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. 1994 May;176(9):2543–2550. doi: 10.1128/jb.176.9.2543-2550.1994

Delta mu Na+ drives the synthesis of ATP via an delta mu Na(+)-translocating F1F0-ATP synthase in membrane vesicles of the archaeon Methanosarcina mazei Gö1.

B Becher 1, V Müller 1
PMCID: PMC205391  PMID: 8169202

Abstract

Methanosarcina mazei Gö1 couples the methyl transfer from methyl-tetrahydromethanopterin to 2-mercaptoethanesulfonate (coenzyme M) with the generation of an electrochemical sodium ion gradient (delta mu Na+) and the reduction of the heterodisulfide of coenzyme M and 7-mercaptoheptanoylthreoninephosphate with the generation of an electrochemical proton gradient (delta muH+). Experiments with washed inverted vesicles were performed to investigate whether both ion gradients are used directly for the synthesis of ATP. delta mu Na+ and delta mu H+ were both able to drive the synthesis of ATP in the vesicular system. ATP synthesis driven by heterodisulfide reduction (delta mu H+) or an artificial delta pH was inhibited by the protonophore SF6847 but not by the sodium ionophore ETH157, whereas ETH157 but not SF6847 inhibited ATP synthesis driven by a chemical sodium ion gradient (delta pNa) as well as the methyl transfer reaction (delta mu Na+). Inhibition of the Na+/H+ antiporter led to a stimulation of ATP synthesis driven by the methyl transfer reaction (delta mu Na+), as well as by delta pNa. These experiments indicate that delta mu Na+ and delta mu H+ drive the synthesis of ATP via an Na(+)- and an H(+)-translocating ATP synthase, respectively. Inhibitor studies were performed to elucidate the nature of the ATP synthase(s) involved. delta pH-driven ATP synthesis was specifically inhibited by bafilomycin A1, whereas delta pNa-driven ATP synthesis was exclusively inhibited by 7-chloro-4-nitro-2-oxa-1,3-diazole, azide, and venturicidin. These results are evidence for the presence of an F(1)F(0)-ATP synthase in addition to the A(1)A(0)-ATP synthase in membranes of M. Mazei Gö1 and suggest that the F(1)F(0)-type enzyme is an Na+-translocating ATP synthase, whereas the A(1)A(0)-ATP synthase uses H+ as the coupling ion.

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Selected References

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  1. Becher B., Müller V., Gottschalk G. N5-methyl-tetrahydromethanopterin:coenzyme M methyltransferase of Methanosarcina strain Gö1 is an Na(+)-translocating membrane protein. J Bacteriol. 1992 Dec;174(23):7656–7660. doi: 10.1128/jb.174.23.7656-7660.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blaut M., Müller V., Gottschalk G. Energetics of methanogenesis studied in vesicular systems. J Bioenerg Biomembr. 1992 Dec;24(6):529–546. doi: 10.1007/BF00762346. [DOI] [PubMed] [Google Scholar]
  3. Bowman E. J. Comparison of the vacuolar membrane ATPase of Neurospora crassa with the mitochondrial and plasma membrane ATPases. J Biol Chem. 1983 Dec 25;258(24):15238–15244. [PubMed] [Google Scholar]
  4. Bowman E. J., Siebers A., Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972–7976. doi: 10.1073/pnas.85.21.7972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  6. CHANCE B., WILLIAMS G. R. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134. doi: 10.1002/9780470122624.ch2. [DOI] [PubMed] [Google Scholar]
  7. Chen W., Konisky J. Characterization of a membrane-associated ATPase from Methanococcus voltae, a methanogenic member of the Archaea. J Bacteriol. 1993 Sep;175(17):5677–5682. doi: 10.1128/jb.175.17.5677-5682.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crider B. P., Carper S. W., Lancaster J. R. Electron transfer-driven ATP synthesis in Methanococcus voltae is not dependent on a proton electrochemical gradient. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6793–6796. doi: 10.1073/pnas.82.20.6793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Denda K., Konishi J., Hajiro K., Oshima T., Date T., Yoshida M. Structure of an ATPase operon of an acidothermophilic archaebacterium, Sulfolobus acidocaldarius. J Biol Chem. 1990 Dec 15;265(35):21509–21513. [PubMed] [Google Scholar]
  10. Denda K., Konishi J., Oshima T., Date T., Yoshida M. A gene encoding the proteolipid subunit of Sulfolobus acidocaldarius ATPase complex. J Biol Chem. 1989 May 5;264(13):7119–7121. [PubMed] [Google Scholar]
  11. Deppenmeier U., Blaut M., Mahlmann A., Gottschalk G. Reduced coenzyme F420: heterodisulfide oxidoreductase, a proton- translocating redox system in methanogenic bacteria. Proc Natl Acad Sci U S A. 1990 Dec 1;87(23):9449–9453. doi: 10.1073/pnas.87.23.9449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dharmavaram R. M., Konisky J. Characterization of a P-type ATPase of the archaebacterium Methanococcus voltae. J Biol Chem. 1989 Aug 25;264(24):14085–14089. [PubMed] [Google Scholar]
  13. Dharmavaram R. M., Konisky J. Identification of a vanadate-sensitive, membrane-bound ATPase in the archaebacterium Methanococcus voltae. J Bacteriol. 1987 Sep;169(9):3921–3925. doi: 10.1128/jb.169.9.3921-3925.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dybas M., Konisky J. Energy transduction in the methanogen Methanococcus voltae is based on a sodium current. J Bacteriol. 1992 Sep;174(17):5575–5583. doi: 10.1128/jb.174.17.5575-5583.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. ELLMAN G. L. A colorimetric method for determining low concentrations of mercaptans. Arch Biochem Biophys. 1958 Apr;74(2):443–450. doi: 10.1016/0003-9861(58)90014-6. [DOI] [PubMed] [Google Scholar]
  16. Fischer R., Gärtner P., Yeliseev A., Thauer R. K. N5-methyltetrahydromethanopterin: coenzyme M methyltransferase in methanogenic archaebacteria is a membrane protein. Arch Microbiol. 1992;158(3):208–217. doi: 10.1007/BF00290817. [DOI] [PubMed] [Google Scholar]
  17. Gärtner P., Ecker A., Fischer R., Linder D., Fuchs G., Thauer R. K. Purification and properties of N5-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanobacterium thermoautotrophicum. Eur J Biochem. 1993 Apr 1;213(1):537–545. doi: 10.1111/j.1432-1033.1993.tb17792.x. [DOI] [PubMed] [Google Scholar]
  18. Heise R., Müller V., Gottschalk G. Presence of a sodium-translocating ATPase in membrane vesicles of the homoacetogenic bacterium Acetobacterium woodii. Eur J Biochem. 1992 Jun 1;206(2):553–557. doi: 10.1111/j.1432-1033.1992.tb16959.x. [DOI] [PubMed] [Google Scholar]
  19. Hippe H., Caspari D., Fiebig K., Gottschalk G. Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Proc Natl Acad Sci U S A. 1979 Jan;76(1):494–498. doi: 10.1073/pnas.76.1.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hochstein L. I. ATP synthesis in Halobacterium saccharovorum: evidence that synthesis may be catalysed by an F0F1-ATP synthase. FEMS Microbiol Lett. 1992 Oct 1;76(1-2):155–159. doi: 10.1111/j.1574-6968.1992.tb05455.x. [DOI] [PubMed] [Google Scholar]
  21. Ihara K., Mukohata Y. The ATP synthase of Halobacterium salinarium (halobium) is an archaebacterial type as revealed from the amino acid sequences of its two major subunits. Arch Biochem Biophys. 1991 Apr;286(1):111–116. doi: 10.1016/0003-9861(91)90015-b. [DOI] [PubMed] [Google Scholar]
  22. Ihara K, Abe T, Sugimura KI, Mukohata Y. HALOBACTERIAL A-ATP SYNTHASE IN RELATION TO V-ATPase. J Exp Biol. 1992 Nov 1;172(Pt 1):475–485. doi: 10.1242/jeb.172.1.475. [DOI] [PubMed] [Google Scholar]
  23. Inatomi K. Characterization and purification of the membrane-bound ATPase of the archaebacterium Methanosarcina barkeri. J Bacteriol. 1986 Sep;167(3):837–841. doi: 10.1128/jb.167.3.837-841.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Inatomi K., Eya S., Maeda M., Futai M. Amino acid sequence of the alpha and beta subunits of Methanosarcina barkeri ATPase deduced from cloned genes. Similarity to subunits of eukaryotic vacuolar and F0F1-ATPases. J Biol Chem. 1989 Jul 5;264(19):10954–10959. [PubMed] [Google Scholar]
  25. Inatomi K., Kamagata Y., Nakamura K. Membrane ATPase from the aceticlastic methanogen Methanothrix thermophila. J Bacteriol. 1993 Jan;175(1):80–84. doi: 10.1128/jb.175.1.80-84.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Inatomi K., Maeda M., Futai M. Dicyclohexylcarbodiimide-binding protein is a subunit of the Methanosarcina barkeri ATPase complex. Biochem Biophys Res Commun. 1989 Aug 15;162(3):1585–1590. doi: 10.1016/0006-291x(89)90856-5. [DOI] [PubMed] [Google Scholar]
  27. Inatomi K., Maeda M. Isolation of subunits from Methanosarcina barkeri ATPase: nucleotide-binding site in the alpha subunit. J Bacteriol. 1988 Dec;170(12):5960–5962. doi: 10.1128/jb.170.12.5960-5962.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kaesler B., Schönheit P. The role of sodium ions in methanogenesis. Formaldehyde oxidation to CO2 and 2H2 in methanogenic bacteria is coupled with primary electrogenic Na+ translocation at a stoichiometry of 2-3 Na+/CO2. Eur J Biochem. 1989 Sep 1;184(1):223–232. doi: 10.1111/j.1432-1033.1989.tb15010.x. [DOI] [PubMed] [Google Scholar]
  29. Kaesler B., Schönheit P. The sodium cycle in methanogenesis. CO2 reduction to the formaldehyde level in methanogenic bacteria is driven by a primary electrochemical potential of Na+ generated by formaldehyde reduction to CH4. Eur J Biochem. 1989 Dec 8;186(1-2):309–316. doi: 10.1111/j.1432-1033.1989.tb15210.x. [DOI] [PubMed] [Google Scholar]
  30. Kakinuma Y., Igarashi K., Konishi K., Yamato I. Primary structure of the alpha-subunit of vacuolar-type Na(+)-ATPase in Enterococcus hirae. Amplification of a 1000-bp fragment by polymerase chain reaction. FEBS Lett. 1991 Nov 4;292(1-2):64–68. doi: 10.1016/0014-5793(91)80835-q. [DOI] [PubMed] [Google Scholar]
  31. Kengen S. W., Daas P. J., Duits E. F., Keltjens J. T., van der Drift C., Vogels G. D. Isolation of a 5-hydroxybenzimidazolyl cobamide-containing enzyme involved in the methyltetrahydromethanopterin: coenzyme M methyltransferase reaction in Methanobacterium thermoautotrophicum. Biochim Biophys Acta. 1992 Feb 1;1118(3):249–260. doi: 10.1016/0167-4838(92)90282-i. [DOI] [PubMed] [Google Scholar]
  32. Kibak H., Taiz L., Starke T., Bernasconi P., Gogarten J. P. Evolution of structure and function of V-ATPases. J Bioenerg Biomembr. 1992 Aug;24(4):415–424. doi: 10.1007/BF00762534. [DOI] [PubMed] [Google Scholar]
  33. Kimmich G. A., Randles J., Brand J. S. Assay of picomole amounts of ATP, ADP, and AMP using the luciferase enzyme system. Anal Biochem. 1975 Nov;69(1):187–206. doi: 10.1016/0003-2697(75)90580-1. [DOI] [PubMed] [Google Scholar]
  34. Kleyman T. R., Cragoe E. J., Jr Amiloride and its analogs as tools in the study of ion transport. J Membr Biol. 1988 Oct;105(1):1–21. doi: 10.1007/BF01871102. [DOI] [PubMed] [Google Scholar]
  35. Kluge C., Dimroth P. 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. 1993 Oct 5;32(39):10378–10386. doi: 10.1021/bi00090a013. [DOI] [PubMed] [Google Scholar]
  36. Laubinger W., Dimroth P. Characterization of the Na+-stimulated ATPase of Propionigenium modestum as an enzyme of the F1F0 type. Eur J Biochem. 1987 Oct 15;168(2):475–480. doi: 10.1111/j.1432-1033.1987.tb13441.x. [DOI] [PubMed] [Google Scholar]
  37. Lübben M., Schäfer G. Chemiosmotic energy conversion of the archaebacterial thermoacidophile Sulfolobus acidocaldarius: oxidative phosphorylation and the presence of an F0-related N,N'-dicyclohexylcarbodiimide-binding proteolipid. J Bacteriol. 1989 Nov;171(11):6106–6116. doi: 10.1128/jb.171.11.6106-6116.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mountfort D. O. Evidence from ATP synthesis driven by a proton gradient in Methanosarcina barkeri. Biochem Biophys Res Commun. 1978 Dec 29;85(4):1346–1351. doi: 10.1016/0006-291x(78)91151-8. [DOI] [PubMed] [Google Scholar]
  39. Müller V., Blaut M., Gottschalk G. Generation of a transmembrane gradient of Na+ in Methanosarcina barkeri. Eur J Biochem. 1987 Jan 15;162(2):461–466. doi: 10.1111/j.1432-1033.1987.tb10624.x. [DOI] [PubMed] [Google Scholar]
  40. Müller V., Winner C., Gottschalk G. Electron-transport-driven sodium extrusion during methanogenesis from formaldehyde and molecular hydrogen by Methanosarcina barkeri. Eur J Biochem. 1988 Dec 15;178(2):519–525. doi: 10.1111/j.1432-1033.1988.tb14478.x. [DOI] [PubMed] [Google Scholar]
  41. Nelson N. Evolution of organellar proton-ATPases. Biochim Biophys Acta. 1992 May 20;1100(2):109–124. doi: 10.1016/0005-2728(92)90072-a. [DOI] [PubMed] [Google Scholar]
  42. Nelson N., Taiz L. The evolution of H+-ATPases. Trends Biochem Sci. 1989 Mar;14(3):113–116. doi: 10.1016/0968-0004(89)90134-5. [DOI] [PubMed] [Google Scholar]
  43. Peinemann S., Blaut M., Gottschalk G. ATP synthesis coupled to methane formation from methyl-CoM and H2 catalyzed by vesicles of the methanogenic bacterial strain Gö1. Eur J Biochem. 1989 Dec 8;186(1-2):175–180. doi: 10.1111/j.1432-1033.1989.tb15192.x. [DOI] [PubMed] [Google Scholar]
  44. Scheel E., Schäfer G. Chemiosmotic energy conversion and the membrane ATPase of Methanolobus tindarius. Eur J Biochem. 1990 Feb 14;187(3):727–735. doi: 10.1111/j.1432-1033.1990.tb15360.x. [DOI] [PubMed] [Google Scholar]
  45. Schäfer G., Meyering-Vos M. F-type or V-type? The chimeric nature of the archaebacterial ATP synthase. Biochim Biophys Acta. 1992 Jul 17;1101(2):232–235. doi: 10.1016/0005-2728(92)90233-r. [DOI] [PubMed] [Google Scholar]
  46. Smigán P., Rusnák P., Greksák M., Zhilina T. N., Zavarzin G. A. Mode of sodium ion action on methanogenesis and ATPase of the moderate halophilic methanogenis bacterium Methanohalophilus halophilus. FEBS Lett. 1992 Mar 30;300(2):193–196. doi: 10.1016/0014-5793(92)80194-l. [DOI] [PubMed] [Google Scholar]
  47. Stan-Lotter H., Bowman E. J., Hochstein L. I. Relationship of the membrane ATPase from Halobacterium saccharovorum to vacuolar ATPases. Arch Biochem Biophys. 1991 Jan;284(1):116–119. doi: 10.1016/0003-9861(91)90272-k. [DOI] [PubMed] [Google Scholar]
  48. Sumi M., Sato M. H., Denda K., Date T., Yoshida M. A DNA fragment homologous to F1-ATPase beta subunit was amplified from genomic DNA of Methanosarcina barkeri. Indication of an archaebacterial F-type ATPase. FEBS Lett. 1992 Dec 21;314(3):207–210. doi: 10.1016/0014-5793(92)81472-x. [DOI] [PubMed] [Google Scholar]
  49. Takase K., Yamato I., Kakinuma Y. Cloning and sequencing of the genes coding for the A and B subunits of vacuolar-type Na(+)-ATPase from Enterococcus hirae. Coexistence of vacuolar- and F0F1-type ATPases in one bacterial cell. J Biol Chem. 1993 Jun 5;268(16):11610–11616. [PubMed] [Google Scholar]

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