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Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria

Key Points

  • Acetogenic bacteria are an anaerobic group of microorganisms that use the Wood–Ljungdahl pathway (WLP) to live from the conversion of two molecules of carbon dioxide (CO2) to acetate.

  • The WLP is suggested to be one of the oldest biochemical pathways and is the only pathway that couples the fixation of inorganic carbon to energy conservation.

  • In acetogenic bacteria, the WLP is not directly involved in energy conservation but is coupled to one of two membrane-bound enzyme complexes.

  • Acetogenic bacteria use either the Rnf complex (a ferredoxin–NAD+ oxidoreductase) or potentially an Ech hydrogenase (a ferredoxin–H2 oxidoreductase) for chemiosmotic energy conservation. The coupling ion can be either Na+ or H+.

  • The actual energy equivalent in the acetogenic metabolism is the iron–sulphur cluster of the small protein ferredoxin. The metabolism is focused on transferring electrons to this soluble electron carrier.

  • Acetogenic bacteria should be classified as Rnf- and Ech-containing acetogens according to the bioenergetic differences between organisms in these two groups.

Abstract

Life on earth evolved in the absence of oxygen with inorganic gases as potential sources of carbon and energy. Among the alternative mechanisms for carbon dioxide (CO2) fixation in the living world, only the reduction of CO2 by the Wood–Ljungdahl pathway, which is used by acetogenic bacteria, complies with the two requirements to sustain life: conservation of energy and production of biomass. However, how energy is conserved in acetogenic bacteria has been an enigma since their discovery. In this Review, we discuss the latest progress on the biochemistry and genetics of the energy metabolism of model acetogens, elucidating how these bacteria couple CO2 fixation to energy conservation.

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Figure 1: The Wood–Ljungdahl pathway of acetogenesis.
Figure 2: Model for acetogenesis in Acetobacterium woodii.
Figure 3: Model for acetogenesis in Clostridium ljungdahlii.
Figure 4: Model for acetogenesis in Moorella thermoacetica.

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Acknowledgements

Work in the authors' laboratory was supported by the Deutsche Forschungsgemeinschaft. K.S. received a fellowship of the Studienstiftung des deutschen Volkes. V.M. thanks his co-workers for their excellent contributions over the years.

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SLP or chemiosmotic gradients (PDF 189 kb)

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Glossary

Wood–Ljungdahl pathway

(WLP). The pathway was named according to its discoverers, Harland G. Wood and Lars G. Ljungdahl. It is also referred to as the reductive acetyl-CoA pathway. In this pathway, two molecules of CO2 are reduced and joined to form acetyl-CoA and then acetate.

Autotrophs

Organisms that have the ability to grow in the absence of organic carbon. The organic carbon for biosynthesis is assimilated from inorganic carbon sources such as CO2. (Heterotrophy is used to describe a dependence on organic carbon sources).

Cytochromes

Membrane-bound, haem group-containing electron-transfer proteins that are especially involved in chemiosmotic energy conservation in the aerobic and anaerobic respiratory chains or photosynthesis.

Quinones

Lipid-soluble electron carriers that are often associated with chemiosmotic respiratory chains.

Exergonic reaction

A reaction that releases energy (the change in the free energy is negative) and thus takes place without external energy input.

Tetrahydrofolate

(THF). A cofactor that is involved in transfer reactions of single carbon groups. It is important not only in acetogenesis but also in the metabolism of amino acids or nucleic acids.

Corrinoid

A cofactor based on the corrin skeleton that is, in acetogenesis, involved in methyl-transfer reactions. Cobalamines (as vitamin B12) are the most prominent example of this group of cofactors that contain a cobalt ion bound in the centre of the corrin system.

Endergonic

A term used to describe a reaction that consumes energy (the change in the free energy is positive) and thus can only take place with external energy input.

Flavin

A cofactor for redox reactions based on pteridine. Depending on the attached moiety, flavins are found as flavine adenine dinucleotide or flavine adenine mononucleotide.

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Schuchmann, K., Müller, V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12, 809–821 (2014). https://doi.org/10.1038/nrmicro3365

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