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  • 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.

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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.

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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.

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  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

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Related links

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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.

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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

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