CO2-Fixation Strategies in Energy Extremophiles: What Can We Learn From Acetogens?

Abstract

Domestication of CO 2-fixation became a worldwide priority enhanced by the will to convert this greenhouse gas into fuels and valuable chemicals. Because of its high stability, CO 2-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 CO 2capture system to fulfill their carbon and energy needs. While other autotrophs assimilate CO 2 via carboxylation followed by a reduction, acetogens and methanogens do the opposite. They first generate formate and CO by CO 2-reduction, which are subsequently fixed to funnel the carbon toward their central metabolism. Yet their CO 2-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 CO 2-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 CO 2-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 CO 2-fixation systems. We discuss the consequences of their CO 2reduction strategies on the evolution of Life, their wide distribution and their impact in biotechnological applications.

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“…Finally, the one-carbon unit transfers to nickel-bound CO and forms acetyl-CoA. In acetogens, CO 2 is reduced to acetic acid with H 2 via the Wood-Ljungdahl pathway, in which the ATP required for formate activation is regenerated in the acetate kinase reaction (Mock et al, 2015;Lemaire et al, 2020).…”

“…NAD-independent FDH is characterized by high activity toward CO 2 and sensitivity to oxygen (Maia et al, 2016;Yu et al, 2017). This class of FDH contains complex redox-active centers harboring different transition metals, such as molybdenum (Mo), tungsten and nonhaemiron, molybdopterin guanine dinucleotide (MGD) and selenocysterine (Niks and Hille, 2019;Lemaire et al, 2020). It has been identified only in prokaryotic organisms.…”

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“…Thereby using CO 2 to produce truly degradable biopolymers might be solution that solves two problems. It reduces the global CO 2 emission and makes significant contribution to the advances towards plastics removal (Lemaire et al 2020 ).…”

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“…Hydrogenotrophic methanogens use the reductive acetyl-CoA pathway for CO2 fixation 6 , an energy-efficient route to synthesize organic carbon from CO2 and hydrogen that is similar to the pathway present in acetogens. There are, however, subtle differences between the acetogenic 7 and the methanogenic way of CO2 reduction in terms of ATP vs. ion-gradient investment, and in terms of cofactor utilization 8 . It is therefore recommended to consider both, acetogens and methanogens, as possible host organisms for the production of fuels and chemicals from CO2 as the carbon source.…”

“…Hydrogenotrophic methanogens utilize the reductive acetyl-CoA pathway for CO 2 fixation 5 , an energy-efficient route to synthesize organic carbon from CO 2 and hydrogen (H 2 ), which is similar to that found in acetogens 6 . However, subtle differences exist between the acetogenic 7 and methanogenic pathways of CO 2 reduction in terms of ATP investment and cofactor utilization 8 . Depending on the requested product that needs to be generated from CO 2 as the carbon source, methanogens may be better suited host organisms than acetogens.…”