Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Methanogens catalyze the hydrogen-dependent eight-electron reduction of carbon dioxide to methane. Two of the key catalysts in the eight-electron reduction pathway are the nickel-containing enzymes F420-reducing hydrogenase and methyl reductase. In the present study, the structures of these archaebacterial enzymes from Methanobacterium thermoautotrophicum delta H have been determined by electron microscopy. By negative stain techniques, F420 hydrogenase was found to be a ring structure with a diameter of 15.7 nm and an inner channel 4 nm in diameter. Shadow-casting experiments demonstrated that the rings were 8.5 nm deep, indicating a holoenzyme molecular weight of 8.0 X 10(5). Methyl reductase appeared to be an oligomeric complex of dimensions 8.5 by 9 by 11 nm, with a central stain-penetrating region. The morphology and known subunit composition suggest a model in which the subunits are arranged as an eclipsed pair of open trimers. Methyl reductase was also found in the form of larger aggregates and in paracrystalline arrays derived from highly concentrated solutions. The extremely large size of F420 hydrogenase and the methyl reductase supramolecular assemblies may have relevance in vivo in the construction of multiprotein arrays that function in methane biogenesis.

Bibliography

Wackett, L. P., Hartwieg, E. A., King, J. A., Orme-Johnson, W. H., & Walsh, C. T. (1987). Electron microscopy of nickel-containing methanogenic enzymes: methyl reductase and F420-reducing hydrogenase. Journal of Bacteriology, 169(2), 718–727.

Authors 5
  1. L P Wackett (first)
  2. E A Hartwieg (additional)
  3. J A King (additional)
  4. W H Orme-Johnson (additional)
  5. C T Walsh (additional)
References 28 Referenced 41
  1. Ames , G. F. 1974 . Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs: membrane, soluble, and periplasmic proteins . J. Biol. Chem. 249 : 634 644. (10.1016/S0021-9258(19)43074-3) / J. Biol. Chem. / Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs: membrane, soluble, and periplasmic proteins by Ames G. F. (1974)
  2. Ankel-Fuchs , D. , and R. K. Thauer . 1986 . Methane formation from methyl-coenzyme M in a system containing methylcoenzyme M reductase, component B and reduced cobalamin . Eur. J. Biochem. 156 : 171 - 177 . (10.1111/j.1432-1033.1986.tb09563.x) / Eur. J. Biochem. / Methane formation from methyl-coenzyme M in a system containing methylcoenzyme M reductase, component B and reduced cobalamin by Ankel-Fuchs D. (1986)
  3. Bacher , A. , H. C. Ludwig , and H. Schnepple . 1986 . Heavy riboflavin synthase from Bacillus subtilis: quaternary structure and reaggregation . J. Mol. Biol. 187 : 75 - 86 . (10.1016/0022-2836(86)90407-9) / J. Mol. Biol. / Heavy riboflavin synthase from Bacillus subtilis: quaternary structure and reaggregation by Bacher A. (1986)
  4. Cantor C. R. and P. R. Schimmel. 1980. Biophysical chemistry. Part II. Techniques for the study of biological structure and function. W. H. Freeman and Company San Francisco.
  5. Daniels , L. , R. Sparling , and D. Sprott . 1984 . The bioenergetics of methanogenesis . Biochim. Biophys. Acta 768 : 113 - 163 . (10.1016/0304-4173(84)90002-8) / Biochim. Biophys. Acta / The bioenergetics of methanogenesis by Daniels L. (1984)
  6. Doddema , H. J. , C. van der Drift , G. D. Vogels , and M. Veenhuis . 1979 . Chemiosmotic coupling in Methanobacterium thermoautotrophicum: hydrogen-dependent adenosine 5'- triphosphate synthesis by subcellular particles . J. Bacteriol. 140 : 1081 - 1089 . (10.1128/jb.140.3.1081-1089.1979) / J. Bacteriol. / Chemiosmotic coupling in Methanobacterium thermoautotrophicum: hydrogen-dependent adenosine 5'- triphosphate synthesis by subcellular particles by Doddema H. J. (1979)
  7. Eliefson , W. L. , and R. S. Wolfe . 1981 . Component C of the methyl reductase system of Methanobacterium . J. Biol. Chem. 256 : 4259 - 4262 . (10.1016/S0021-9258(19)69427-5) / J. Biol. Chem. / Component C of the methyl reductase system of Methanobacterium by Eliefson W. L. (1981)
  8. Fox , G. E. , E. Stackebrandt , R. B. Hespell , J. Gibson , J. Maniloff , T. A. Dyer , R. S. Wolfe , W. E. Balch , R. S. Tanner , L. J. Margum , L. B. Zablen , R. Blakemore , R. Gupta , L. Bonen , B. J. Lewis , D. A. Stahl , K. R. Luehrsen , K. N. Chen , and C. R. Woese . 1980 . The phylogeny of prokaryotes . Science 209 : 457 - 463 . (10.1126/science.6771870) / Science / The phylogeny of prokaryotes by Fox G. E. (1980)
  9. Gunsalus , R. P. , and R. S. Wolfe . 1977 . Stimulation of CO2 reduction to methane by methyl coenzyme M in extracts of Methanobacterium . Biochem. Biophys. Res. Commun. 76 : 790 - 795 . (10.1016/0006-291X(77)91570-4) / Biochem. Biophys. Res. Commun. / Stimulation of CO2 reduction to methane by methyl coenzyme M in extracts of Methanobacterium by Gunsalus R. P. (1977)
  10. Gunsalus , R. P. , and R. S. Wolfe . 1980 . Methyl coenzyme M reductase from Methanobacterium thermoautotrophicum: resolution and properties of the components . J. Biol. Chem. 255 : 1891 - 1895 . (10.1016/S0021-9258(19)85966-5) / J. Biol. Chem. / Methyl coenzyme M reductase from Methanobacterium thermoautotrophicum: resolution and properties of the components by Gunsalus R. P. (1980)
  11. Hausinger , R. P. , W. H. Orme-Johnson , and C. T. Walsh . 1984 . Nickel tetrapyrole cofactor F430: comparison of forms bound to methyl coenzyme M reductase and protein free in cells of Methanobacterium thermoautotrophicum AH . Biochemistry 23 : 801 - 804 . (10.1021/bi00300a003) / Biochemistry / Nickel tetrapyrole cofactor F430: comparison of forms bound to methyl coenzyme M reductase and protein free in cells of Methanobacterium thermoautotrophicum AH by Hausinger R. P. (1984)
  12. Jacobson , F. S. , L. Daniels , J. A. Fox , C. T. Walsh , and W. H. Orme-Johnson . 1982 . Purification and properties of an 8- hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum . J. Biol. Chem. 257 : 3385 - 3388 . (10.1016/S0021-9258(18)34788-4) / J. Biol. Chem. / Purification and properties of an 8- hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum by Jacobson F. S. (1982)
  13. Jin , S. - L. C. , D. K. Blanchard , and J. -S. Chen . 1983 . Two hydrogenases with distinct electron carrier specificity and subunit composition in Methanobacterium formicicum . Biochim. Biophys. Acta 748 : 8 - 20 . (10.1016/0167-4838(83)90021-3) / Biochim. Biophys. Acta / Two hydrogenases with distinct electron carrier specificity and subunit composition in Methanobacterium formicicum by Jin S. (1983)
  14. Kell D. B. H. J. Doddema J. G. Morris and G. D. Vogels. 1980. Energy coupling in methanogens p. 43-59. In H. Dalton (ed.) Proceedings of the third international symposium on microbial growth on C-1 compounds. Heyden Press London.
  15. Lake , J. A. , and L. Kahan . 1975 . Ribosomal proteins S5, S11, S13, and S19 localized by electron microscopy of antibodylabelled subunits . J. Mol. Biol. 99 : 631 - 644 . (10.1016/S0022-2836(75)80177-X) / J. Mol. Biol. / Ribosomal proteins S5, S11, S13, and S19 localized by electron microscopy of antibodylabelled subunits by Lake J. A. (1975)
  16. Metzler D. E. 1977. Biochemistry: chemical reactions of living cells. Academic Press Inc. New York.
  17. Moura , I. , J. J. G. Moura , H. Santos , A. V. Xavier , G. Burch , H. D. Peck , and J. Le Gall . 1983 . Proteins containing the factor F430 from Methanosarcina barkeri and Methanobacterium thermoautotrophicum: isolation and properties . Biochim. Biophys. Acta 742 : 84 - 90 . (10.1016/0167-4838(83)90362-X) / Biochim. Biophys. Acta / Proteins containing the factor F430 from Methanosarcina barkeri and Methanobacterium thermoautotrophicum: isolation and properties by Moura I. (1983)
  18. Pfaltz , A. , B. Juan , A. Fassler , A. Eschenmoser , R. Jaenchen , H. H. Gilles , G. Diekert , and R. K. Thauer . 1982 . Zur Kenntnis des Faktors F430 aus methanogenen Bakterien: Struktur des porphinoiden Ligandsystems . Helv. Chim. Acta 65 : 828 - 865 . (10.1002/hlca.19820650320) / Helv. Chim. Acta / Zur Kenntnis des Faktors F430 aus methanogenen Bakterien: Struktur des porphinoiden Ligandsystems by Pfaltz A. (1982)
  19. Pfaltz , A. , D. A. Livingston , B. Juan , G. Diekert , R. K. Thauer , and A. Eschenmoser . 1985 . Zur Kenntnis des Faktors F430 aus methanogenen Bakterien: uber die Natur der Isolierungsartefakte von F430, ein Beitrag zur Chemie von F430 und zur konformationellenStereochemiederLigandperipherievonhydroporphinoiden Nickel (II)-Komplexen . Helv. Chim. Acta 68 : 1338 - 1358 . (10.1002/hlca.19850680527) / Helv. Chim. Acta / Zur Kenntnis des Faktors F430 aus methanogenen Bakterien: uber die Natur der Isolierungsartefakte von F430, ein Beitrag zur Chemie von F430 und zur konformationellenStereochemiederLigandperipherievonhydroporphinoiden Nickel (II)-Komplexen by Pfaltz A. (1985)
  20. Shively , J. M. , F. L. Ball , and B. W. Kline . 1973 . Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neopolitanus . J. Bacteriol. 116 : 1405 - 1411 . (10.1128/jb.116.3.1405-1411.1973) / J. Bacteriol. / Electron microscopy of the carboxysomes (polyhedral bodies) of Thiobacillus neopolitanus by Shively J. M. (1973)
  21. Sprott , G. D. , L. C. Sowden , J. R. Colvin , K. F. Jarrell , and T. J. Beveridge . 1984 . Methanogenesis in the absence of intracytoplasmic membranes . Can. J. Microbiol. 30 : 594 - 604 . (10.1139/m84-089) / Can. J. Microbiol. / Methanogenesis in the absence of intracytoplasmic membranes by Sprott G. D. (1984)
  22. Srere P. A. 1985. Organization of proteins within the mitochondrion p. 1-61. In G. R. Welch (ed.) Organized multienzyme systems: catalytic properties. Academic Press Inc. Orlando Fla. (10.1016/B978-0-12-744040-8.50006-2)
  23. Stadtman E. R. and A. Ginsburg. 1974. The glutamine synthetase of Escherichia coli: structure and control p. 766. In P. D. Boyer (ed.) The enzymes vol. 10. Academic Press Inc. New York. (10.1016/S1874-6047(08)60156-0)
  24. Stupperich , E. , K. E. Hammel , G. Fuchs , and R. K. Thauer . 1983 . Carbon monoxide fixation into the carboxyl group of acetyl coenzyme A during autotrophic growth of Methanobacterium . FEBS Lett. 152 : 21 - 23 . (10.1016/0014-5793(83)80473-6) / FEBS Lett. / Carbon monoxide fixation into the carboxyl group of acetyl coenzyme A during autotrophic growth of Methanobacterium by Stupperich E. (1983)
  25. Tiedge , H. , H. Lunsdorf , G. Schafer , and H. U. Schairer . 1985 . Subunit stoichiometry and juxtaposition of the photosynthetic coupling factor 1: immunoelectron microscopy using monoclonal antibodies . Proc. Natl. Acad. Sci. USA 80 : 4894 - 4898 . / Proc. Natl. Acad. Sci. USA / Subunit stoichiometry and juxtaposition of the photosynthetic coupling factor 1: immunoelectron microscopy using monoclonal antibodies by Tiedge H. (1985)
  26. Wolfe , R. S. 1985 . Unusual coenzymes of methanogenesis . Trends Biochem. Sci. 10 : 396 - 399 . (10.1016/0968-0004(85)90068-4) / Trends Biochem. Sci. / Unusual coenzymes of methanogenesis by Wolfe R. S. (1985)
  27. Yamazaki , S. 1982 . A selenium-containing hydrogenase from Methanococcus vannielii . J. Biol. Chem. 257 : 7926 - 7929 . (10.1016/S0021-9258(18)34271-6) / J. Biol. Chem. / A selenium-containing hydrogenase from Methanococcus vannielii by Yamazaki S. (1982)
  28. Zeikus , J. G. , and R. S. Wolfe . 1972 . Methanobacterium thermoautotrophicus sp. n., an anaerobic, autotrophic, extreme thermophile . J. Bacteriol. 109 : 707 - 713 . (10.1128/jb.109.2.707-713.1972) / J. Bacteriol. / Methanobacterium thermoautotrophicus sp. n., an anaerobic, autotrophic, extreme thermophile by Zeikus J. G. (1972)
Dates
Type When
Created 8 years, 9 months ago (Nov. 2, 2016, 6:42 p.m.)
Deposited 3 years, 1 month ago (July 11, 2022, 11:18 p.m.)
Indexed 1 year, 8 months ago (Dec. 24, 2023, 11:26 a.m.)
Issued 38 years, 6 months ago (Feb. 1, 1987)
Published 38 years, 6 months ago (Feb. 1, 1987)
Published Print 38 years, 6 months ago (Feb. 1, 1987)
Funders 0

None

@article{Wackett_1987, title={Electron microscopy of nickel-containing methanogenic enzymes: methyl reductase and F420-reducing hydrogenase}, volume={169}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.169.2.718-727.1987}, DOI={10.1128/jb.169.2.718-727.1987}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Wackett, L P and Hartwieg, E A and King, J A and Orme-Johnson, W H and Walsh, C T}, year={1987}, month=feb, pages={718–727} }