The Moon‐Forming Impact and the Autotrophic Origin of Life

Mrnjavac, Natalia; Wimmer, Jessica L. E.; Brabender, Max; Schwander, Loraine; Martin, William F.

doi:10.1002/cplu.202300270

Cited by 8 publications

(5 citation statements)

References 232 publications

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“…Fougèrite (Green Rust) may also have played a role as a microchamber catalytic site [101]. These reactions generate the backbone of carbon and energy for metabolism [102]. The products produced are similar to the intermediates formed in the Acetyl-CoA pathway of autotrophic microbes, such as formate and acetate [9,103].…”

Section: Initial Rafsmentioning

confidence: 99%

“…In the absence of enzymes (or ribozymes), metal complexes such as Fe3S4, Fe3O4, and Ni3Fe are capable of catalyzing Acetyl-CoA type reactions [9], and the fact that today enzymes with Fe-Ni cores play a major role in the Acetyl-CoA pathway strongly supports the idea that these vents were the cradles of life (following the QWERTY principle [see Section 1.1.2. above]). Note that it has recently been proposed that the planetary impact that created the moon led to the huge pool of CO2 upon which first life may have depended [102]. In an alkaline hydrothermal vent system, simple organic molecules will form from the hydrogen and carbon dioxide in the vent flux, catalyzed by transition metals in the microchamber walls and the vent flux [23,97].…”

Section: Initial Rafsmentioning

confidence: 99%

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Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell

Brunk,

Marshall

2024

Life

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The path from life’s origin to the emergence of the eukaryotic cell was long and complex, and as such it is rarely treated in one publication. Here, we offer a sketch of this path, recognizing that there are points of disagreement and that many transitions are still shrouded in mystery. We assume life developed within microchambers of an alkaline hydrothermal vent system. Initial simple reactions were built into more sophisticated reflexively autocatalytic food-generated networks (RAFs), laying the foundation for life’s anastomosing metabolism, and eventually for the origin of RNA, which functioned as a genetic repository and as a catalyst (ribozymes). Eventually, protein synthesis developed, leading to life’s biology becoming dominated by enzymes and not ribozymes. Subsequent enzymatic innovation included ATP synthase, which generates ATP, fueled by the proton gradient between the alkaline vent flux and the acidic sea. This gradient was later internalized via the evolution of the electron transport chain, a preadaptation for the subsequent emergence of the vent creatures from their microchamber cradles. Differences between bacteria and archaea suggests cellularization evolved at least twice. Later, the bacterial development of oxidative phosphorylation and the archaeal development of proteins to stabilize its DNA laid the foundation for the merger that led to the formation of eukaryotic cells.

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Section: Initial Rafsmentioning

confidence: 99%

Section: Initial Rafsmentioning

confidence: 99%

Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell

Brunk,

Marshall

2024

Life

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“…All ecosystems today start from CO 2 with autotrophs providing the reduced carbon compounds required by heterotrophs. Carbon from space is too reduced and structurally too heterogeneous to support fermentations, and the Moon-forming impact transformed all accreted carbon on the early Earth into CO 2 . , That means that CO 2 was the starting material for the first organic syntheses and the source of carbon for primary producers (autotrophs) that fueled the first ecosystems, the foundation of autotrophic theories for origins. − The Moon-forming impact generated a primordial atmosphere rich in CO 2 that dissolved in the ocean, generating a pH of roughly 6.5 from carbonic acid . That localizes primordial CO 2 to the Earth’s entire surface and oceans, but provides no direct clues about the specific environment where the CO 2 reduction process might have gotten started.…”

Section: Introductionmentioning

confidence: 99%

“…In acetogen and methanogen metabolism, the main intermediates and products of the acetyl-CoA pathway are formate (an intermediate), pyruvate (the main source of carbon for biosynthesis), acetate and methane (the end products of acetogens and methanogens, respectively). , The acetyl-CoA pathway is linear, exergonic, the only CO 2 -fixing pathway that occurs in bacteria and archaea , and can simultaneously support CO 2 fixation and ATP synthesis, and it is the only multistep biochemical pathway that can be replaced entirely by single metals as catalysts. The acetyl-CoA pathway requires a total of 127 enzymesabout 20 enzymes of the pathway itself (in acetogens and methanogens) plus >100 enzymes for the synthesis of required cofactors . That massive enzymatic demand might not seem ancient at first sight.…”

Section: Introductionmentioning

confidence: 99%

Chemical Antiquity in Metabolism

Mrnjavac,

Schwander,

Brabender

et al. 2024

Acc. Chem. Res.

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Metrics & MoreArticle Recommendations * sı Supporting Information CONSPECTUS: Life is an exergonic chemical reaction. The same was true when the very first cells emerged at life's origin. In order to live, all cells need a source of carbon, energy, and electrons to drive their overall reaction network (metabolism). In most cells, these are separate pathways. There is only one biochemical pathway that serves all three needs simultaneously: the acetyl-CoA pathway of CO 2 fixation. In the acetyl-CoA pathway, electrons from H 2 reduce CO 2 to pyruvate for carbon supply, while methane or acetate synthesis are coupled to energy conservation as ATP. This simplicity and thermodynamic favorability prompted Georg Fuchs and Erhard Stupperich to propose in 1985 that the acetyl-CoA pathway might mark the origin of metabolism, at the same time that Steve Ragsdale and Harland Wood were uncovering catalytic roles for Fe, Co, and Ni in the enzymes of the pathway. Subsequent work has provided strong support for those proposals. In the presence of Fe, Co, and Ni in their native metallic state as catalysts, aqueous H 2 and CO 2 react specifically to formate, acetate, methane, and pyruvate overnight at 100 °C. These metals (and their alloys) thus replace the function of over 120 enzymes required for the conversion of H 2 and CO 2 to pyruvate via the pathway and its cofactors, an unprecedented set of findings in the study of biochemical evolution. The reactions require alkaline conditions, which promote hydrogen oxidation by proton removal and are naturally generated in serpentinizing (H 2 -producing) hydrothermal vents. Serpentinizing hydrothermal vents furthermore produce natural deposits of native Fe, Co, Ni, and their alloys. These are precisely the metals that reduce CO 2 with H 2 in the laboratory; they are also the metals found at the active sites of enzymes in the acetyl-CoA pathway. Iron, cobalt and nickel are relicts of the environments in which metabolism arose, environments that still harbor ancient methane-and acetate-producing autotrophs today. This convergence indicates bedrock-level antiquity for the acetyl-CoA pathway. In acetogens and methanogens growing on H 2 as reductant, the acetyl-CoA pathway requires flavin-based electron bifurcation as a source of reduced ferredoxin (a 4Fe4S clustercontaining protein) in order to function. Recent findings show that H 2 can reduce the 4Fe4S clusters of ferredoxin in the presence of native iron, uncovering an evolutionary precursor of flavin-based electron bifurcation and suggesting an origin of FeS-dependent electron transfer in proteins. Traditionally discussed as catalysts in early evolution, the most common function of FeS clusters in metabolism is one-electron transfer, also in radical SAM enzymes, a large and ancient enzyme family. The cofactors and active sites in enzymes of the acetyl-CoA pathway uncover chemical antiquity in metabolism involving metals, methyl groups, methyl transfer reactions, cobamides, pterins, GTP, S-adenosylmethionine, radical SAM enzymes, and carb...

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“…The enzymes of the acetyl-CoA pathway are replete with transition metals as electron carriers and catalysts ( 4 – 8 ), inorganic cofactors that are reasonably interpreted as relicts ( 9 – 12 ) from a geochemical setting ( 13 ) within which metabolism and life arose. In acetogens and methanogens growing on H 2 and CO 2 , the acetyl-CoA pathway converts H 2 and CO 2 into formate ( 4 ), acetate, and pyruvate ( 2 ) via ~10 enzymatic reactions that require 14 cofactors and 127 proteins, including the cofactor biosynthesis pathways ( 14 ).…”

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confidence: 99%

Ferredoxin reduction by hydrogen with iron functions as an evolutionary precursor of flavin-based electron bifurcation

Brabender,

Henriques Pereira,

Mrnjavac

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Autotrophic theories for the origin of metabolism posit that the first cells satisfied their carbon needs from CO 2 and were chemolithoautotrophs that obtained their energy and electrons from H 2 . The acetyl-CoA pathway of CO 2 fixation is central to that view because of its antiquity: Among known CO 2 fixing pathways it is the only one that is i) exergonic, ii) occurs in both bacteria and archaea, and iii) can be functionally replaced in full by single transition metal catalysts in vitro. In order to operate in cells at a pH close to 7, however, the acetyl-CoA pathway requires complex multi-enzyme systems capable of flavin-based electron bifurcation that reduce low potential ferredoxin—the physiological donor of electrons in the acetyl-CoA pathway—with electrons from H 2 . How can the acetyl-CoA pathway be primordial if it requires flavin-based electron bifurcation? Here, we show that native iron (Fe 0 ), but not Ni 0 , Co 0 , Mo 0 , NiFe, Ni 2 Fe, Ni 3 Fe, or Fe 3 O 4 , promotes the H 2 -dependent reduction of aqueous Clostridium pasteurianum ferredoxin at pH 8.5 or higher within a few hours at 40 °C, providing the physiological function of flavin-based electron bifurcation, but without the help of enzymes or organic redox cofactors. H 2 -dependent ferredoxin reduction by iron ties primordial ferredoxin reduction and early metabolic evolution to a chemical process in the Earth’s crust promoted by solid-state iron, a metal that is still deposited in serpentinizing hydrothermal vents today.

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The Moon‐Forming Impact and the Autotrophic Origin of Life

Cited by 8 publications

References 232 publications

Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell

Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell

Chemical Antiquity in Metabolism

Ferredoxin reduction by hydrogen with iron functions as an evolutionary precursor of flavin-based electron bifurcation

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