, Baty D, Duché D. 2002. Translocation of a functional protein by a voltage-dependent ion channel. Proc Natl Acad Sci USA 99:1286–1291. [PubMed][CrossRef]
86. Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY. 1987. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237:749–753. [PubMed][CrossRef]
87. Heginbotham L, Lu Z, Abramson T, MacKinnon R. 1994. Mutations in the K+ channel signature sequence. Biophys J 66:1061–1067. [PubMed][CrossRef]
88. Milkman R. 1994. An Escherichia coli homologue of eukaryotic potassium channel proteins. Proc Natl Acad Sci USA 91:3510–3514. [PubMed][CrossRef]
89. Schrempf H, Schmidt O, Kümmerlen R, Hinnah S, Müller D, Betzler M, Steinkamp T, Wagner R. 1995. A prokaryotic potassium ion channel with two predicted transmembrane segments from Streptomyces lividans. EMBO J 14:5170–5178.[PubMed]
90. Heginbotham L, Kolmakova-Partensky L, Miller C. 1998. Functional reconstitution of a prokaryotic K+ channel. J Gen Physiol 111:741–749. [PubMed][CrossRef]
91. Heginbotham L, LeMasurier M, Kolmakova-Partensky L, Miller C. 1999. Single streptomyces lividans K(+) channels: functional asymmetries and sidedness of proton activation. J Gen Physiol 114:551–560. [PubMed][CrossRef]
92. Heginbotham L, Odessey E, Miller C. 1997. Tetrameric stoichiometry of a prokaryotic K+ channel. Biochemistry 36:10335–10342. [PubMed][CrossRef]
93. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77. [PubMed][CrossRef]
94. Jiang Y, MacKinnon R. 2000. The barium site in a potassium channel by x-ray crystallography. J Gen Physiol 115:269–272. [PubMed][CrossRef]
95. Morais-Cabral JH, Zhou Y, MacKinnon R. 2001. Energetic optimization of ion conduction rate by the K+ selectivity filter. Nature 414:37–42. [PubMed][CrossRef]
96. Zhou Y, MacKinnon R. 2003. The occupancy of ions in the K+ selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J Mol Biol 333:965–975. [PubMed][CrossRef]
97. Zhou Y, MacKinnon R. 2004. Ion binding affinity in the cavity of the KcsA potassium channel. Biochemistry 43:4978–4982. [PubMed][CrossRef]
98. Zhou M, MacKinnon R. 2004. A mutant KcsA K(+) channel with altered conduction properties and selectivity filter ion distribution. J Mol Biol 338:839–846. [PubMed][CrossRef]
99. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R. 2001. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 Å resolution. Nature 414:43–48. [PubMed][CrossRef]
100. Zhou M, Morais-Cabral JH, Mann S, MacKinnon R. 2001. Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors. Nature 411:657–661. [PubMed][CrossRef]
101. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:515–522. [PubMed][CrossRef]
102. Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R. 2003. X-ray structure of a voltage-dependent K+ channel. Nature 423:33–41. [PubMed][CrossRef]
103. Alam A, Jiang Y. 2009. High-resolution structure of the open NaK channel. Nat Struct Mol Biol 16:30–34. [PubMed][CrossRef]
104. Clayton GM, Altieri S, Heginbotham L, Unger VM, Morais-Cabral JH. 2008. Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel. Proc Natl Acad Sci USA 105:1511–1515. [PubMed][CrossRef]
105. Schultz SG, Solomon AK. 1961. Cation transport in Escherichia coli. I. Intracellular Na and K concentrations and net cation movement. J Gen Physiol 45:355–369. [PubMed][CrossRef]
106. Kuo MM, Haynes WJ, Loukin SH, Kung C, Saimi Y. 2005. Prokaryotic K(+) channels: from crystal structures to diversity. FEMS Microbiol Rev 29:961–985. [PubMed][CrossRef]
107. Kuo MM, Saimi Y, Kung C. 2003. Gain-of-function mutations indicate that Escherichia coli Kch forms a functional K+ conduit in vivo. EMBO J 22:4049–4058. [PubMed][CrossRef]
108. Stingl K, Brandt S, Uhlemann EM, Schmid R, Altendorf K, Zeilinger C, Ecobichon C, Labigne A, Bakker EP, de Reuse H. 2007. Channel-mediated potassium uptake in Helicobacter pylori is essential for gastric colonization. EMBO J 26:232–241. [PubMed][CrossRef]
109. 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. [PubMed][CrossRef]
110. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R. 2002. X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature 415:287–294. [PubMed][CrossRef]
111. Mindell JA, Maduke M, Miller C, Grigorieff N. 2001. Projection structure of a ClC-type chloride channel at 6.5 Å resolution. Nature 409:219–223. [PubMed][CrossRef]
112. 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. [PubMed][CrossRef]
113. Accardi A, Miller C. 2004. Secondary active transport mediated by a prokaryotic homologue of ClC Cl-channels. Nature 427:803–807. [PubMed][CrossRef]
114. Picollo A, Pusch M. 2005. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436:420–423. [PubMed][CrossRef]
115. Scheel O, Zdebik AA, Lourdel S, Jentsch TJ. 2005. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436:424–427. [PubMed][CrossRef]
116. 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. [PubMed][CrossRef]
117. 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. [PubMed][CrossRef]
118. Accardi A, et al. 2005. The intracellular gate of ClC-ec1. Biophys Soc Abstr
119. Bell SP, Curran PK, Choi S, Mindell JA. 2006. Site-directed fluorescence studies of a prokaryotic ClC antiporter. Biochemistry 45:6773–6782. [PubMed][CrossRef]
120. Matulef K, Maduke M. 2005. Side-dependent inhibition of a prokaryotic ClC by DIDS. Biophys J 89:1721–1730. [PubMed][CrossRef]
121. Nguitragool W, Miller C. 2006. Uncoupling of a CLC Cl-/H+ exchange transporter by polyatomic anions. J Mol Biol 362:682–690. [PubMed][CrossRef]
122. Nguitragool W, Miller C. 2007. Inaugural Article: CLC Cl /H+ transporters constrained by covalent cross-linking. Proc Natl Acad Sci USA 104:20659–20665. [PubMed][CrossRef]
123. Walden M, Accardi A, Wu F, Xu C, Williams C, Miller C. 2007. Uncoupling and turnover in a Cl/H+ exchange transporter. J Gen Physiol 129:317–329. [PubMed][CrossRef]
124. Iyer R, Iverson TM, Accardi A, Miller C. 2002. A biological role for prokaryotic ClC chloride channels. Nature 419:715–718. [PubMed][CrossRef]
125. Dutzler R, Campbell EB, MacKinnon R. 2003. Gating the selectivity filter in ClC chloride channels. Science 300:108–112. [PubMed][CrossRef]
126. Hilf RJ, Dutzler R. 2008. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452:375–379. [PubMed][CrossRef]
127. Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE. 2001. A prokaryotic voltage-gated sodium channel. Science 294:2372–2375. [PubMed][CrossRef]
128. Shi N, Ye S, Alam A, Chen L, Jiang Y. 2006. Atomic structure of a Na+- and K+-conducting channel. Nature 440:570–574. [PubMed][CrossRef]
129. Chiu PL, Pagel MD, Evans J, Chou HT, Zeng X, Gipson B, Stahlberg H, Nimigean CM. 2007. The structure of the prokaryotic cyclic nucleotide-modulated potassium channel MloK1 at 16 Å resolution. Structure 15:1053–1064. [PubMed][CrossRef]
130. Nimigean CM, Pagel MD. 2007. Ligand binding and activation in a prokaryotic cyclic nucleotide-modulated channel. J Mol Biol 371:1325–1337. [PubMed][CrossRef]
131. Nimigean CM, Shane T, Miller C. 2004. A cyclic nucleotide modulated prokaryotic K+ channel. J Gen Physiol 124:203–210. [PubMed][CrossRef]
132. Chen GQ, Cui C, Mayer ML, Gouaux E. 1999. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402:817–821. [PubMed][CrossRef]
133. Tasneem A, Iyer LM, Jakobsson E, Aravind L. 2005. Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol 6:R4. [PubMed][CrossRef]
134. Bocquet N, Prado de Carvalho L, Cartaud J, Neyton J, Le Poupon C, Taly A, Grutter T, Changeux JP, Corringer PJ. 2007. A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 445:116–119. [PubMed][CrossRef]
ecosalplus.3.3.2.citations
ecosalplus/4/1
content/journal/ecosalplus/10.1128/ecosalplus.3.3.2
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/ecosalplus/10.1128/ecosalplus.3.3.2
2010-06-01
2017-12-14

Abstract:

Bacterial ion channels were known, but only in special cases, such as outer membrane porins in and bacterial toxins that form pores in their target (bacterial or mammalian) membranes. The exhaustive coverage provided by a decade of bacterial genome sequencing has revealed that ion channels are actually widespread in bacteria, with homologs of a broad range of mammalian channel proteins coded throughout the bacterial and archaeal kingdoms. This review discusses four groups of bacterial channels: porins, mechano-sensitive (MS) channels, channel-forming toxins, and bacterial homologs of mammalian channels. The outer membrane (OM) of gram-negative bacteria blocks access of essential nutrients; to survive, the cell needs to provide a mechanism for nutrients to penetrate the OM. Porin channels provide this access by forming large, nonspecific aqueous pores in the OM that allow ions and vital nutrients to cross it and enter the periplasm. MS channels act as emergency release valves, allowing solutes to rapidly exit the cytoplasm and to dissipate the large osmotic disparity between the internal and external environments. MS channels are remarkable in that they do this by responding to forces exerted by the membrane itself. Some bacteria produce toxic proteins that form pores in , attacking and killing other organisms by virtue of their pore formation. The review focuses on those bacterial toxins that kill other bacteria, specifically the class of proteins called colicins. Colicins reveal the dangers of channel formation in the plasma membrane, since they kill their targets with exactly that approach.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed

Figures

Image of Figure 1
Figure 1

Views along (left) and perpendicular (right) to the plane of the lipid bilayer are shown, colored by subunit. (a) OmpF porin (PDB ID code 2zfg) ( 37 ) is shown. Loop L2 (red) stabilizes the trimer and loop L3 (orange) constricts the pore and contributes to determining ion selectivity. (b) MscL (PDB ID code 2oar) ( 38 ) is shown in the closed state. Residues that occlude the permeation pathway are shown as blue and red space-filling representations. (c) MscS (PDB ID code 2vv5) ( 39 ) shown in the open state. Residues lining the narrow part of the transmembrane pore are shown as red and blue space-filling representations.

Citation: Compton E, Mindell J. 2010. Bacterial Ion Channels, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

(a) KcsA (PDB ID code 1k4c) ( 99 ). (b) MethK (PDB ID code 1lnq) ( 101 ). (c) NaK (PDB ID code 3e86) ( 103 ). (d) MlotK1 (PDB ID code 3beh) ( 104 ). All structures are shown parallel to the plane of the membrane, colored by subunit. In panels a, c, and d, individual ions are shown in the channel pores.

Citation: Compton E, Mindell J. 2010. Bacterial Ion Channels, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

(a) ClC-ec1 (PDB ID code 1ots) ( 125 ). (b) pGLIC (PDB ID code 2VL0) ( 126 ). Structures are viewed parallel to the plane of the membrane, colored by subunit. Bound Cl ions are shown in red in ClC-ec1 and possible “gate” residues are shown in blue and red for pGLIC.

Citation: Compton E, Mindell J. 2010. Bacterial Ion Channels, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.2
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error