Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Autotrophic carbon fixation in archaea

Nature Reviews Microbiology volume 8, pages 447–460 (2010)Cite this article

Subjects

Key Points

  • The Archaea form the third domain of life alongside the other two domains, the Bacteria and Eukarya. Most cultivated autotrophic archaea live under conditions resembling the conditions of early life (no oxygen, high temperature and purely inorganic substrates), and their autotrophic pathways can serve as models for an ancestral metabolism.

  • None of the autotrophic archaea seems to use the Calvin cycle for CO2 fixation. Instead, they use three different CO2 fixation mechanisms to generate acetyl-coenzyme A (acetyl-CoA), from which the biosynthesis of building blocks can start.

  • The reductive acetyl-CoA pathway function in Euryarchaeota, notably in methanogens, and has the lowest energetic costs among the autotrophic CO2 fixation pathways. However, the demanding requirements for metals, cofactors, anaerobiosis and substrates with low reducing potential restrict this pathway to a limited set of anoxic niches.

  • Two recently discovered cycles function in Crenarchaeota, the dicarboxylate–hydroxybutyrate cycle and the hydroxypropionate–hydroxybutyrate cycle. They have in common the synthesis of succinyl-CoA from acetyl-CoA and two inorganic carbons, although this is accomplished in different ways and using different carboxylases. However, the regeneration of acetyl-CoA, the primary CO2 acceptor, from succinyl-CoA is similar in both pathways.

  • The oxygen-sensitive dicarboxylate–hydroxybutyrate cycle is restricted to the anaerobic Thermoproteales and Desulfurococcales, whereas the oxygen-insensitive hydroxypropionate–hydroxybutyrate cycle is restricted to the mostly aerobic Sulfolobales and possibly marine Crenarchaeota. The two lifestyles presuppose different electron donors with different redox potentials and different oxygen sensitivity of cofactors and enzymes.

  • The distribution of an autotrophic pathway in bacteria and archaea depends on both the genetic predisposition (phylogeny) of the organisms and the constraints of their occupied niches (ecology). The main external factors are the presence of oxygen in the environment, but also the availability of trace metals and C1 compounds. The energy demand of the autotrophic pathways is decisive under energy limitation and caused mainly by the costs for synthesizing autotrophy-related auxiliary enzymes. Further determinants are the main metabolic fluxes in an organism, the usage of CO2 or HCO3− by the carboxylases of the pathway and the possibility of co-assimilating traces of organic compounds present in the environment.

  • According to the 'metabolism first' theory, life started in a hydrothermal vent setting in the Hadean ocean with catalytic metal sulphide surfaces or compartments. The structural (and catalytic) similarity between the minerals themselves and the catalytic metal or Fe–S-containing centres of the enzymes or cofactors in the acetyl-CoA pathway suggests that minerals catalysed a primitive acetyl-CoA pathway. The unique features of this pathway indeed indicate that it might be close to an ancestral autotrophic carbon fixation mechanism.

  • Recently a highly conserved, heat-stabile and bifunctional fructose 1,6-bisphosphate aldolase–phosphatase was identified in archaea and deep-branching lineages of bacteria. This enzyme is regarded as the pace-making ancestral gluconeogenic enzyme. The finding supports the idea that in evolution gluconeogenesis preceded glycolysis. The distribution pattern of this enzyme, its phylogenetic tree and the unidirectional catalysis lend further support to the theory of a chemolithoautotrophic origin of life.

Abstract

The acquisition of cellular carbon from inorganic carbon is a prerequisite for life and marked the transition from the inorganic to the organic world. Recent theories of the origins of life assume that chemoevolution took place in a hot volcanic flow setting through a transition metal-catalysed, autocatalytic carbon fixation cycle. Many archaea live in volcanic habitats under such constraints, in high temperatures with only inorganic substances and often under anoxic conditions. In this Review, we describe the diverse carbon fixation mechanisms that are found in archaea. These reactions differ fundamentally from those of the well-known Calvin cycle, and their distribution mirrors the phylogenetic positions of the archaeal lineages and the needs of the ecological niches that they occupy.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The phylogenetic (unrooted) tree of Archaea.
Figure 2: The reductive acetyl-coenzyme A pathway.
Figure 3: Pathways of autotrophic CO2 fixation in Crenarchaeota.
Figure 4: Central carbohydrate metabolism in archaea.

Similar content being viewed by others

References

  1. Garrity, G. M. & Holt, J. G. Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 1 (eds Boone, D. R., Castenholz, R. W. & Garrity, G. M.) 119–166 (Springer, New York, 2001).

    Book  Google Scholar 

  2. Stetter, K. O. History of discovery of the first hyperthermophiles. Extremophiles 10, 357–362 (2006).

    Article  PubMed  Google Scholar 

  3. Sapra, R., Bagramyan, K. & Adams, M. W. A simple energy-conserving system: proton reduction coupled to proton translocation. Proc. Natl Acad. Sci. USA 100, 7545–7550 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hedderich, R. & Forzi, L. Energy-converting [NiFe] hydrogenases: more than just H2 activation. J. Mol. Microbiol. Biotechnol. 10, 92–104 (2005).

    Article  CAS  PubMed  Google Scholar 

  5. Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nature Rev, Microbiol. 6, 579–591 (2008).

    Article  CAS  Google Scholar 

  6. Taylor, G. T., Kelly, D. P. & Pirt, S. J. in Microbial Production and Utilization of Gases (eds Schlegel, H. G., Gottschalk, G. & Pfennig, N.) 173–180 (E. Goltze, K. G., Göttingen, 1976).

    Google Scholar 

  7. Ljungdahl, L. G. The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu. Rev. Microbiol. 40, 415–450 (1986).

    Article  CAS  PubMed  Google Scholar 

  8. Wood, H. G. Life with CO or CO2 and H2 as a source of carbon and energy. FASEB J. 5, 156–163 (1991).

    Article  CAS  PubMed  Google Scholar 

  9. Drake, H. L., Göβner, A. S. & Daniel, S. L. Old acetogens, new light. Ann. N. Y. Acad. Sci. 1125, 100–128 (2008).

    Article  CAS  PubMed  Google Scholar 

  10. Ragsdale, S. W. Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann. N. Y. Acad. Sci. 1125, 129–136 (2008).

    CAS  Google Scholar 

  11. Vorholt, J. A., Kunow, J., Stetter, K. O. & Thauer, R. K. 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).

    Article  CAS  Google Scholar 

  12. Vorholt, J. A., Hafenbradl, D., Stetter, K. O. & Thauer, R. K. Pathways of autotrophic CO2 fixation and of dissimilatory nitrate reduction to N2O in Ferroglobus placidus. Arch. Microbiol. 167, 19–23 (1997).

    Article  CAS  PubMed  Google Scholar 

  13. Huber, H. et al. A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic archaeum Ignicoccus hospitalis. Proc. Natl Acad. Sci. USA 105, 7851–7856 (2008). Reports the discovery of a dicarboxylate–hydroxybutyrate cycle in the archaeal order Desulfurococcales.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ramos-Vera, W. H., Berg, I. A. & Fuchs, G. Autotrophic carbon dioxide assimilation in Thermoproteales revisited. J. Bacteriol. 191, 4286–4297 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Berg, I. A., Ramos-Vera, W. H., Petri, A., Huber, H. & Fuchs, G. Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota. Microbiology 156, 256–269 (2010).

    Article  CAS  PubMed  Google Scholar 

  16. Huber, H., Huber, R. & Stetter, K. O. in The Prokaryotes, 3rd ed., vol. 3 (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.), 10–22 (Springer, New York, 2006).

    Book  Google Scholar 

  17. Huber, H. & Stetter, K. O. in The Prokaryotes, 3rd ed., vol. 3 (eds. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.), 52–68 (Springer, New York, 2006).

    Book  Google Scholar 

  18. Patel, H. M., Kraszewski, J. L. & Mukhopadhyay, B. The phosphoenolpyruvate carboxylase from Methanothermobacter thermoautotrophicus has a novel structure. J. Bacteriol. 186, 5129–5137 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ettema, T. J. G. et al. Identification and functional verification of archaeal-type phosphoenolpyruvate carboxylase, a missing link in archaeal central carbohydrate metabolism. J. Bacteriol. 186, 7754–7762 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Strauss, G., Eisenreich, W., Bacher, A. & Fuchs, G. 13C-NMR study of autotrophic CO2 fixation pathways in the sulphur-reducing archaebacterium Thermoproteus neutrophilus and in the phototrophic eubacterium Chloroflexus aurantiacus. Eur. J. Biochem. 205, 853–866 (1992).

    Article  CAS  PubMed  Google Scholar 

  21. Buckel, W. & Golding, G. T. Radical enzymes in anaerobes. Annu. Rev. Microbiol. 60, 27–49 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Martins, B. M., Dobbek, H., Cinkaya, I., Buckel, W. & Messerschmidt, A. Crystal structure of 4-hydroxybutyryl-CoA dehydratase: radical catalysis involving a [4Fe-4S] cluster and flavin. Proc. Natl Acad. Sci. USA 101, 15645–15649 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ishii, M. et al. Autotrophic carbon dioxide fixation in Acidianus brierleyi. Arch. Microbiol. 166, 368–371 (1997). First report of the presence of a modified 3-hydroxypropionate cycle in Archaea.

    Article  Google Scholar 

  24. Menendez, C. et al. Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J. Bacteriol. 181, 1088–1098 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Berg, I. A., Kockelkorn, D., Buckel, W. & Fuchs, G. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782–1786 (2007). Reports the discovery of a hydroxypropionate–hydroxybutyrate cycle in Sulfolobales.

    Article  CAS  PubMed  Google Scholar 

  26. Huber, H. & Prangishvili, D. in The Prokaryotes, 3rd ed., vol. 3 (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.), 23–51 (Springer, New York, 2006).

    Book  Google Scholar 

  27. Auernik, K. S., Cooper, C. R. & Kelly, R. M. Life in hot acid: pathway analyses in extremely thermoacidophilic archaea. Curr. Opin. Biotechnol. 19, 445–453 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hallam, S. J. et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Norris, P., Nixon, A. & Hart, A. Microbiology of Extreme Environments and its Potential for Biotechnology (eds Da Costa, M. S., Duarte, J. C. & Williams, R. A. D.) 24–43 (Elsevier, London, 1989). First report on the presence of an acetyl-CoA carboxylase in Archaea.

    Google Scholar 

  31. Burton, N. P., Williams, T. D. & Norris, P. R. Carboxylase genes in Sulfolobus metallicus. Arch. Microbiol. 172, 349–353 (1999).

    Article  CAS  PubMed  Google Scholar 

  32. Hügler, M., Krieger, R. S., Jahn, M. & Fuchs, G. Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula. Carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur. J. Biochem. 270, 736–744 (2003).

    Article  CAS  PubMed  Google Scholar 

  33. Chuakrut, S., Arai, H., Ishii, M. & Igarashi, Y. Characterization of a bifunctional archaeal acyl coenzyme A carboxylase. J. Bacteriol. 185, 938–947 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Alber, B. et al. Malonyl-coenzyme A reductase in the modified 3-hydroxypropionate cycle for autotrophic carbon fixation in archaeal Metallosphaera and Sulfolobus spp. J. Bacteriol. 188, 8551–8559 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kockelkorn, D. & Fuchs, G. Malonic semialdehyde reductase, succinic semialdehyde reductase, and succinyl-coenzyme A reductase from Metallosphaera sedula: enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in Sulfolobales. J. Bacteriol. 191, 6352–6362 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Alber, B. E., Kung, J. W. & Fuchs, G. 3-Hydroxypropionyl-coenzyme A synthetase from Metallosphaera sedula, an enzyme involved in the autotrophic CO2 fixation. J. Bacteriol. 190, 1383–1389 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Teufel, R., Kung, J. W., Kockelkorn, D., Alber, B. E. & Fuchs, G. 3-Hydroxypropionyl-coenzyme A dehydratase and acryloyl-coenzyme A reductase, enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in Sulfolobales. J. Bacteriol. 191, 4572–4581 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Holo, H. Chloroflexus aurantiacus secretes 3-hydroxypropionate, a possible intermediate in the assimilation of CO2 and acetate. Arch. Microbiol. 151, 252–256 (1989). First hint of the role of 3-hydroxypropionate in autotrophic carbon fixation.

    Article  CAS  Google Scholar 

  39. Strauss, G. & Fuchs, G. Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur. J. Biochem. 215, 633–643 (1993).

    Article  CAS  PubMed  Google Scholar 

  40. Herter, S., Fuchs, G., Bacher, A. & Eisenreich, W. A bicyclic autotrophic CO2 fixation pathway in Chloroflexus aurantiacus. J. Biol. Chem. 277, 20277–20283 (2002).

    Article  CAS  PubMed  Google Scholar 

  41. Alber, B. E. & Fuchs, G. Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J. Biol. Chem. 277, 12137–12143 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Hügler, M., Menendez, C., Schägger, H. & Fuchs, G. Malonyl-coenzyme A reductase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J. Bacteriol. 184, 2404–2410 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zarzycki, J., Brecht, V., Müller, M. & Fuchs, G. Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc. Natl Acad. Sci. USA 106, 21317–21322 (2009). Shows the final steps of the 3-hydroxypropionate bicycle.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Eyzaguirre, J., Jansen, K. & Fuchs, G. Phosphoenolpyruvate synthetase in Methanobacterium thermoautotrophicum. Arch. Microbiol. 132, 67–74 (1982).

    Article  CAS  Google Scholar 

  45. Tjaden, B., Plagens, A., Dörr, C., Siebers, B. & Hensel, R. Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism. Mol. Microbiol. 60, 287–298 (2006).

    Article  CAS  PubMed  Google Scholar 

  46. Fuchs, G., Winter, H., Steiner, I. & Stupperich, E. Enzymes of gluconeogenesis in the autotroph Methanobacterium thermoautotrophicum. Arch. Microbiol. 136, 160–162 (1983).

    Article  CAS  Google Scholar 

  47. Jahn, U., Huber, H., Eisenreich, W., Hügler, M. & Fuchs, G. Insights into the autotrophic CO2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism. J. Bacteriol. 189, 4108–4119 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Schäfer, S., Barkowski, C. & Fuchs, G. Carbon assimilation by the autotrophic thermophilic archaebacterium Thermoproteus neutrophilus. Arch. Microbiol. 146, 301–308 (1986).

    Article  Google Scholar 

  49. Lorentzen, E., Siebers, B., Hensel, R. & Pohl, E. Mechanism of the Schiff base forming fructose-1, 6-bisphosphate aldolase: structural analysis of reaction intermediates. Biochemistry 44, 4222–4229 (2005).

    Article  CAS  PubMed  Google Scholar 

  50. Rashid, N. et al. A novel candidate for the true fructose-1,6-bisphosphatase in archaea. J. Biol. Chem. 277, 30649–30655 (2002).

    Article  CAS  PubMed  Google Scholar 

  51. Say, R. S. & Fuchs, G. Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077–1081 (2010) Discovery of the bifunctional FBP aldolase–phosphatase.

    Article  CAS  PubMed  Google Scholar 

  52. Van der Oost, J. & Siebers, B. in Archaea: Evolution, Physiology and Molecular Biology (eds Garrett, R. A. & Klenk, H.-P.) 247–259 (Blackwell, Malden, Massachusetts, 2007).

    Google Scholar 

  53. Siebers, B. & Schönheit, P. Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr. Opin. Microbiol. 8, 695–705 (2005).

    Article  CAS  PubMed  Google Scholar 

  54. Ronimus, R. S. & Morgan, H. W. Distribution and phylogenies of enzymes of the Embden-Meyerhof-Parnas pathway from archaea and hyperthermophilic bacteria support a gluconeogenic origin of metabolism. Archaea 1, 199–221 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Soderberg, T. Biosynthesis of ribose-5-phosphate and erythrose-4-phosphate in archaea: a phylogenetic analysis of archaeal genomes. Archaea 1, 347–352 (2005).

    Article  CAS  PubMed  Google Scholar 

  56. Grochowski, L. L., Xu, H. & White, R. H. Ribose-5-phosphate biosynthesis in Methanocaldococcus jannaschii occurs in the absence of a pentose-phosphate pathway. J. Bacteriol. 187, 7382–7389 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Orita, I. et al. The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon Thermococcus kodakaraensis. J. Bacteriol. 188, 4698–4704 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kato, N., Yurimoto, H. & Thauer, R. K. The physiological role of the ribulose monophosphate pathway in bacteria and archaea. Biosci. Biotechnol. Biochem. 70, 10–21 (2006).

    Article  CAS  PubMed  Google Scholar 

  59. Grochowski, L. L. & White, R. H. Promiscuous anaerobes: new and unconvensional metabolism in methanogenic Archaea. Ann. N. Y. Acad. Sci. 1125, 190–214 (2008).

    CAS  Google Scholar 

  60. Auernik, K. S., Maezato, Y., Blum, P. H. & Kelly, R. M. The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl. Environ. Microbiol. 74, 682–692 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Podar, M. et al. A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol. 9, R158 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Auernik, K. S. & Kelly, R. M. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by heterotrophy, autotrophy and mixotrophy transcriptomes. Appl. Environ. Microbiol. 76, 2268–2672 (2010).

    Google Scholar 

  63. Zaparty, M. et al. DNA microarray analysis of central carbohydrate metabolism: glycolytic/gluconeogenic carbon switch in the hyperthermophilic crenarchaeum Thermoproteus tenax. J. Bacteriol. 190, 2231–2238 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chong, P. K., Burja, A. M., Radianingtyas, H., Fazeli, A. & Wright, P. C. Proteome and transcriptional analysis of ethanol-grown Sulfolobus solfataricus P2 reveals ADH2, a potential alcohol dehydrogenase. J. Proteome Res. 6, 3985–3994 (2007).

    Article  CAS  PubMed  Google Scholar 

  65. DeLong, E. F. & Karl, D. M. Genomic perspectives in microbial oceanography. Nature 437, 336–342 (2005).

    Article  CAS  PubMed  Google Scholar 

  66. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, e77 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Schleper, C., Jurgens, G. & Jonuscheit, M. Genomic studies of uncultivated archaea. Nature Rev. Microbiol. 3, 479–488 (2005).

    Article  CAS  Google Scholar 

  68. Allen, E. E. et al. Genome dynamics in a natural archaeal population. Proc. Natl Acad. Sci. USA 104, 1883–1888 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ferrer, M., Golyshina, O. V., Beloqui, A., Golyshin, P. N. & Timmis, K. N. The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated. Nature 445, 91–94 (2007).

    Article  CAS  PubMed  Google Scholar 

  70. Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hu, Y. & Holden, J. F. Citric acid cycle in the hyperthermophilic archaeon Pyrobaculum islandicum grown autotrophically, heterotrophically, and mixotrophically with acetate. J. Bacteriol. 188, 4350–4355 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Tabita, F. R. et al. Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71, 576–599 (2008). Excellent review concerning the evolution of RubisCO and RLPs proposing their archaeal origins.

    Article  CAS  Google Scholar 

  73. Ashida, H. et al. RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO. J. Exp. Bot. 59, 1543–1554 (2008).

    Article  CAS  PubMed  Google Scholar 

  74. Imker, H. J., Singh, J., Warlick, B. P., Tabita, F. R. & Gerlt, J. A. Mechanistic diversity in the RuBisCO superfamily: a novel isomerization reaction catalyzed by the RuBisCO-like protein from Rhosdospirillum rubrum. Biochemistry 47, 11171–11173 (2008).

    Article  CAS  PubMed  Google Scholar 

  75. Maeda, N., Kanai, T., Atomi, H. & Imanaka, T. The unique pentagonal structure of an archaeal RuBisCO is essential for its high thermostability. J. Biol. Chem. 277, 31656–31662 (2002).

    Article  CAS  PubMed  Google Scholar 

  76. Finn, M. W. & Tabita, F. R. Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. J. Bacteriol. 185, 3049–3059 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Finn, M. W. & Tabita, F. R. Modified pathway to synthesize ribulose 1,5-bisphosphate in methanogenic Archaea. J. Bacteriol. 186, 6360–6366 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kreel, N. E. & Tabita, F. R. Substitutions at methionine 295 of Archaeoglobus fulgidus ribulose-1,5-bisphosphate carboxylase/oxygenase affect oxygen binding and CO2/O2 specificity. J. Biol. Chem. 282, 1341–1351 (2007).

    Article  CAS  PubMed  Google Scholar 

  79. Sato, T., Atomi, H. & Imanaka, T. Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315, 1003–1006 (2007).

    Article  CAS  PubMed  Google Scholar 

  80. Mueller-Cajar, O. & Badger, M. R. New roads lead to RuBiscO in Archaebacteria. BioEssays 29, 722–724 (2007).

    Article  CAS  PubMed  Google Scholar 

  81. Reysenbach, A. L. & Flores, G. E. Electron microscopy encounters with unusual thermophiles helps direct genomic analysis of Aciduliprofundum boonei. Geobiology 6, 331–336 (2008).

    Article  CAS  PubMed  Google Scholar 

  82. Klenk, H.P. et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).

    Article  CAS  PubMed  Google Scholar 

  83. Fuchs, G. in Biology of Autotrophic Bacteria (ed. Schlegel, H. G.) 365–382 (Science Tech., Madison, Wisconsin, 1989).

    Google Scholar 

  84. Wächtershäuser, G. Evolution of the first metabolic cycles. Proc. Natl Acad. Sci. USA 87, 200–204 (1990).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Russell, M. J. & Martin, W. The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29, 358–363 (2004). Detailed discussion of the idea that acetyl-CoA pathway is an initial biochemical route.

    Article  CAS  PubMed  Google Scholar 

  86. Makarova, K. S., Sorokin, A. V., Novichkov, P. S., Wolf, Y. I. & Koonin, E. V. Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol. Direct 2, 33 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Fuchs, G., Stupperich, E. & Thauer, R. K. Acetate assimilation and the synthesis of alanine, aspartate and glutamate in Methanobacterium thermoautotrophicum. Arch. Microbiol. 117, 61–66 (1978).

    Article  CAS  PubMed  Google Scholar 

  88. Ragsdale, S. W. Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem. Rev. 103, 2333–2346 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Wächtershäuser, G. On the chemistry and evolution of the pioneer organism. Chem. Biodivers. 4, 584–602 (2007). The last update of Wächtershäuser's iron–sulphur world' theory of the chemolithoautotrophic origin of life.

    Article  PubMed  Google Scholar 

  90. Wächtershäuser, G. Before enzymes and templates: theory of surface metabolism. Microbiol. Rev. 52, 452–484 (1988). Discusses the basic concept of surface metabolism.

    PubMed  PubMed Central  Google Scholar 

  91. Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nature Rev. Microbiol. 6, 805–814 (2008).

    Article  CAS  Google Scholar 

  92. Huber, C. & Wächtershäuser, G. Activated acetic acid by carbon fixation on (Fe, Ni)S under primordial conditions. Science 276, 245–247 (1997).

    Article  CAS  PubMed  Google Scholar 

  93. Eschenmoser, A. Vitamin B12: experiments concerning the origin of its molecular structure. Angew. Chem. Int. Ed. Engl. 27, 5–39 (1988).

    Article  Google Scholar 

  94. Schauder, R., Preuβ, A., Jetten, M. & Fuchs, G. 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 (1989).

    Article  CAS  Google Scholar 

  95. Thauer, R. K., Möller-Zinkhan, D. & Spormann, A. M. Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Annu. Rev. Microbiol. 43, 43–67 (1989).

    Article  CAS  PubMed  Google Scholar 

  96. Hattori, S., Galushko, A. S., Kamagata, Y. & Schink, B. Operation of the CO dehydrogenase/acetyl coenzyme A pathway in both acetate oxidation and acetate formation by the syntrophically acetate-oxidizing bacterium Thermacetogenium phaeum. J. Bacteriol. 187, 3471–3476 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Cody, G. D. et al. Geochemical roots of autotrophic carbon fixation: hydrothermal experiments in the system citric acid, H2O-(±FeS)-(±NiS). Geochim. Cosmochim. Acta 65, 3557–3576 (2001).

    Article  CAS  Google Scholar 

  98. Smith, E. & Morowitz, H. J. Universality in intermediary metabolism. Proc. Natl Acad. Sci. USA 101, 13168–13173 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Eschenmoser, A. The search for the chemistry of life. Tetrahedron 63, 12821–12844 (2007).

    Article  CAS  Google Scholar 

  100. Kummer, C. Der Glaube der Christen. Ein ökumenisches Handbuch (eds Biser, E., Hahn, F. & Langer, M.) 25–44 (Pattloch Verlag, Munich, 1999).

    Google Scholar 

  101. Dagan, T., Artzy-Randrup, Y. & Martin, W. Modular networks and cumulative impact of lateral gene transfer in prokaryote genome evolution. Proc. Natl Acad. Sci. USA 105, 10039–10044 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Zhaxybayeva, O. et al. On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc. Natl Acad. Sci. USA 106, 5865–5870 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Bassham, J. A. & Calvin, M. The Path of Carbon in Photosynthesis (Prentice Hall, Englewood Cliffs, 1957).

    Google Scholar 

  104. Evans, M. C. W., Buchanan, B. B. & Arnon, D. I. A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc. Natl Acad. Sci. USA 55, 928–934 (1966).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Tcherkez, G. G., Farquhar, G. D. & Andrews, T. J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl Acad. Sci. USA 103, 7246–7251 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ellis, R. J. The most abundant protein on Earth. Trends Biochem. Sci. 4, 241–244 (1979).

    Article  CAS  Google Scholar 

  107. Keeley, J. E. & Rundel, P. W. Evolution of CAM and C4 carbon-concentrationg mechanisms. Int. J. Plant Sci. 164, S55–S77 (2003).

    Article  CAS  Google Scholar 

  108. Todd, J. D. et al. Molecular dissection of bacterial acrylate catabolism - unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Environ. Microbiol. 12, 327–343 (2010)

    Article  CAS  PubMed  Google Scholar 

  109. Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Brochier, C., Gribaldo, S., Zivanovic, Y., Confalonieri, F. & Forterre, P. Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol. 6, R42 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaea: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Rev. Microbiol. 6, 245–252 (2008).

    Article  CAS  Google Scholar 

  112. Robertson, C. E., Harris, J. K., Spear, J. R. & Pace, N. R. Phylogenetic diversity and ecology of environmental Archaea. Curr. Opin. Microbiol. 8, 638–642 (2005).

    Article  CAS  PubMed  Google Scholar 

  113. Quandt, L., Gottschalk, G., Ziegler, H. & Stichler, W. Isotope discrimination by photosynthetic bacteria. FEMS Microbiol. Lett. 1, 125–128 (1977).

    Article  CAS  Google Scholar 

  114. McNevin, D. B. et al. Differences in carbon isotope discrimination of three variants of D-ribulose-1,5-bisphosphate carboxylase/oxygenase reflect differences in their catalytic mechanisms. J. Biol. Chem. 282, 36068–36076 (2007).

    Article  CAS  PubMed  Google Scholar 

  115. Sirevåg, R., Buchanan, B. B., Berry, J. A. & Troughton, J. H. Mechanisms of CO2 fixation in bacterial photosynthesis studied by the carbon isotope fractionation technique. Arch. Microbiol. 112, 35–38 (1977).

    Article  PubMed  Google Scholar 

  116. Preub, A., Schauder, R. & Fuchs, G. Carbon isotope fractionation by autotrophic bacteria with three different CO2 fixation pathways. Z. Naturforsch. 44c, 397–402 (1989).

    Google Scholar 

  117. House, C. H. et al. Carbon isotopic composition of individual Precambrian microfossils. Geology 28, 707–710 (2000).

    Article  CAS  PubMed  Google Scholar 

  118. Holo, H. & Sirevåg, R. Autotrophic growth and CO2 fixation in Chloroflexus aurantiacus. Arch. Microbiol. 145, 173–180 (1986).

    Article  CAS  Google Scholar 

  119. Ivanovsky, R. N. et al. Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. Microbiology 145, 1743–1748 (1999).

    Article  CAS  PubMed  Google Scholar 

  120. van der Meer, M. T., Schouten, S., de Leeuw, J. W. & Ward, D. M. Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record. Environ. Microbiol. 2, 428–435 (2000).

    Article  CAS  PubMed  Google Scholar 

  121. House, C. H., Schopf, J. W. & Stetter, K. O. Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org. Geochem. 34, 345–356 (2003).

    Article  CAS  Google Scholar 

  122. Aoshima, M., Ishii, M. & Igarashi, Y. A novel biotin protein required for reductive carboxylation of 2-oxoglutarate by isocitrate dehydrogenase in Hydrogenobacter thermophilus TK-6. Mol. Microbiol. 51, 791–798 (2004).

    Article  CAS  PubMed  Google Scholar 

  123. Miura, A., Kameya, M., Arai, H., Ishii, M. & Igarashi, Y. A soluble NADH-dependent fumarate reductase in the reductive citric acid cycle of Hydrogenobacter thermophilus TK-6. J. Bacteriol. 190, 7170–7177 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

G. F. acknowledges the contributions of numerous doctoral or postdoctoral students during the past 30 years: E. Stupperich, G. Eden and K. Jansen (Marburg); M. Rühlemann, S. Länge, R. Schauder, S. Schäfer and G. Strauβ (Ulm); and S. Herter, S. Friedmann and C. Menendez (Freiburg). Our work depended on fruitful collaborations with W. Eisenreich, A. Bacher, H. Huber, K. Stetter, M. Müller, W. Buckel and R. Thauer. This work was supported by Deutsche Forschungsgemeinschaft and Evonik–Degussa. Thanks to M. Ziemski for the database analysis that was used as the basis for Fig. 1.

Author information

Author notes

  1. Michael Hügler

    Present address: Present address: Water Technology Center (TZW), Karlsruher Strasse 84, D-76139 Karlsruhe, Germany.,

  2. Birgit E. Alber

    Present address: Present address: The Ohio State University, Department of Microbiology, 484 West 12th Avenue, 417A Biological Science Building, Columbus, Ohio 43210-1292, USA.,

Authors and Affiliations

  1. Mikrobiologie, Fakultät Biologie, Universität Freiburg, Schänzlestrasse 1, D-79104, Freiburg, Germany

    Ivan A. Berg, Daniel Kockelkorn, W. Hugo Ramos-Vera, Rafael F. Say, Jan Zarzycki, Michael Hügler, Birgit E. Alber & Georg Fuchs

Authors
  1. Ivan A. Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Kockelkorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. Hugo Ramos-Vera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rafael F. Say
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jan Zarzycki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Hügler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Birgit E. Alber
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Georg Fuchs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Georg Fuchs.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez Genome Project

Aciduliprofundum boonei

Ammonifex degensii

Archaeoglobus fulgidus

Chloroflexus aurantiacus

Ferroglobus placidus

Metallosphaera sedula

Methanosaeta thermophila

Pyrobaculum arsenaticum

Pyrobaculum islandicum

Thermoproteus neutrophilus

FURTHER INFORMATION

DOE Joint Genome Institute website

Georg Fuchs' homepage

Glossary

Thermophilic

An organism that grows best at temperatures exceeding the ambient temperature. Extreme thermophiles (hyperthermophiles) have optimal growth temperatures above 80 °C.

Chemolithoautotroph

An organism that derives energy from a chemical reaction (chemotrophic) based on inorganic substrates as electron donors (lithotrophic), and CO2 serves as sole carbon source (autotrophic = self-nourishing).

Monsanto process

An important method for the manufacture of acetic acid. The feedstock methanol is combined catalytically with CO to give acetic acid. The reaction is catalysed by a metal (rhodium) catalyst. Methanol reacts with catalytic amounts of HI to give methyl iodide. The reaction cycle is completed by the loss of CH3COI to regenerate the metal catalyst. The CH3COI reacts with water to generate acetic acid and regenerate HI.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berg, I., Kockelkorn, D., Ramos-Vera, W. et al. Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8, 447–460 (2010). https://doi.org/10.1038/nrmicro2365

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2365

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing