Experimental and Theoretical Constraints on Amino Acid Formation from PAHs in Asteroidal Settings.

Amino acids and polycyclic aromatic hydrocarbons (PAHs) belong to the range of organic compounds detected in meteorites. In this study, we tested empirically and theoretically if PAHs are precursors for amino acids in carbonaceous chondrites, as previously suggested. We conducted experiments to synthesize amino acids from fluoranthene (PAH), with ammonium bicarbonate as a source for ammonia and carbon dioxide under mimicked asteroidal conditions. In our thermodynamic calculations, we extended our analysis to additional PAH-amino acid combinations. We explored 36 reactions involving the PAHs naphthalene, anthracene, fluoranthene, pyrene, triphenylene, and coronene and the amino acids glycine, alanine, valine, leucine, phenylalanine, and tyrosine. Our experiments do not show the formation of amino acids, whereas our theoretical results hint that PAHs could be precursors of amino acids in carbonaceous chondrites at low temperatures.

The Future of Origin of Life Research: Bridging Decades-Old Divisions.

Research on the origin of life is highly heterogeneous. After a peculiar historical development, it still includes strongly opposed views which potentially hinder progress. In the 1st Interdisciplinary Origin of Life Meeting, early-career researchers gathered to explore the commonalities between theories and approaches, critical divergence points, and expectations for the future. We find that even though classical approaches and theories-e.g. bottom-up and top-down, RNA world vs. metabolism-first-have been prevalent in origin of life research, they are ceasing to be mutually exclusive and they can and should feed integrating approaches. Here we focus on pressing questions and recent developments that bridge the classical disciplines and approaches, and highlight expectations for future endeavours in origin of life research.

Acetyl Phosphate as a Primordial Energy Currency at the Origin of Life.

Metabolism is primed through the formation of thioesters via acetyl CoA and the phosphorylation of substrates by ATP. Prebiotic equivalents such as methyl thioacetate and acetyl phosphate have been proposed to catalyse analogous reactions at the origin of life, but their propensity to hydrolyse challenges this view. Here we show that acetyl phosphate (AcP) can be synthesised in water within minutes from thioacetate (but not methyl thioacetate) under ambient conditions. AcP is stable over hours, depending on temperature, pH and cation content, giving it an ideal poise between stability and reactivity. We show that AcP can phosphorylate nucleotide precursors such as ribose to ribose-5-phosphate and adenosine to adenosine monophosphate, at modest (~2%) yield in water, and at a range of pH. AcP can also phosphorylate ADP to ATP in water over several hours at 50 °C. But AcP did not promote polymerization of either glycine or AMP. The amino group of glycine was preferentially acetylated by AcP, especially at alkaline pH, hindering the formation of polypeptides. AMP formed small stacks of up to 7 monomers, but these did not polymerise in the presence of AcP in aqueous solution. We conclude that AcP can phosphorylate biologically meaningful substrates in a manner analogous to ATP, promoting the origins of metabolism, but is unlikely to have driven polymerization of macromolecules such as polypeptides or RNA in free solution. This is consistent with the idea that a period of monomer (cofactor) catalysis preceded the emergence of polymeric enzymes or ribozymes at the origin of life.

Iron catalysis at the origin of life.

Iron-sulphur proteins are ancient and drive fundamental processes in cells, notably electron transfer and CO2 fixation. Iron-sulphur minerals with equivalent structures could have played a key role in the origin of life. However, the 'iron-sulphur world' hypothesis has had a mixed reception, with questions raised especially about the feasibility of a pyrites-pulled reverse Krebs cycle. Phylogenetics suggests that the earliest cells drove carbon and energy metabolism via the acetyl CoA pathway, which is also replete in Fe(Ni)S proteins. Deep differences between bacteria and archaea in this pathway obscure the ancestral state. These differences make sense if early cells depended on natural proton gradients in alkaline hydrothermal vents. If so, the acetyl CoA pathway diverged with the origins of active ion pumping, and ancestral CO2 fixation might have been equivalent to methanogens, which depend on a membrane-bound NiFe hydrogenase, energy converting hydrogenase. This uses the proton-motive force to reduce ferredoxin, thence CO2 . The mechanism suggests that pH could modulate reduction potential at the active site of the enzyme, facilitating the difficult reduction of CO2 by H2 . This mechanism could be generalised under abiotic conditions so that steep pH differences across semi-conducting Fe(Ni)S barriers drives not just the first steps of CO2 fixation to C1 and C2 organics such as CO, CH3 SH and CH3 COSH, but a series of similar carbonylation and hydrogenation reactions to form longer chain carboxylic acids such as pyruvate, oxaloacetate and α-ketoglutarate, as in the incomplete reverse Krebs cycle found in methanogens. We suggest that the closure of a complete reverse Krebs cycle, by regenerating acetyl CoA directly, displaced the acetyl CoA pathway from many modern groups. A later reliance on acetyl CoA and ATP eliminated the need for the proton-motive force to drive most steps of the reverse Krebs cycle. © 2017 IUBMB Life, 69(6):373-381, 2017.

The Origin of Life in Alkaline Hydrothermal Vents.

Over the last 70 years, prebiotic chemists have been very successful in synthesizing the molecules of life, from amino acids to nucleotides. Yet there is strikingly little resemblance between much of this chemistry and the metabolic pathways of cells, in terms of substrates, catalysts, and synthetic pathways. In contrast, alkaline hydrothermal vents offer conditions similar to those harnessed by modern autotrophs, but there has been limited experimental evidence that such conditions could drive prebiotic chemistry. In the Hadean, in the absence of oxygen, alkaline vents are proposed to have acted as electrochemical flow reactors, in which alkaline fluids saturated in H2 mixed with relatively acidic ocean waters rich in CO2, through a labyrinth of interconnected micropores with thin inorganic walls containing catalytic Fe(Ni)S minerals. The difference in pH across these thin barriers produced natural proton gradients with equivalent magnitude and polarity to the proton-motive force required for carbon fixation in extant bacteria and archaea. How such gradients could have powered carbon reduction or energy flux before the advent of organic protocells with genes and proteins is unknown. Work over the last decade suggests several possible hypotheses that are currently being tested in laboratory experiments, field observations, and phylogenetic reconstructions of ancestral metabolism. We analyze the perplexing differences in carbon and energy metabolism in methanogenic archaea and acetogenic bacteria to propose a possible ancestral mechanism of CO2 reduction in alkaline hydrothermal vents. Based on this mechanism, we show that the evolution of active ion pumping could have driven the deep divergence of bacteria and archaea.

An origin-of-life reactor to simulate alkaline hydrothermal vents.

Chemiosmotic coupling is universal: practically all cells harness electrochemical proton gradients across membranes to drive ATP synthesis, powering biochemistry. Autotrophic cells, including phototrophs and chemolithotrophs, also use proton gradients to power carbon fixation directly. The universality of chemiosmotic coupling suggests that it arose very early in evolution, but its origins are obscure. Alkaline hydrothermal systems sustain natural proton gradients across the thin inorganic barriers of interconnected micropores within deep-sea vents. In Hadean oceans, these inorganic barriers should have contained catalytic Fe(Ni)S minerals similar in structure to cofactors in modern metabolic enzymes, suggesting a possible abiotic origin of chemiosmotic coupling. The continuous supply of H2 and CO2 from vent fluids and early oceans, respectively, offers further parallels with the biochemistry of ancient autotrophic cells, notably the acetyl CoA pathway in archaea and bacteria. However, the precise mechanisms by which natural proton gradients, H2, CO2 and metal sulphides could have driven organic synthesis are uncertain, and theoretical ideas lack empirical support. We have built a simple electrochemical reactor to simulate conditions in alkaline hydrothermal vents, allowing investigation of the possibility that abiotic vent chemistry could prefigure the origins of biochemistry. We discuss the construction and testing of the reactor, describing the precipitation of thin-walled, inorganic structures containing nickel-doped mackinawite, a catalytic Fe(Ni)S mineral, under prebiotic ocean conditions. These simulated vent structures appear to generate low yields of simple organics. Synthetic microporous matrices can concentrate organics by thermophoresis over several orders of magnitude under continuous open-flow vent conditions.