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Antonie van Leeuwenhoek

, Volume 87, Issue 4, pp 289–299 | Cite as

The energy metabolism of Methanomicrococcus blatticola: physiological and biochemical aspects

  • Wander W. Sprenger
  • Johannes H.P. Hackstein
  • Jan T. KeltjensEmail author
Article

Abstract

Methanomicrococcus blatticola, a methanogenic archaeon isolated from the cockroach Periplaneta americana, is specialised in methane formation by the hydrogen-dependent reduction of methanol, monomethyl-, dimethyl- or trimethylamine. Experiments with resting cells demonstrated that the capability to utilise the methylated one-carbon compounds was growth substrate dependent. Methanol-grown cells were unable of methylamine conversion, while cells cultured on one of the methylated amines did not metabolise methanol. Unlike trimethylamine, monomethyl- and dimethylamine metabolism appeared to be co-regulated. The central reaction in the energy metabolism of all methanogens studied so far, the reduction of CoM-S-S-CoB, was catalysed with high specific activity by a cell-free system. Activity was associated with the membrane fraction. Phenazine was an efficient artificial substrate in partial reactions, suggesting that the recently discovered methanophenazine might act in the organism as the physiological intermediary electron carrier. Our experiments also showed that M. blatticola apparently lacks the pathway for methyl-coenzyme oxidation to CO2, explaining the strict requirement for hydrogen in methanogenesis and the obligately heterotrophic character of the organism.

Keywords

Energy metabolism Methanogenic Archaea Methanol Methanomicrococcus blatticola Methanophenazine Methylamine 

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References

  1. 1.
    Abken, H.J., Tietze, M., Brodersen, J., Bäumer, S., Beifuss, U., Deppenmeier, U. 1998Isolation and characterization of methanophenazine and function of phenazines in membrane-bound electron transport of Methanosarcina mazei GölJ. Bacteriol.18020272032PubMedGoogle Scholar
  2. 2.
    Burke, S.A., Krzycki, J.A. 1997Reconstitution of monomethylamine:coenzyme M methyl transfer with a corrinoid protein and two methyltransferases purified from Methanosarcina barkeriJ. Biol. Chem.2721657016577CrossRefPubMedGoogle Scholar
  3. 3.
    Burke, S.A., Lo, S.L., Krzycki, J.A. 1998Clustered genes encoding the methyltransferases of methanogenesis from monomethylamineJ. Bacteriol.18034323440PubMedGoogle Scholar
  4. 4.
    Daas, P.J.H., Gerrits, K.A.A., Keltjens, J.T., der Drift, C., Vogels, G.D. 1993Involvement of an activation protein in the methanol:2-mercaptoethanesulfonic methyltransferase reaction in Methanosarcina barkeriJ. Bacteriol.17512781283PubMedGoogle Scholar
  5. 5.
    Daas, P.J.H., Wassenaar, R.W., Willemsen, P., Keltjens, J.T., der Drift, C., Vogels, G.D. 1996Purification and properties of an enzyme involved in the ATP-dependent activation of the methanol:2-mercaptoethanesulfonic acid methyltransferase reaction in Methanosarcina barkeriJ. Biol. Chem.2712233922345CrossRefPubMedGoogle Scholar
  6. 6.
    Deppenmeier, U. 2003Redox-driven proton translocation in methanogenic ArchaeaCell Mol. Life Sci.5915131533Google Scholar
  7. 7.
    Deppenmeier, U., Johann, A., Hartsch, T. 2002The genome of Methanosarcina mazei: evidence for lateral gene transfer between Bacteria and ArchaeaJ. Mol. Microbiol. Biotechnol.4453461PubMedGoogle Scholar
  8. 8.
    Deppenmeier, U., Lienard, T., Gottschalk, G. 1999Novel reactions involved in energy conservation by methanogenic archaeaFEBS Lett.457291297CrossRefPubMedGoogle Scholar
  9. 9.
    Ellermann, J., Hedderich, R., Bücher, R., Thauer, R.K. 1988The final step in methane formationEur. J. Biochem.172669677CrossRefPubMedGoogle Scholar
  10. 10.
    Ferguson, D.J., Krzycki, J.A. 1997Reconstitution of trimethylamine-dependent coenzyme M methylation with the trimethylamine corrinoid protein and the isozymes of methyltransferase II from Methanosarcina barkeriJ. Bacteriol.179846852PubMedGoogle Scholar
  11. 11.
    Ferguson, D.J., Gorlatova, N., Grahame, D.A., Krzycki, J.A. 2000Reconstitution of dimethylamine : coenzyme M methyl transfer with a discrete corrinoid protein and two methyltransferases purified from Methanosarcina barkeriJ. Biol. Chem.2752905329060CrossRefPubMedGoogle Scholar
  12. 12.
    Ferry, J.G. 1999Enzymology of one-carbon metabolism in methanogenic pathwaysFEMS Microbiol. Rev.231338CrossRefPubMedGoogle Scholar
  13. 13.
    Galagan, J.E., Nusbaum, C., Roy, A. 2002The genome of M. acetivorans reveals extensive metabolic and physiological diversityGenome Res.12532542CrossRefPubMedGoogle Scholar
  14. 14.
    Gijzen, H.J., Broers, C.A.M., Barugahare, M., Stumm, C.K. 1991Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach Periplaneta americanaAppl. Environ. Microbiol.5716301634PubMedGoogle Scholar
  15. 15.
    Hippe, H., Caspari, D., Fiebig, K., Gottschalk, G. 1979Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeriProc. Natl. Acad. Sci. USA76494498PubMedGoogle Scholar
  16. 16.
    Kengen, S.W., Daas, P.J.H., Keltjens, J.T., der Drift, C., Vogels, G.D. 1990Stimulation of the methyl-tetrahydromethanopterin:coenzyme M methyltransferase reaction in cell-free extracts of Methanobacterium thermoautotrophicum by the heterodisulfide of coenzyme M and 7-mercaptoheptanoylthreonine phosphateArch. Microbiol.154156161CrossRefGoogle Scholar
  17. 17.
    Paul, L., Krzycki, J.A. 1996Sequence and transcript analysis of a novel Methanosarcina barkeri methyltransferase II homolog and its associated corrinoid protein homologous to methionine synthetaseJ. Bacteriol.17865996607PubMedGoogle Scholar
  18. 18.
    Sprenger, W.W., van Belzen, M.C., Rosenberg, J., Hackstein, J.H.P., Keltjens, J.T. 2000Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americanaInt. J. Sys. Evol. Microbiol.5019891999Google Scholar
  19. 19.
    te Brömmelstroet, B.W., Hensgens, C.M.H., Keltjens, J.T., der Drift, C., Vogels, G.D. 1991Purification and characterization of coenzyme F420-dependent 5,10-methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum strain ΔHBiochim. Biophys. Acta10737784PubMedGoogle Scholar
  20. 20.
    Thauer, R.K. 1998Biochemistry of methanogenesis: a tribute to Marjory StephensonMicrobiology UK14423772406Google Scholar
  21. 21.
    Vermeij, P., Broers, F.J.M., Detmers, F.J.M., Keltjens, J.T., der Drift, C. 1994Purification and characterization of factor F390 synthetase from Methanobacterium thermoautotrophicum (strain ΔH)Eur. J. Biochem.226185191CrossRefPubMedGoogle Scholar
  22. 22.
    Vogels, G.D., Keltjens, J.T., der Drift, C. 1988Biochemistry of methane productionZehnder, A.J.B. eds. Biology of Anaerobic MicroorganismsJohn Wiley & SonsNew York707770Google Scholar
  23. 23.
    Wassenaar, R.W., Daas, P.J.H., Geerts, W.J., Keltjens, J.T., der Drift, C. 1996Involvement of methyltransferase-activating protein and methyltransferase 2 isoenzyme II in methylamine:coenzyme M methyltransferase reactions in MethanosarcinaJ. Bacteriol.17869376944PubMedGoogle Scholar
  24. 24.
    Wassenaar, R.W., Keltjens, J.T., der Drift, C., Vogels, G.D. 1998Purification and characterization of dimethylamine: 5-hydroxybenzimidazolylcobamide methyltransferase from Methanosarcina barkeri FusaroEur. J. Biochem.253692697CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Wander W. Sprenger
    • 1
    • 2
  • Johannes H.P. Hackstein
    • 1
  • Jan T. Keltjens
    • 1
    Email author
  1. 1.Department of Microbiology, Faculty of ScienceRadboud University of NijmegenNijmegenThe Netherlands
  2. 2.Department of Aquatic Ecology and EcotoxicologyUniversity of AmsterdamAmsterdamThe Netherlands

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