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Native Iron Reduces CO2 to Intermediates and End- Products of the Acetyl-Coa Pathway

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Native Iron Reduces CO2 to Intermediates and End- Products of the Acetyl-Coa Pathway ARTICLES https://doi.org/10.1038/s41559-018-0542-2 Native iron reduces CO2 to intermediates and end- products of the acetyl-CoA pathway Sreejith J. Varma 1,2, Kamila B. Muchowska 1,2, Paul Chatelain1 and Joseph Moran 1* Autotrophic theories for the origin of life propose that CO2 was the carbon source for primordial biosynthesis. Among the six known CO2 fixation pathways in nature, the acetyl-CoA (AcCoA; or Wood–Ljungdahl) pathway is the most ancient, and relies on transition metals for catalysis. Modern microbes that use the AcCoA pathway typically fix CO2 with electrons from H2, which requires complex flavin-based electron bifurcation. This presents a paradox: how could primitive metabolic systems have fixed 0 0 0 CO2 before the origin of proteins? Here, we show that native transition metals (Fe , Ni and Co ) selectively reduce CO2 to acetate and pyruvate—the intermediates and end-products of the AcCoA pathway—in near millimolar concentrations in water over hours to days using 1–40 bar CO2 and at temperatures from 30 to 100 °C. Geochemical CO2 fixation from native metals could have supplied critical C2 and C3 metabolites before the emergence of enzymes. rom the earliest stages of the transition from chemistry to bio- nanoparticles have been shown to reduce CO2 to formate, with chemistry at the origin of life, synthetic pathways must have acetate formed as a minor product at 200 °C under 40 bar CO2 pres- Foperated to build molecular complexity from simple starting sure21. Before the emergence of electron-bifurcating enzymes, could materials. Life’s fundamental need to build up carbon-based mol- native metals achieve reductive CO2 fixation under conditions mild ecules has understandably orientated research on prebiotic chem- enough for a protometabolism? istry towards high-energy C1 and C2 compounds such as HCN and formaldehyde, which react in ways that bear little resemblance to Results biosynthesis, often requiring ultraviolet light1–3 (see also references Anticipating a link between the role of metallic cofactors in extant within ref. 1). However, as far as we can infer from extant biology, microbial metabolism and in prebiotic chemistry22–24, we set out life has always built its biomass from CO2. Could this attribute have to investigate whether the native forms of the metals involved in extended back to prebiotic chemistry? Of the six known pathways the reductive AcCoA pathway might promote C–C bond forma- 4,5 of CO2 fixation in nature , the acetyl-CoA (AcCoA; or Wood– tion from CO2 in water. Initially, we screened reactions of 1 mmol 6–8 Ljungdahl) pathway is the most ancient . It reduces CO2 to acetyl of Fe, Co, Ni, Mn, Mo and W powders (for specifications see and then pyruvate—the ubiquitous C2 and C3 building blocks for Supplementary Table 1) in a 1 M KCl solution in deionized H2O life. Its enzymes and cofactors are replete with transition metals (Fe, by heating to 100 °C under 35 bar CO2 pressure for 16 h. The reac- Ni, Co, Mo or W) and, unlike the other five pathways, it is short, tion mixtures were then treated with KOH to precipitate hydrox- linear, exergonic and found in both bacteria and archaea, with the ides, which were removed by centrifugation before analysis by archaeal version being ATP-independent (Fig. 1)9–12. For all these 1H NMR and gas chromatography mass spectrometry (GC-MS) reasons, the AcCoA pathway is often proposed to have prebiotic (Supplementary Figs. 1–8). Quantification was achieved by com- origins13, although such a proposition faces some difficulties. Most parison with a calibration curve prepared from authentic samples modern microbes that run the AcCoA pathway fix CO2 using elec- (Supplementary Fig. 9). To our surprise, all of these metals were trons from H2 gas, whose midpoint potential is not sufficient to gen- found to promote the formation of acetate in up to 0.28 ±​ 0.01 mM erate the required highly reduced ferredoxin proteins in the absence concentrations, with considerable amounts of pyruvate observed of flavin-based electron bifurcation14. Therein lies a problem for in the cases of iron (0.03 ±​ 0.01 mM), nickel (0.02 ±​ 0.00 mM) autotrophic theories of the origin of life: how could CO2 fixation and cobalt (0.01 ±​ 0.00 mM) (Fig. 2). Substantial quantities of for- have occurred before there were proteins to enable electron bifur- mate (up to 2.3 ±​ 0.2 mM in the case of cobalt) and methanol (up cation? Many experimental attempts to address this question have to 0.39 ±​ 0.00 mM in the case of molybdenum) were also found in bypassed the direct use of CO2 altogether, focusing instead on its almost all cases. Control experiments in the absence of metal pow- 15,16 more reduced derivatives such as CO or formic acid . However, ders or in the absence of CO2 did not produce detectable quantities clues from extant biology and the chemical literature suggest that of carbon fixation products (Supplementary Figs. 10 and 11). native metals might warrant further experimental consideration In light of iron’s position as the most Earth-abundant metal (pre- 17 0 2+ 3+ as a prebiotic source of electrons for CO2 fixation . Even today, dominantly as Fe in the Earth’s core and Fe /Fe in the Earth’s 25 some bacteria that use the AcCoA pathway grow using native iron mantle and crust) , we elected to study Fe-mediated CO2 fixation as the sole source of electrons18,19. We recently reported chemical in more detail by evaluating the influence of temperature, pres- experiments where many reactions of the reductive tricarboxylic sure, time, pH, salt identity and salt concentration on the reac- acid (rTCA) cycle—another potentially prebiotic CO2-fixing path- tion outcome. First, we studied the effect of temperature over the way—can be driven in sequence without enzymes using native iron range 30–150 °C under typical conditions (35 bar CO2, unbuf- 20 as the source of electrons . Meanwhile, freshly prepared native iron fered 1 M KCl solution in deionized H2O, 16 h) (Fig. 3a; see also 1Institute of Supramolecular Science and Engineering (UMR 7006), University of Strasbourg, National Center for Scientific Research , Strasbourg, France. 2These authors contributed equally: Sreejith J. Varma and Kamila B. Muchowska. *e-mail: [email protected] NATURE EcoLOGY & EvoLUTION | www.nature.com/natecolevol © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. ARTICLES NATURE ECOLOGY & EVOLUTION – 2e O 2H+ C CO2 CO2 –H2O 2e– O + – O CH3 2H O Me – – O – + 2e 2e 2e , H O H 2H+ HO 2H+ AcCoA Pyruvate CH CO2 3 –H2O Fig. 1 | Mechanistic outline of the ATP-independent AcCoA pathway found in archaea. The reductive carboxylation of AcCoA to pyruvate is also found in the first step of the rTCA cycle. For clarity, organic and metallic cofactors are depicted as a squiggly horizontal line. Supplementary Fig. 12 and Supplementary Table 2). At the lower Table 19). On the basis of these observations, we conclude that CO2 end of the temperature range, acetate is the major product in solu- fixation occurs on the surface of the metal and that its intermediates tion, with pyruvate and formate produced in slightly smaller quan- and end-products remain bound to the surface during the reaction. tities. Increasing the reaction temperature to 100 °C results in the In light of this surface chemistry, the observed product distribu- appearance of methanol among the other products. At 150 °C, pyru- tion and the reaction’s kinetic profile, we propose a plausible yet vate is no longer observed, presumably due to thermal decomposi- still largely hypothetical mechanism whereby the initial reduction tion. The reaction is robust to CO2 pressure over the investigated of CO2 occurs to generate surface-bound CO and formyl groups. range 1–40 atm at 30 °C, with acetate and pyruvate being the major Further reductions of the formyl group with expulsion of water lead products at lower pressures (Fig. 3b; see also Supplementary Fig. 13 to a surface-bound methyl group. Chain growth via migratory inser- and Supplementary Table 3). The reaction progress was monitored tion of CO into the methyl group produces an acetyl species, which at different times under two representative sets of conditions. At itself can undergo further migratory insertion of CO or reductive 30 °C and 1 bar CO2, acetate and pyruvate are the major products, carboxylation with CO2 to furnish a surface-bound pyruvyl or with acetate reaching nearly 0.7 mM after 40 h before decreasing in pyruvate species, respectively. The resistance of pyruvate or pyruvyl 0 concentration (Fig. 3c). At 100 °C and 35 bar CO2, the initial build- to reduction by Fe may be rationalized by a diminished reactivity up of formate is rapid, increasing to 7.2 ±​ 0.4 mM after 6 h before of the surface-bound species compared with pyruvate in solution. decreasing sharply as acetate and pyruvate begin to appear (Fig. 3d; Basic workup at the end of the reaction with KOH is required to see also Supplementary Fig. 14 and Supplementary Table 4). cleave the products from the surface to furnish formate, methanol, After 60 h, acetate and pyruvate reach maximal concentrations of acetate or pyruvate in solution (Fig. 4). One possible interpreta- 1.09 ±​ 0.00 mM and 0.11 ±​ 0.01 mM, respectively. Stopping the reac- tion of the kinetic profile observed in Fig. 3c is that the Fe surface tion at this time reveals that no Fe0 visibly remains, although only becomes initially saturated with formyl and CO groups, with sub- ~1% of the available electrons from Fe0 were channelled towards the sequent reactions of these groups producing acetyl and, eventually, 2+ 24 described C1–C3 products in solution (assuming Fe is the terminal pyruvyl groups .
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