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The energy metabolism of Methanomicrococcus blatticola: physiological and biochemical aspects

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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.

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References

  1. H.J. Abken M. Tietze J. Brodersen S. Bäumer U. Beifuss U. Deppenmeier (1998) ArticleTitleIsolation and characterization of methanophenazine and function of phenazines in membrane-bound electron transport of Methanosarcina mazei Göl J. Bacteriol. 180 2027–2032 Occurrence Handle1:CAS:528:DyaK1cXisVCgsLY%3D Occurrence Handle9555882

    CAS  PubMed  Google Scholar 

  2. S.A. Burke J.A. Krzycki (1997) ArticleTitleReconstitution of monomethylamine:coenzyme M methyl transfer with a corrinoid protein and two methyltransferases purified from Methanosarcina barkeri J. Biol. Chem. 272 16570–16577 Occurrence Handle10.1074/jbc.272.26.16570 Occurrence Handle1:CAS:528:DyaK2sXkt1ars7o%3D Occurrence Handle9195968

    Article  CAS  PubMed  Google Scholar 

  3. S.A. Burke S.L. Lo J.A. Krzycki (1998) ArticleTitleClustered genes encoding the methyltransferases of methanogenesis from monomethylamine J. Bacteriol. 180 3432–3440 Occurrence Handle1:CAS:528:DyaK1cXkt1KmtL4%3D Occurrence Handle9642198

    CAS  PubMed  Google Scholar 

  4. P.J.H. Daas K.A.A. Gerrits J.T. Keltjens C. der Drift G.D. Vogels (1993) ArticleTitleInvolvement of an activation protein in the methanol:2-mercaptoethanesulfonic methyltransferase reaction in Methanosarcina barkeri J. Bacteriol. 175 1278–1283 Occurrence Handle1:CAS:528:DyaK3sXhvVKlsLk%3D Occurrence Handle8444790

    CAS  PubMed  Google Scholar 

  5. P.J.H. Daas R.W. Wassenaar P. Willemsen J.T. Keltjens C. der Drift G.D. Vogels (1996) ArticleTitlePurification and properties of an enzyme involved in the ATP-dependent activation of the methanol:2-mercaptoethanesulfonic acid methyltransferase reaction in Methanosarcina barkeri J. Biol. Chem. 271 22339–22345 Occurrence Handle10.1074/jbc.271.37.22339 Occurrence Handle1:CAS:528:DyaK28XlslaitLs%3D Occurrence Handle8798394

    Article  CAS  PubMed  Google Scholar 

  6. U. Deppenmeier (2003) ArticleTitleRedox-driven proton translocation in methanogenic Archaea Cell Mol. Life Sci. 59 1513–1533

    Google Scholar 

  7. U. Deppenmeier A. Johann T. Hartsch (2002) ArticleTitleThe genome of Methanosarcina mazei: evidence for lateral gene transfer between Bacteria and Archaea J. Mol. Microbiol. Biotechnol. 4 453–461 Occurrence Handle1:CAS:528:DC%2BD38XlsVGks7Y%3D Occurrence Handle12125824

    CAS  PubMed  Google Scholar 

  8. U. Deppenmeier T. Lienard G. Gottschalk (1999) ArticleTitleNovel reactions involved in energy conservation by methanogenic archaea FEBS Lett. 457 291–297 Occurrence Handle10.1016/S0014-5793(99)01026-1 Occurrence Handle1:CAS:528:DyaK1MXls12itrc%3D Occurrence Handle10471795

    Article  CAS  PubMed  Google Scholar 

  9. J. Ellermann R. Hedderich R. Bücher R.K. Thauer (1988) ArticleTitleThe final step in methane formation Eur. J. Biochem. 172 669–677 Occurrence Handle10.1111/j.1432-1033.1988.tb13941.x Occurrence Handle1:CAS:528:DyaL1cXitFyjt7Y%3D Occurrence Handle3350018

    Article  CAS  PubMed  Google Scholar 

  10. D.J. Ferguson J.A. Krzycki (1997) ArticleTitleReconstitution of trimethylamine-dependent coenzyme M methylation with the trimethylamine corrinoid protein and the isozymes of methyltransferase II from Methanosarcina barkeri J. Bacteriol. 179 846–852 Occurrence Handle1:CAS:528:DyaK2sXovV2rtg%3D%3D Occurrence Handle9006042

    CAS  PubMed  Google Scholar 

  11. D.J. Ferguson N. Gorlatova D.A. Grahame J.A. Krzycki (2000) ArticleTitleReconstitution of dimethylamine : coenzyme M methyl transfer with a discrete corrinoid protein and two methyltransferases purified from Methanosarcina barkeri J. Biol. Chem. 275 29053–29060 Occurrence Handle10.1074/jbc.M910218199 Occurrence Handle1:CAS:528:DC%2BD3cXms1CqtLs%3D Occurrence Handle10852929

    Article  CAS  PubMed  Google Scholar 

  12. J.G. Ferry (1999) ArticleTitleEnzymology of one-carbon metabolism in methanogenic pathways FEMS Microbiol. Rev. 23 13–38 Occurrence Handle10.1016/S0168-6445(98)00029-1 Occurrence Handle1:CAS:528:DyaK1MXht1OgtLc%3D Occurrence Handle10077852

    Article  CAS  PubMed  Google Scholar 

  13. J.E. Galagan C. Nusbaum A. Roy (2002) ArticleTitleThe genome of M. acetivorans reveals extensive metabolic and physiological diversity Genome Res. 12 532–542 Occurrence Handle10.1101/gr.223902 Occurrence Handle1:CAS:528:DC%2BD38XivVemt74%3D Occurrence Handle11932238

    Article  CAS  PubMed  Google Scholar 

  14. H.J. Gijzen C.A.M. Broers M. Barugahare C.K. Stumm (1991) ArticleTitleMethanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach Periplaneta americana Appl. Environ. Microbiol. 57 1630–1634 Occurrence Handle1:STN:280:By6A3snntVA%3D Occurrence Handle1908205

    CAS  PubMed  Google Scholar 

  15. H. Hippe D. Caspari K. Fiebig G. Gottschalk (1979) ArticleTitleUtilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri Proc. Natl. Acad. Sci. USA 76 494–498 Occurrence Handle1:CAS:528:DyaE1MXpvFynsA%3D%3D Occurrence Handle284366

    CAS  PubMed  Google Scholar 

  16. S.W. Kengen P.J.H. Daas J.T. Keltjens C. der Drift G.D. Vogels (1990) ArticleTitleStimulation of the methyl-tetrahydromethanopterin:coenzyme M methyltransferase reaction in cell-free extracts of Methanobacterium thermoautotrophicum by the heterodisulfide of coenzyme M and 7-mercaptoheptanoylthreonine phosphate Arch. Microbiol. 154 156–161 Occurrence Handle10.1007/BF00423326 Occurrence Handle1:CAS:528:DyaK3cXlsVylt7w%3D

    Article  CAS  Google Scholar 

  17. L. Paul J.A. Krzycki (1996) ArticleTitleSequence and transcript analysis of a novel Methanosarcina barkeri methyltransferase II homolog and its associated corrinoid protein homologous to methionine synthetase J. Bacteriol. 178 6599–6607 Occurrence Handle1:CAS:528:DyaK28Xmsl2lu7s%3D Occurrence Handle8932317

    CAS  PubMed  Google Scholar 

  18. W.W. Sprenger M.C. van Belzen J. Rosenberg J.H.P. Hackstein J.T. Keltjens (2000) ArticleTitleMethanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana Int. J. Sys. Evol. Microbiol. 50 1989–1999 Occurrence Handle1:CAS:528:DC%2BD3MXls1Ghuw%3D%3D

    CAS  Google Scholar 

  19. B.W. te Brömmelstroet C.M.H. Hensgens J.T. Keltjens C. der Drift G.D. Vogels (1991) ArticleTitlePurification and characterization of coenzyme F420-dependent 5,10-methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum strain ΔH Biochim. Biophys. Acta 1073 77–84 Occurrence Handle1991149

    PubMed  Google Scholar 

  20. R.K. Thauer (1998) ArticleTitleBiochemistry of methanogenesis: a tribute to Marjory Stephenson Microbiology UK 144 2377–2406 Occurrence Handle1:CAS:528:DyaK1cXmt1ygurc%3D

    CAS  Google Scholar 

  21. P. Vermeij F.J.M. Broers F.J.M. Detmers J.T. Keltjens C. der Drift (1994) ArticleTitlePurification and characterization of factor F390 synthetase from Methanobacterium thermoautotrophicum (strain ΔH) Eur. J. Biochem. 226 185–191 Occurrence Handle10.1111/j.1432-1033.1994.tb20040.x Occurrence Handle1:CAS:528:DyaK2cXmsV2iurc%3D Occurrence Handle7957247

    Article  CAS  PubMed  Google Scholar 

  22. G.D. Vogels J.T. Keltjens C. der Drift (1988) Biochemistry of methane production A.J.B. Zehnder (Eds) Biology of Anaerobic Microorganisms John Wiley & Sons New York 707–770

    Google Scholar 

  23. R.W. Wassenaar P.J.H. Daas W.J. Geerts J.T. Keltjens C. der Drift (1996) ArticleTitleInvolvement of methyltransferase-activating protein and methyltransferase 2 isoenzyme II in methylamine:coenzyme M methyltransferase reactions in Methanosarcina J. Bacteriol. 178 6937–6944 Occurrence Handle1:CAS:528:DyaK28Xnt1ertL8%3D Occurrence Handle8955317

    CAS  PubMed  Google Scholar 

  24. R.W. Wassenaar J.T. Keltjens C. der Drift G.D. Vogels (1998) ArticleTitlePurification and characterization of dimethylamine: 5-hydroxybenzimidazolylcobamide methyltransferase from Methanosarcina barkeri Fusaro Eur. J. Biochem. 253 692–697 Occurrence Handle10.1046/j.1432-1327.1998.2530692.x Occurrence Handle1:CAS:528:DyaK1cXkt1SqtLY%3D Occurrence Handle9654067

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Jan T. Keltjens.

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Sprenger, W., Hackstein, J. & Keltjens, J. The energy metabolism of Methanomicrococcus blatticola: physiological and biochemical aspects. Antonie Van Leeuwenhoek 87, 289–299 (2005). https://doi.org/10.1007/s10482-004-5941-5

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  • DOI: https://doi.org/10.1007/s10482-004-5941-5

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