Cloning and functional expression of an MscL ortholog from Rhizobium etli: Characterization of a mechanosensitive channel

Journal of Membrane Biology

Volumn 234, Issue 1, 2010, Pages 13-27

  Balleza, Daniel ^a,b,d   Gómez Lagunas, Froylan ^b   Quinto, Carmen ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Gating modulation; Mechanosensitive channel; Rhizobium etli

Indexed keywords

ARACHIDONIC ACID;

ARTICLE; BACTERIAL STRAIN; BACTERIOLYSIS; BACTERIUM MUTANT; CELL MUTANT; CLONING; ESCHERICHIA COLI; HABITAT; HYPOOSMOTIC STRESS; IN VIVO STUDY; MEMBRANE CHANNEL; MICROORGANISM; ORTHOLOGY; OSMOSIS; PARALOGY; PATCH CLAMP; PH; PROTEIN CONFORMATION; RHIZOBIUM ETLI; RHIZOSPHERE; SPHEROPLAST;

AMINO ACID SEQUENCE; ARACHIDONIC ACID; BACTERIAL PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GADOLINIUM; ION CHANNEL GATING; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; MOLECULAR SEQUENCE DATA; OSMOTIC PRESSURE; PATCH-CLAMP TECHNIQUES; RHIZOBIUM ETLI; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI; RHIZOBIALES; RHIZOBIUM ETLI;

EID: 77949424698     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-010-9235-8     Document Type: Article

References (79)

1. Anishkin A, Chiang CS, Sukharev S (2005) Gain-of-function mutations reveal expanded intermediate states and a sequential action of two gates in MscL. J Gen Physiol 125:155-170
2. Balleza D, Gómez-Lagunas F (2009) Conserved motifs in mechanosensitive channels MscL and MscS. Eur Biophys J 38:1013-1027
3. Batiza AF, Kuo MM-C, Yoshimura K, Kung C (2002) Gating the bacterial mechanosensitive channel MscL in vivo. Proc Natl Acad Sci USA 99:5643-5648
4. 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
5. Blount P, Sukharev SI, Moe PC, Schroeder MJ, Guy HR, Kung C (1996a) Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J 15:4798-4805
6. Blount P, Sukharev SI, Schroeder MJ, Nagle SK, Kung C (1996b) Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc Natl Acad Sci USA 93:11652-11657
7. Blount P, Iscla I, Moe PC, Li Y (2007) MscL: the bacterial mechanosensitive channel of large conductance. In: Hamill OP (ed) Current topics in membranes. Academic Press, New York, pp 201-233
8. Boncompagni E, Osteras M, Poggi MC, le Rudulier D (1999) Occurrence of choline and glycine betaine uptake and metabolism in the family Rhizobiaceae and their roles in osmoprotection. Appl Environ Microbiol 65:2072-2077
9. Booth IR, Edwards MD, Black S, Schumann U, Bartlett W, Rasmussen T, Rasmussen A, Miller S (2007) Physiological analysis of bacterial mechanosensitive channels. Methods Enzymol 428:47-61
10. Boscari A, Van de Sype G, Le Rudulier D, Mandon K (2006) Overexpression of BetS, a Sinorhizobium meliloti high-affinity betaine transporter, in bacteroids from Medicago sativa nodules sustains nitrogen fixation during early salt stress adaptation. Mol Plant Microbe Interact 19:896-903
11. Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SG (2004) Computational inferences of scenarios for a-proteobacterial genome evolution. Proc Natl Acad Sci USA 101:9722-9727
12. Brash AR (2001) Arachidonic acid as a bioactive molecule. J Clin Invest 107:1339-1345
13. Breedveld MW, Miller KJ (1994) Cyclic b-glucans of members of the family Rhizobiaceae. Microbiol Rev 58:145-161
14. Caldwell RA, Clemo HF, Baumgarten CM (1998) Using gadolinium to identify stretch-activated channels: technical considerations. Am J Physiol 275:C619-C621
15. Carrillo-Tripp M, Feller SE (2005) Evidence for a mechanism by which x-3 polyunsaturated lipids may affect membrane protein function. Biochemistry 44:10164-10169
16. Chevalier G, Delamarche C (1992) Protein IIIa of Rhizobium leguminosarum is probably a porin. Biochimie 74:1121-1123
17. Chiang CS, Anishkin A, Sukharev S (2004) Gating of the large mechanosensitive channel in situ: estimation of the spatial scale of the transition from channel population responses. Biophys J 86:2846-2861
18. Chiu P-L, Pagel MD, Evans J, Chou H-T, 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
19. 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
20. Dedman A, Sharif-Naeini R, Folgering JH, Duprat F, Patel A, Honoré E (2009) The mechano-gated K(2P) channel TREK-1. Eur Biophys J 38:293-303
21. Epstein W, Kim BS (1971) Potassium transport loci in Escherichia coli K-12. J Bacteriol 108:639-644
22. Ermakov YA, Averbakh AZ, Yusipovich AI, Sukharev SI (2001) Dipole potentials indicate restructuring of the membrane interface induced by gadolinium and beryllium ions. Biophys J 80:1851-1862
23. Evans CH (1990) Biochemistry of lanthanides. Plenum, New York
24. Farge E, Devaux PF (1992) Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys J 61:347-357
25. Folgering JH, Kuiper JM, de Vries AH, Engberts JBFN, Poolman B (2004) Lipid-mediated light activation of a mechanosensitive channel of large conductance. Langmuir 20:6985-6987
26. Folgering JH, Moe PC, Schuurman-Wolters GK, Blount P, Poolman B (2005) Lactococcus lactis uses MscL as its principal mechanosensitive channel. J Biol Chem 280:8784-8789
27. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the Rhizobium-legume symbiosis. Eur J Biochem 270:1365-1380
28. Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413-441
29. Gill CO (1975) Effect of growth temperature on the lipids of Pseudomonas fluorescens. J Gen Microbiol 89:293-298
30. Gonzalez V, Santamar?́a RI, Bustos P, Hernández- González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ram?́rez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834-3839
31. Guillén-Navarro K, Ara?́za G, Garc?́a-de los Santos A, Mora Y, Dunn MF (2005) The Rhizobium etli bioMNY operon is involved in biotin transport. FEMS Microbiol Lett 250:209-219
32. Hamill OP, McBride DW (1996) The pharmacology of mechanogated membrane ion channels. Pharmacol Rev 48:231-252
33. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100
34. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580
35. Häse CC, Le Dain AC, Martinac B (1995) Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 270:18329-18334
36. Häse CC, Le Dain AC, Martinac B (1997) Molecular dissection of the large mechanosensitive ion channel (MscL) of E. coli: mutants with altered channel gating and pressure sensitivity. J Membr Biol 157:17-25
37. Kloda A, Martinac B (2001) Mechanosensitive channel of thermoplasma, the cell wall-less Archaea: cloning and molecular characterization. Cell Biochem Biophys 34:321-347
38. Kloda A, Martinac B (2002) Common evolutionary origins of mechanosensitive ion channels in Archaea, bacteria and cellwalled Eukarya. Archaea 1:35-44
39. Kloda A, Ghazi A, Martinac B (2006) C-terminal charged cluster of MscL, RKKEE, functions as a pH sensor. Biophys J 90:1992-1998
40. Kloda A, Lua L, Hall R, Adams DJ, Martinac B (2007) Liposome reconstitution and modulation of recombinant N-methyl-Daspartate receptor channels by membrane stretch. Proc Natl Acad Sci USA 104:1540-1545
41. Krehenbrink M, Downie JA (2008) Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae. BMC Genomics 9:1-19
42. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologistcentric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299-306
43. 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
44. Liu Z, Gandhi CS, Rees DC (2009) Structure of a tetrameric MscL in an expanded intermediate state. Nature 461:120-124
45. López-Lara IM, Sohlenkamp C, Geiger O (2003) Membrane lipids in plant-associated bacteria: their biosyntheses and possible functions. Mol Plant-Microbe Interact 16:567-579
46. + channels TREK-1 and TRAAK. J Biol Chem 275:10128-10133
47. 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
48. Martinac B, Adler J, Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261-263
49. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149:114-122
50. Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103:5230-5235
51. Meves H (1994) Modulation of ion channels by arachidonic acid. Prog Neurobiol 43:175-186
52. Meves H (2008) Arachidonic acid and ion channels: an update. Br J Pharmacol 155:4-16
53. Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101-136
54. Moe PC, Blount P, Kung C (1998) Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol Microbiol 28:583-592
55. Moe PC, Levin G, Blount P (2000) Correlating a protein structure with function of a bacterial mechanosensitive channel. J Biol Chem 275:31121-31127
56. Müller J, Wiemken A, Boller T (2001) Redifferentiation of bacteria isolated from Lotus japonicus root nodules colonized by Rhizobium sp. NGR234. J Exp Bot 52:2181-2186
57. Noel KD, Sanchez A, Fernandez L, Leemans J, Cevallos MA (1984) Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J Bacteriol 158:148-155
58. + channels. Curr Opin Cell Biol 13:422-427
59. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B (2002a) Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 418:942-948
60. Perozo E, Kloda A, Cortes DM, Martinac B (2002b) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9:696-703
61. Petrov E, Martinac B (2007) Modulation of channel activity and gadolinium block of MscL by static magnetic fields. Eur Biophys J 36:95-105
62. Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459:379-385
63. Pivetti CD, Yen MR, Miller S, Busch W, Tseng YH, Booth IR, Saier MH Jr (2003) Two families of mechanosensitive channel proteins. Microbiol Mol Biol Rev 67:66-85
64. Rojas-Jiménez K, Sohlenkamp C, Geiger O, Mart?́nez-Romero E, Werner D, Vinuesa P (2005) A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant Microbe Interact 18:1175-1185
65. Sheetz MP, Singer SJ (1974) Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci USA 71:4457-4461
66. Shukla SD, Green C, Turner JM (1980) Phosphatidylethanolamine distribution and fluidity in outer and inner membranes of the gram-negative bacterium Erwinia carotovora. Biochem J 188:131-135
67. 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
68. Sukharev SI, Sigurdson WJ, Kung C, Sachs F (1999) Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J Gen Physiol 113:525-540
69. Sukharev SI, Anishkin A, Chiang C-S, Betanzos M, Guy HR (2005) MscL, a bacterial mechanosensitive channel. In: Kubalski A, Martinac B (eds) Bacterial ion channels and their eukaryotic homologs. ASM Press, Washington
70. Sutton WD, Jepsen NM, Shaw BD (1977) Changes in the number, viability, and amino-acid-incorporating activity of Rhizobium bacteroids during lupin nodule development. Plant Physiol 59:741-744
71. Sutton JM, Lea EJ, Downie JA (1994) The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91:9990-9994
72. Szabó I, Petronilli V, Zoratti M (1992) A patch-clamp study of Bacillus subtilis. Biochim Biophys Acta 1112:29-38
73. Szabó I, Petronilli V, Zoratti M (1993) A patch-clamp investigation of the Streptococcus faecalis cell membrane. J Membr Biol 131:203-218
74. + transporter is down-regulated early during bacteroid differentiation. Mol Plant-Microbe Interact 11:188-198
75. Taté R, Ferraioli S, Filosa S, Cermola M, Riccio A, Iaccarino M, Patriarca EJ (2004) Glutamine utilization by Rhizobium etli. Mol Plant-Microbe Interact 17:720-728
76. Tsien HC, Cain PS, Schmidt EL (1977) Viability of Rhizobium bacteroids. Appl Environ Microbiol 34:854-856
77. Wiggins P, Phillips R (2004) Analytic models for mechanotransduction: gating a mechanosensitive channel. Proc Natl Acad Sci USA 101:4071-4076
78. Wiggins P, Phillips R (2005) Membrane-protein interactions in mechanosensitive channels. Biophys J 88:880-902
79. Yurgel SN, Kahn ML (2004) Dicarboxylate transport by rhizobia. FEMS Microbiol Rev 28:489-501