Abstract
Domestication of CO2-fixation became a worldwide priority enhanced by the will to convert this greenhouse gas into fuels and valuable chemicals. Because of its high stability, CO2-activation/fixation represents a true challenge for chemists. Autotrophic microbial communities, however, perform these reactions under standard temperature and pressure. Recent discoveries shine light on autotrophic acetogenic bacteria and hydrogenotrophic methanogens, as these anaerobes use a particularly efficient CO2-capture system to fulfill their carbon and energy needs. While other autotrophs assimilate CO2 via carboxylation followed by a reduction, acetogens and methanogens do the opposite. They first generate formate and CO by CO2-reduction, which are subsequently fixed to funnel the carbon toward their central metabolism. Yet their CO2-reduction pathways, with acetate or methane as end-products, constrain them to thrive at the “thermodynamic limits of Life”. Despite this energy restriction acetogens and methanogens are growing at unexpected fast rates. To overcome the thermodynamic barrier of CO2-reduction they apply different ingenious chemical tricks such as the use of flavin-based electron-bifurcation or coupled reactions. This mini-review summarizes the current knowledge gathered on the CO2-fixation strategies among acetogens. While extensive biochemical characterization of the acetogenic formate-generating machineries has been done, there is no structural data available. Based on their shared mechanistic similarities, we apply the structural information obtained from hydrogenotrophic methanogens to highlight common features, as well as the specific differences of their CO2-fixation systems. We discuss the consequences of their CO2-reduction strategies on the evolution of Life, their wide distribution and their impact in biotechnological applications.
Highlights
CO2, the most oxidized state of carbon, has become a major concern to society due to its greenhouse gas properties and its increasing accumulation in our atmosphere since the 20thcentury
The formate dehydrogenase (Fdh) subunit and CODH/ACS complex are conserved in methanogens and acetogens
These elementary modules are thought to have evolved before the divergence of acetogens and methanogens, in the Last Universal Common Ancestor (LUCA) (Sousa et al, 2013; Martin and Thauer, 2017)
Summary
CO2, the most oxidized state of carbon, has become a major concern to society due to its greenhouse gas properties and its increasing accumulation in our atmosphere since the 20thcentury. The energy metabolism of acetogens and methanogens was puzzling for a long time until the discovery of energy conserving enzymes (i.e., Rnf and Ech membrane complexes), which use low-potential electrons from ferredoxins, reduced by H2 oxidation via flavin-based electron bifurcation (Figure 1D). The enzyme can perform carbon fixation by ferredoxin oxidation, albeit exhibiting a 1000times lower reaction rate (Figure 2B, 2) This ability is thought to be crucial in presence of CO, a strong inhibitor of hydrogenases. The selenium-dependent tungstopterin-containing Fdh module performs CO2-reduction by receiving electrons from H2-oxidation via a [FeFe]hydrogenase subunit (similar to HDCR) or by concomitant oxidation of NADPH and ferredoxin through an internal confurcation event (Figures 1D, 2B, 4). The structural features of this bifurcation mechanism have to be deciphered and as said by Buckel and Thauer (2018): “A crystal structure is urgently needed to solve this problem.”
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