A sodium ion-dependent A1AO ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus

FEBS Journal

Volumn 274, Issue 15, 2007, Pages 3928-3938

  Pisa, Kim Y ^a   Huber, Harald ^b   Thomm, Michael ^b   Müller, Volker ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

A1AO ATP synthase; Archaea; Hyperthermophile; Na +; Pyrococcus

Indexed keywords

DETERGENT; DICYCLOHEXYLCARBODIIMIDE; DIETHYLSTILBESTROL; DIETHYLSTILBESTROL DERIVATIVE; HYDROGEN; LITHIUM; OLIGOMER; POTASSIUM ION; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SODIUM ION;

ARTICLE; BINDING SITE; CHROMATOGRAPHY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME ISOLATION; HYDROLYSIS; HYPERTHERMOPHILIC ARCHAEON; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PYROCOCCUS FURIOSUS; SOLUBILIZATION; TEMPERATURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CARBODIIMIDES; CATALYSIS; CATIONS; CELL MEMBRANE; CONSERVED SEQUENCE; CYCLOHEXANES; ENZYME INHIBITORS; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS; PYROCOCCUS FURIOSUS; SEQUENCE ALIGNMENT; SODIUM; SOLUBILITY; TEMPERATURE;

ARCHAEA; PYROCOCCUS; PYROCOCCUS FURIOSUS;

EID: 34447629933     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05925.x     Document Type: Article

References (79)

1. Hilario E Gogarten JP (1998) The prokaryote-to-eucaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J Mol Evol 46, 703 715.
2. Gogarten JP Taiz L (1992) Evolution of proton pumping ATPases - rooting the tree of life. Photosynth Res 33, 137 146.
3. Nelson N (1992) Evolution of organellar proton-ATPases. Biochim Biophys Acta 1100, 109 124.
4. Cross RL Müller V (2004) The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP stoichiometry. FEBS Lett 576, 1 4.
5. Pedersen PL, Ko YH Hong S (2000) ATP synthases in the year 2000: evolving views about the structures of these remarkable enzyme complexes. J Bioenerg Biomembr 32, 325 332.
6. Domgall I, Venzke D, Lüttge U, Ratajczak R Böttcher B (2002) Three-dimensional map of a plant V-ATPase based on electron microscopy. J Biol Chem 277, 13115 13121.
7. Karrasch S Walker JE (1999) Novel features in the structure of bovine ATP synthase. J Mol Biol 290, 379 384.
8. Böttcher B Gräber P (2000) The structure of the H+-ATP synthase from chloroplasts and its subcomplexes as revealed by electron microscopy. Biochim Biophys Acta 1458, 404 416.
9. Wilkens S Capaldi RA (1998) Electron microscopic evidence of two stalks linking the F1 and FO parts of the Escherichia coli ATP synthase. Biochim Biophys Acta 1365, 93 97.
10. Boekema EJ, Ubbink-Kok T, Lolkema JS, Brisson A Konings WN (1997) Visualization of a peripheral stalk in V-type ATPase: evidence for the stator structure essential for rotational catalysis. Proc Natl Acad Sci USA 94, 14291 14293.
11. Coskun Ü, Radermacher M, Müller V, Ruiz T Grüber G (2004) Three-dimensional organization of the archaeal A1-ATPase from Methanosarcina mazei Gö1. J Biol Chem 279, 22759 22764.
12. Leslie AG Walker JE (2000) Structural model of F1-ATPase and the implications for rotary catalysis. Philos Trans R Soc Lond B Biol Sci 355, 465 471.
13. Schäfer G, Engelhard M Müller V (1999) Bioenergetics of the Archaea. Microbiol Mol Biol Rev 63, 570 620.
14. Forgac M (2000) Structure, mechanism and regulation of the clathrin-coated vesicle and yeast vacuolar H+-ATPases. J Exp Biol 203, 71 80.
15. Senior AE, Nadanaciva S Weber J (2000) Rate acceleration of ATP hydrolysis by A1AO-ATP synthase. J Exp Biol 203 (Part 1 35 40.
16. Futai M, Omote H Maeda M (1995) Escherichia coli H+-ATPase (ATP synthase): catalytic site and roles of subunit interactions in energy coupling. Biochem Soc Trans 23, 785 789.
17. Dimroth P (1997) Primary sodium ion translocating enzymes. Biochim Biophys Acta 1318, 11 51.
18. Müller V, Aufurth S Rahlfs S (2001) The Na+ cycle in Acetobacterium woodii: identification and characterization of a Na+ translocating F1FO-ATPase with a mixed oligomer of 8 and 16 kDa proteolipids. Biochim Biophys Acta 1505, 108 120.
19. Fillingame RH, Jiang W Dmitriev OY (2000) Coupling H+ transport to rotary catalysis in F-type ATP synthases: structure and organization of the transmembrane rotary motor. J Exp Biol 203, 9 17.
20. Altendorf K, Stalz W, Greie J Deckers-Hebestreit G (2000) Structure and function of the FO complex of the ATP synthase from Escherichia coli. J Exp Biol 203, 19 28.
21. Abrahams JP, Leslie AGW, Lutter R Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621 628.
22. Pänke O, Gumbiowski K, Junge W Engelbrecht S (2000) F-ATPase: specific observation of the rotating c subunit oligomer of EFOEF1. FEBS Lett 472, 34 38.
23. Sambongi Y, Iko Y, Tanabe M, Omote H, Iwamoto-Kihara A, Ueda I, Yanagida T, Wada Y Futai M (1999) Mechanical rotation of the c subunit oligomer in ATP synthase (FOF1): direct observation. Science 286, 1722 1724.
24. Stock D, Gibbons C, Arechaga I, Leslie AG Walker JE (2000) The rotary mechanism of ATP synthase. Curr Opin Struct Biol 10, 672 679.
25. Yoshida M, Muneyuki E Hisabori T (2001) ATP synthase - a marvellous rotary engine of the cell. Nat Rev Mol Cell Biol 2, 669 677.
26. Duncan TM, Zhou Y, Bulygin VV, Hutcheon ML Cross RL (1995) Probing interactions of the Escherichia coli F0F1 ATP synthase beta and gamma subunits with disulphide cross-links. Biochem Soc Trans 23, 736 741.
27. Cross RL Duncan TM (1996) Subunit rotation in FOF1-ATP synthases as a means of coupling proton transport through FO to the binding changes in F1. J Bioenerg Biomembr 28, 403 408.
28. Nakano T, Ikegami T, Suzuki T, Yoshida M Akutsu H (2006) A new solution structure of ATP synthase subunit c from thermophilic Bacillus PS3, suggesting a local conformational change for H+-translocation. J Mol Biol 358, 132 144.
29. Yokoyama K, Nakano M, Imamura H, Yoshida M Tamakoshi M (2003) Rotation of the proteolipid ring in the V-ATPase. J Biol Chem 278, 24255 24258.
30. Dimroth P, von Ballmoos C, Meier T Kaim G (2003) Electrical power fuels rotary ATP synthase. Structure 11, 1469 1473.
31. Xing J, Wang H, von Ballmoos C, Dimroth P Oster G (2004) Torque generation by the Fo motor of the sodium ATPase. J Biophys 87, 2148 2163.
32. Altendorf K, Lukas M, Kohl B, Müller CR Sandermann H Jr. (1977) Isolation and purification of bacterial membrane proteins by the use of organic solvents: the lactose permease and the carbodiimide-reactive protein of the adenosinetriphosphatase complex of Escherichia coli. J Supramol Struct 6, 229 238.
33. Wachter E, Schmid R, Deckers G Altendorf K (1980) Amino acid replacement in dicyclohexylcarbodiimide-reactive proteins from mutant strains of Escherichia coli defective in the energy-transducing ATPase complex. FEBS Lett 113, 265 270.
34. Sebald W Hoppe J (1981) On the structure and genetics of the proteolipid subunit of the ATPase complex. Curr Top Bioenerg 12, 1 64.
35. Beechey RB, Linnett PE Fillingame RH (1979) Isolation of carbodiimide-binding proteins from mitochondria and Escherichia coli. Methods Enzymol 55, 426 434.
36. Fillingame RH Wopat AE (1978) Carbodiimide-resistant mutant of Escherichia coli: suppression of resistance to dicyclohexylcarbodiimide by growth on glucose or glycerol. J Bacteriol 134, 687 689.
37. Fillingame RH (1976) Purification of the carbodiimide-reactive protein component of the ATP energy-transducing system of Escherichia coli. J Biol Chem 251, 6630 6637.
38. Meier T, Polzer P, Diederichs K, Welte W Dimroth P (2005) Structure of the rotor ring of F-type Na+- ATPase from Ilyobacter tartaricus. Science 308, 659 662.
39. Rahlfs S Müller V (1997) Sequence of subunit c of the Na+-translocating F1F0 ATPase of Acetobacterium woodii: proposal for determinants of Na+ specificity as revealed by sequence comparisons. FEBS Lett 404, 269 271.
40. Meier T, Ferguson SA, Cook GM, Dimroth P Vonck J (2006) Structural investigations of the membrane-embedded rotor ring of the F-ATPase from Clostridium paradoxum. J Bacteriol 188, 7759 7764.
41. Murata T, Yamato I, Kakinuma Y, Leslie AG Walker JE (2005) Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae. Science 308, 654 659.
42. Bentrup KHZ, UbbinkKok T, Lolkema JS Konings WN (1997) An Na+-pumping V1V0-ATPase complex in the thermophilic bacterium Clostridium fervidus. J Bacteriol 179, 1274 1279.
43. Reidlinger J Müller V (1994) Purification of ATP synthase from Acetobacterium woodii and identification as a Na+-translocating F1F0-type enzyme. Eur J Biochem 223, 275 283.
44. Ferguson SA, Keis S Cook GM (2006) Biochemical and molecular characterization of a Na+-translocating F1FO-ATPase from the thermoalkaliphilic bacterium Clostridium paradoxum. J Bacteriol 188, 5045 5054.
45. Neumann S, Matthey U, Kaim G Dimroth P (1998) Purification and properties of the F1F0 ATPase of Ilyobacter tartaricus, a sodium ion pump. J Bacteriol 180, 3312 3316.
46. Laubinger W Dimroth P (1988) Characterization of the ATP synthase of Propionigenium modestum as a primary sodium pump. Biochemistry 27, 7531 7537.
47. Heefner DL Harold FM (1982) ATP-driven sodium pump in Streptococcus faecalis. Proc Natl Acad Sci USA 79, 2798 2802.
48. Lewalter K Müller V (2006) Bioenergetics of archaea: ancient energy conserving mechanisms developed in the early history of life. Biochim Biophys Acta 1757, 437 445.
49. Inatomi KI (1986) Characterization and purification of the membrane-bound ATPase of the archaebacterium Methanosarcina barkeri. J Bacteriol 167, 837 841.
50. Inatomi KI, Kamagata Y Nakamura K (1993) Membrane ATPase from the aceticlastic methanogen Methanothrix thermophila. J Bacteriol 175, 80 84.
51. Steinert K, Wagner V, Kroth-Pancic PG Bickel-Sandkötter S (1997) Characterization and subunit structure of the ATP synthase of the halophilic archaeon Haloferax volcanii and organization of the ATP synthase genes. J Biol Chem 272, 6261 6269.
52. Lingl A, Huber H, Stetter KO, Mayer F, Kellermann J Müller V (2003) Isolation of a complete A1AO ATP synthase comprising nine subunits from the hyperthermophile Methanococcus jannaschii. Extremophiles 7, 249 257.
53. Lemker T, Ruppert C, Stöger H, Wimmers S Müller V (2001) Overproduction of a functional A1 ATPase from the archaeon Methanosarcina mazei Gö1 in Escherichia coli. Eur J Biochem 268, 3744 3750.
54. Yamashita T Kawakita M (1992) Reconstitution of Na+/H+-antiporter of bovine renal brush-border membrane into proteoliposomes and detection of a 110-kDa protein cross-reactive with antibodies against a human Na+/H+-antiporter partial peptide in antiport-active fractions after partial fractionation. J Biochem 111, 162 167.
55. Spruth M, Reidlinger J Müller V (1995) Sodium ion dependence of inhibition of the Na+-translocating F1FO-ATPase from Acetobacterium woodii. Probing the site(s) involved in ion transport. Biochim Biophys Acta 1229, 96 102.
56. Atsumi T, Maekawa Y, Tokuda H Imae Y (1992) Amiloride at pH 7.0 inhibits the Na+-driven flagellar motors of Vibrio alginolyticus but allows cell growth. FEBS Lett 314, 114 116.
57. Kleyman TR Cragoe EJ Jr. (1988) Amiloride and its analogs as tools for the study of ion transport. J Membr Biol 105, 1 21.
58. Kluge C Dimroth P (1993) Kinetics of inactivation of the F1FO-ATPase of Propionigenium modestum by dicyclohexylcarbodiimide in relationship to H+ and Na+ concentration: probing the binding site for the coupling ions. Biochemistry 32, 10378 10386.
59. Müller V (2001) Bacterial fermentation. In Encyclopedia of Life Sciences, doi:.
60. Müller V, Blaut M, Heise R, Winner C Gottschalk G (1990) Sodium bioenergetics in methanogens and acetogens. FEMS Microbiol Rev 87, 373 377.
61. Müller V (2003) Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69, 6345 6353.
62. Gottschalk G Thauer RK (2001) The Na+-translocating methyltransferase complex from methanogenic archaea. Biochim Biophys Acta 1505, 28 36.
63. Deppenmeier U Müller V (2007) Life close to the thermodynamic limit: how methanogenic archaea conserve energy. In Results Probl Cell Differ (Richter D Tiedge H, eds), doi:. Springer, Heidelberg.
64. Müller V, Lingl A, Lewalter K Fritz M (2005) ATP synthases with novel rotor subunits: new insights into structure, function and evolution of ATPases. J Bioenerg Biomembr 37, 455 460.
65. Müller V, Lemker T, Lingl A, Weidner C, Coskun Ü Grüber G (2005) Bioenergetics of archaea: ATP synthesis under harsh environmental conditions. J Mol Microbiol Biotechnol 10, 167 180.
66. Sapra R, Bagramyan K Adams MW (2003) A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci USA 100, 7545 7550.
67. Robb FT, Maeder DL, Brown JR, Di Ruggiero J, Stump MD, Yeh RK, Weiss RB Dunn DM (2001) Genomic sequence of hyperthermophile Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol 330, 134 157.
68. Müller V (2004) An exceptional variability in the motor of archaeal A1AO ATPases: from multimeric to monomeric rotors comprising 6-13 ion binding sites. J Bioenerg Biomembr 36, 115 125.
69. Meier T Dimroth P (2002) Intersubunit bridging by Na+ ions as a rationale for the unusual stability of the c-rings of Na+-translocating F1F0 ATP synthases. EMBO Rep 3, 1094 1098.
70. Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36, 65 75.
71. Krulwich TA, Ito M, Gilmour R, Sturr MG, Guffanti AA Hicks DB (1996) Energetic problems of extremely alkaliphilic aerobes. Biochim Biophys Acta 1275, 21 26.
72. van de Vossenberg JLCM, Ubbink-Kok T, Elferink MGL, Driessen AJM Konings WN (1995) Ion permeability of the cytoplasmic membrane limits the maximum growth temperature of bacteria and archaea. Mol Microbiol 18, 925 932.
73. Huber G, Drobner E, Huber H Stetter KO (1992) Growth by aerobic oxidation of molecular hydrogen in archaea - a metabolic property so far unknown for this domain. Syst Appl Microbiol 15, 502 504.
74. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72, 248 254.
75. Bode C, Goebell H Stahler E (1968) Elimination of errors caused by turbidity in the determination of protein by the biuret method. Z Klin Chem Klin Biochem 6, 418 422.
76. Heinonen JE Lahti RJ (1981) A new and convenient colorimetric determination of inorganic orthophosphate and its application to the assay of inorganic pyrophosphatase. Anal Biochem 113, 313 317.
77. Towbin H, Staehelin T Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76, 4350 4354.
78. Shevchenko A, Wilm M, Vorm O Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68, 850 858.
79. Rosenfeld J, Capdevielle J, Guillemot JC Ferrara P (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal Biochem 203, 173 179.