Skip to main content
Log in

Enzymes and coenzymes of the carbon monoxide dehydrogenase pathway for autotrophic CO2 fixation in Archaeoglobus lithotrophicus and the lack of carbon monoxide dehydrogenase in the heterotrophic A. profundus

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Archaeoglobus lithotrophicus is a hyperthermophilic Archaeon that grows on H2 and sulfate as energy sources and CO2 as sole carbon source. The autotrophic sulfate reducer was shown to contain all the enzyme activities and coenzymes of the reductive carbon monoxide dehydrogenase pathway for autotrophic CO2 fixation as operative in methanogenic Archaea. With the exception of carbon monoxide dehydrogenase these enzymes and coenzymes were also found in A. profundus. This organism grows lithotrophically on H2 and sulfate, but differs from A. lithotrophicus in that it cannot grow autotrophically: A. profundus requires acetate and CO2 for biosynthesis. The absence of carbon monoxide dehydrogenase in A. profundus is substantiated by the observation that this organism, in contrast to A. lithotrophicus, is not mini-methanogenic and contains only relatively low concentrations of corrinoids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

F 420 :

coenzyme F420

MFR :

methanofuran

CHO-MFR :

formylmethanofuran

H 4MPT:

5,6,7,8-tetrahydromethanopterin

CHO−H 4MPT N5 :

formyl-H4MPT

CH≡H4MPT+N5 :

methenyl-H4MPT

CH 2=H4MPT N5, N10 :

methylene-H4MPT

CH 3−H4MPT N5 :

methyl-H4MPT

H 4F:

tetrahydrofolate

I U :

1 μmol/min

t d :

doubling time

References

  • Achenbach-Richter L, Stetter KO, Woese CR (1987) A possible biochemical missing link among archaebacteria. Nature 327: 348–349

    CAS  PubMed  Google Scholar 

  • Bernt E, Bergmeyer HU (1974) Isocitrate-dehydrogenase. In: Bergmeyer HU (ed) Methoden der enzymatischen Analyse, vol 1. Chemie, Weinheim, pp 587–590

    Google Scholar 

  • Boone DR, Whitman WB, Rouvière P (1993) Diversity and taxonomy of methanogens. In: Ferry JG (ed) Methanogenesis, Chapman & Hall, New York London, pp 35–80

    Google Scholar 

  • Börner G, Karrasch M, Thauer RK (1989) Formylmethanofuran dehydrogenase activity in cell extracts of Methanobacterium thermoautotrophicum and of Methanosarcina barkeri. FEBS Lett 244:21–25

    Google Scholar 

  • Bott MH, Eikmanns B, Thauer RK (1985) Defective formation and/or utilization of carbon monoxide in H2/CO2 fermenting methanogens dependent on acetate as carbon source. Arch Microbiol 143:266–269

    CAS  Google Scholar 

  • Brandis A, Thauer RK (1981) Growth of Desulfovibrio species on hydrogen and sulphate as sole energy source. J Gen Microbiol 126:249–252

    CAS  Google Scholar 

  • Breitung J, Schmitz RA, Stetter KO, Thauer RK (1991) N 5,N10-Methenyltetrahydromethanopterin cyclohydrolase from the extreme thermophile Methanopyrus kandleri: increase of catalytic efficiency (kcat/KM) and thermostability in the presence of salts. Arch Microbiol 156:517–524

    CAS  Google Scholar 

  • Breitung J, Börner G, Scholz S, Linder D, Stetter KO, Thauer RK (1992) Salt dependence, kinetic properties and catalytic mechanism of N-formylmethanofuran: tetrahydromethanopterin formyltransferase from the exreme thermophile Methanopyrus kandleri. Eur J Biochem 210:971–981

    CAS  PubMed  Google Scholar 

  • Burggraf S, Jannasch HW, Nicolaus B, Stetter KO (1990) Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. System Appl Microbiol 13: 24–28

    Google Scholar 

  • Choquet CG, Richards JC, Patel GB, Sprott GD (1994) Purine and pyrimdine biosynthesis in methanogenic bacteria. Arch Microbiol 161:471–480

    CAS  Google Scholar 

  • Dahl C, Koch H-G, Keuken O, Trüper HG (1990) Purification and characterization of ATP sulfurylase from the extremely thermophilic archaebacterial sulfate-reducer, Archaeoglobus fulgidus. FEMS Microbiol Lett 67:27–32

    CAS  Google Scholar 

  • Dahl C, Kredich NM, Deutzmann R, Trüper HG (1993) Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physicochemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes. J Gen Microbiol 139:1817–1828

    CAS  PubMed  Google Scholar 

  • DiMarco AA, Bobik TA, Wolfe RS (1990) Unusual coenzymes of methanogenesis. Annu Rev Biochem 59:355–394

    CAS  PubMed  Google Scholar 

  • Donnelly MI, Wolfe RS (1986) The role of formylmethanofuran:terahydromethanopterin formyltransferase in methanogenesis from carbon dioxide. J Biol Chem 261:16653–16659

    CAS  PubMed  Google Scholar 

  • Ekiel I, Smith ICP, Sprott GD (1983) Biosynthetic pathways in Methanospirillum hungatei as determined by 13C nuclear magnetic resonance. J Bacteriol 156:316–326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ekiel I, Sprott GD, Patel GB (1985) Acetate and CO2 assimilation by Methanothrix concilii. J Bacteriol 162:905–908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Escalante-Semerena JC, Rinehart KL, Wolfe RS (1984) Tetrahydromethanopterin, a carbon carrier in methanogenesis. J Biol Chem 259:9447–9455

    CAS  PubMed  Google Scholar 

  • Feny JG (1993) Fermentation of acetate. In: Ferry JG (ed) Methanogenesis. Chapman & Hall, New York London, pp 304–334

    Google Scholar 

  • Fischer R, Gärtner P, Yeliseev A, Thauer RK (1992) N 5-Methyltetra-hydromethanopterin: coenzyme M methyltransferase in methanogenic archaebacteria is a membrane protein. Arch Microbiol 158:208–217

    CAS  PubMed  Google Scholar 

  • Friedrich B, Schwartz E (1993) Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu Rev Microbiol 47:351–383

    CAS  PubMed  Google Scholar 

  • Fuchs G (1989) Alternative pathways of autotrophic CO2 fixation. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, and Springer, Berlin New York, pp 365–382

    Google Scholar 

  • Gorris LGM, Voet ACWA, Drift C van der (1991) Structural characteristics of methanogenic cofactors in the non-methanogenic archaebacterium Archaeoglobus fulgidus. BioFactors 3:29–35

    CAS  PubMed  Google Scholar 

  • Grahame DA (1991) Catalysis of acetyl-CoA cleavage and tetrahydrosarcinapterin methylation by a carbon monoxide dehydrogenase-corrinoid enzhme complex. J Biol Chem 266: 22227–22233

    CAS  PubMed  Google Scholar 

  • Huber H, Thomm M, König H, Thies G, Stetter KO (1982) Methanococcus thermolithotrophicus, a novel thermophilic lithotrophic methanogen. Arch Microbiol 132:47–50

    Google Scholar 

  • Klein AR, Breitung J, Linder D, Stetter KO, Thauer RK (1993) N 5, N10-Methenyltetrahydromethanopterin cyclohydrolase from the extremely thermophilic sulfate reducing Archaeoglobus fulgidus: comparison of its properties with those of the cyclohydrolase from the extremely thermophilic Methanopyrus kandleri. Arch Microbiol 159:213–219

    CAS  PubMed  Google Scholar 

  • Kräutler B, Kohler H-PE, Stupperich E (1988) 5-Methylbenzimidazolyl-cobamides are the corrinoids from some sulfate-reducing and sulfur-metabolizing bacteria. Eur J Biochem 176:461–469

    PubMed  Google Scholar 

  • Krone UE, McFarlan SC, Hogenkamp HPC (1994) Purification and partial characterization of a putative thymidylate synthase from Methanobacterium thermoautotrophicum. Eur J Biochem 220:789–794

    CAS  PubMed  Google Scholar 

  • Kunow J, Schwörer B, Setzke E, Thauer RK (1993a) Si-face stereospecificity at C5 of coenzyme F420 for F420-dependent N 5, N10-methylenetetrahydromethanopterin dehydrogenase, F420-dependent N 5, N10-methylenetetrahydromethanopterin reductase and F420H2:dimethylnaphthoquinone oxidoreductase. Eur J Biochem 214:641–646

    CAS  PubMed  Google Scholar 

  • Kunow J, Schwörer B, Stetter KO, Thauer RK (1993b) A F420-dependent NADP reductase in the extremely thermophilic sulfate-reducing Archaeoglobus fulgidus. Arch Microbiol 160: 199–205

    CAS  Google Scholar 

  • Kunow J, Linder D, Stetter KO, Thauer RK (1994) F420H2:quinone oxidoreductase from Archaeoglobus fulgidus: characterization of a membrane-bound multisubunit complex containing FAD and iron-sulfur clusters. Eur J Biochem 223:503–511

    CAS  PubMed  Google Scholar 

  • Kurr M, Huber R, König H, Jannasch HW, Fricke H, Trincone A, Kristjansson JK, Stetter KO (1991) Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110°C. Arch Microbiol 156:239–247

    CAS  Google Scholar 

  • Lampreia J, Fauque G, Speich N, Dahl C, Moura I, Trüper HG, Moura JJG (1991) Spectroscopic studies on APS reductase isolated from the hyperthermophilic sulfate-reducing archaebacterium Archaeoglobus fulgidus. Biochem Biophys Res Commun 181:342–347

    CAS  PubMed  Google Scholar 

  • Länge S, Fuchs G (1987) Autotrophic synthesis of activated acetic acid from CO2 in Methanobacterium thermoautotrophicum. Eur J Biochem 163:147–154

    PubMed  Google Scholar 

  • Länge S, Scholtz R, Fuchs G (1989) Oxidative and reductive acetyl CoA/carbon monoxide dehydrogenase pathway in Desulfobacterium autotrophicum. Arch Microbiol 151:77–83

    Google Scholar 

  • Ma K, Thauer RK (1990) Purification and properties of N 5,N10-methylenetetrahydromethanopterin reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem 191:187–193

    CAS  PubMed  Google Scholar 

  • Möller-Zinkhan D, Thauer RK (1990) Anaerobic lactate oxidation to 3 CO2 by Archaeoglobus fulgidus via the carbon monoxide dehydrogenase pathway: demonstration of the acetyl-CoA carbon-carbon cleavage reaction in cell extracts. Arch Microbiol 153:215–218

    Google Scholar 

  • Möller-Zinkhan D, Börner G, Thauer RK (1989) Function of methanofuran, tetrahydromethanopterin, and coenzyme F420 in Archaeoglobus fulgidus. Arch Microbiol 152:362–368

    Google Scholar 

  • Peck HD (1993) Bioenergetic strategies of the sulfate-reducing bacteria. In: Odom JM, Singleton R (eds) The sulfate-reducing bacteria: contemporary perspectives. Springer, Berlin New York, pp 41–76

    Google Scholar 

  • Qiu D, Kumar M, Ragsdale SW, Spiro TG (1994) Nature's carbonylation catalyst: raman spectroscopic evidence that carbon monoxide binds to iron, not nickel, in CO dehydrogenase. Science 264:817–819

    CAS  PubMed  Google Scholar 

  • Ragsdale SW (1991) Enzymology of the acetyl-CoA pathway of CO2 fixation. Crit Rev Biochem Mol Biol 26:261–300

    CAS  PubMed  Google Scholar 

  • Schauder R, Eikmanns B, Thauer RK, Widdel F, Fuchs G (1986) Acetate oxidation to CO2 in anaerobic bacteria via a novel pathway not involving reactions of the citric acid cycle. Arch Microbiol 145:162–172

    CAS  Google Scholar 

  • Schauder R, Preuß A, Jetten M, Fuchs G (1989) Oxidative and reductive acetyl CoA/carbon monoxide dehydrogenase pathway in Desulfobacterium autotrophicum. 2. Demonstration of the enzymes of the pathway and comparison of CO dehydrogenase. Arch Microbiol 151:84–89

    CAS  Google Scholar 

  • Schmitz RA, Linder D, Stetter KO, Thauer RK (1991) N 5,N10-Methylenetetrahydromethanopterin reductase (coenzyme F420-dependent) and formylmethanofuran dehydrogenase from the hyperthermophile Archaeoglobus fulgidus. Arch Microbiol 156:427–434

    CAS  Google Scholar 

  • Schwörer B, Breitung J, Klein AR, Stetter KO, Thauer RK (1993) Formylmethanofuran:tetrahydromethanopterin formyltransferase and N 5,N10-methylenetetrahydromethanopterin dehydrogenase from the sulfate-reducing Archaeoglobus fulgidus: similarities with the enzymes from methanogenic Archaea. Arch Microbiol 159:225–232

    PubMed  Google Scholar 

  • Setzke E, Hedderich R, Heiden S, Thauer RK (1994) H2:heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum: composition and properties. Eur J Biochem 220:139–148

    CAS  PubMed  Google Scholar 

  • Smith L (1978) Bacterial cytochromes and their spectral characterization. In: Fleischer S, Packer L (eds) Biomembranes Methods Enzymol 53:202–212

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goecke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    CAS  PubMed  Google Scholar 

  • Speich N, Trüper HG (1988) Adenylylsulphate reductase in a dissimilatory sulphate-reducing archaebacterium. J Gen Microbiol 134:1419–1425

    CAS  Google Scholar 

  • Speich N, Dahl N, Heisig P, Klein A, Lottspeich F, Stetter KO, Trüper HG (1994) Adenylylsulfate reductase from the sulfate-reducing archaeon Archaeoglobus fulgidus: cloning and characterization of the genes and comparison of the enzyme with other iron-sulphur flavoproteins. Microbiology 140:1273–1284

    CAS  PubMed  Google Scholar 

  • Stetter KO (1988) Archaeoglobus fulgidus gen. nov., sp. nov.: a new taxon of extremely thermophilic archaebacteria. System Appl Microbiol 10:171–173

    Google Scholar 

  • Stetter KO (1992) The genus Archaeoglobus. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes, 2nd edn, vol 1. Springer, Berlin New York, pp 707–711

    Google Scholar 

  • Stetter KO, Lauerer G, Thomm M, Neuner A (1987) Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of Archaebacteria. Science 236:822–824

    CAS  PubMed  Google Scholar 

  • Stetter KO, Huber R, Blöchl E, Kurr M, Eden RD, Fleider M, Cash H, Vance I (1993) Hyperthermophilic archaea are thriving in deep North Sea and Alaskan oil reservoirs. Nature 365: 743–745

    Google Scholar 

  • Terlesky KC, Nelson MJK, Ferry JG (1986) Isolation of an enzyme complex with carbon monoxide dehydrogenase activity containing corrinoid and nickel from acetate-grown Methanosarcina thermophila. J Bacteriol 168:1053–1058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thauer RK, Kunow J (1994) Sulfate-reducing Archaea. In: Barton LL (ed) Biotechnology handbooks: sulfate-reducing bacteria. Plenum, New York London Washington (in press)

    Google Scholar 

  • Thauer RK, Möller-Zinkhan D, Spormann AM (1989) Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Annu Rev Microbiol 43:43–67

    CAS  PubMed  Google Scholar 

  • Tindall BJ, Stetter KO, Collins MD (1989) A novel, fully saturated menaquinone from the thermophilic sulphate-reducing Archaebacterium Archaeoglobus fulgidus. J Gen Microbiol 135:693–696

    CAS  Google Scholar 

  • Weimer PJ, Zeikus JG (1979) Acetate assimilation pathway of Methanosarcina barkeri. J Bacteriol 137:332–339

    CAS  PubMed  PubMed Central  Google Scholar 

  • White RH (1988) Structural diversity among methanofurans from different methanogenic bacteria. J Bacteriol 170:4594–4597

    CAS  PubMed  PubMed Central  Google Scholar 

  • White RH (1991) Distribution of folates and modified folates in extremely thermophilic bacteria. J Bacteriol 173:1987–1991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Widdel F (1988) Microbiology and ecology of sulfate-and sulfureducing bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 469–585

    Google Scholar 

  • Woese CR, Achenbach L, Rouvière P, Mandelco L (1991) Archaeal phylogeny: reexamination of the phylogenetic position of Archaeoglobus fulgidus in light of certain composition-induced artifacts. System Appl Microbiol 14:364–371

    CAS  Google Scholar 

  • Zeikus JG, Fuchs G, Kenealy W, Thauer RK (1977) Oxidoreductases involved in cell carbon synthesis of Methanobacterium thermoautotrophicum. J Bacteriol 132:604–613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zellner G, Stackebrandt E, Kneifel H, Messner P, Sleytr UB, Conway de Macario E, Zabel H-P, Stetter KO, Winter J (1989) Isolation and characterization of a thermophilic, sulfate reducing archaebacterium, Archaeoglobus fulgidus strain Z. System Appl Microbiol 11:151–160

    CAS  Google Scholar 

  • Zirngibl C, Hedderich R, Thauer RK (1990) N 5,N10-Methylenetetrahydromethanopterin dehydrogenase from Methanobacterium thermoautotrophicum has hydrogenase activity. FEBS Lett 261:112–116

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vorholt, J., Kunow, J., Stetter, K.O. et al. Enzymes and coenzymes of the carbon monoxide dehydrogenase pathway for autotrophic CO2 fixation in Archaeoglobus lithotrophicus and the lack of carbon monoxide dehydrogenase in the heterotrophic A. profundus. Arch. Microbiol. 163, 112–118 (1995). https://doi.org/10.1007/BF00381784

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00381784

Key words

Navigation