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

ABSTRACT: 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.

SUBMITTER: Whicher A

PROVIDER: S-EPMC6061221 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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

Whicher Alexandra A Camprubi Eloi E Pinna Silvana S Herschy Barry B Lane Nick N

Origins of life and evolution of the biosphere : the journal of the International Society for the Study of the Origin of Life 20180303 2

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, ...[more]

PMID: 29502283

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Project description:ATP is universally conserved as the principal energy currency in cells, driving metabolism through phosphorylation and condensation reactions. Such deep conservation suggests that ATP arose at an early stage of biochemical evolution. Yet purine synthesis requires 6 phosphorylation steps linked to ATP hydrolysis. This autocatalytic requirement for ATP to synthesize ATP implies the need for an earlier prebiotic ATP equivalent, which could drive protometabolism before purine synthesis. Why this early phosphorylating agent was replaced, and specifically with ATP rather than other nucleoside triphosphates, remains a mystery. Here, we show that the deep conservation of ATP might reflect its prebiotic chemistry in relation to another universally conserved intermediate, acetyl phosphate (AcP), which bridges between thioester and phosphate metabolism by linking acetyl CoA to the substrate-level phosphorylation of ADP. We confirm earlier results showing that AcP can phosphorylate ADP to ATP at nearly 20% yield in water in the presence of Fe3+ ions. We then show that Fe3+ and AcP are surprisingly favoured. A wide range of prebiotically relevant ions and minerals failed to catalyse ADP phosphorylation. From a panel of prebiotic phosphorylating agents, only AcP, and to a lesser extent carbamoyl phosphate, showed any significant phosphorylating potential. Critically, AcP did not phosphorylate any other nucleoside diphosphate. We use these data, reaction kinetics, and molecular dynamic simulations to infer a possible mechanism. Our findings might suggest that the reason ATP is universally conserved across life is that its formation is chemically favoured in aqueous solution under mild prebiotic conditions. This study shows that acetyl phosphate is unique among a large panel of plausible prebiotic agents in phosphorylating ADP to ATP in water in the presence of ferric iron. Acetyl phosphate does not phosphorylate other nucleoside diphosphates, suggesting that ATP became established as the universal energy currency in a prebiotic, monomer world on the basis of its unusual chemistry in water.

Project description:BackgroundBiodiversity offsets provide a mechanism to compensate for unavoidable damages from new energy development as the U.S. increases its domestic production. Proponents argue that offsets provide a partial solution for funding conservation while opponents contend the practice is flawed because offsets are negotiated without the science necessary to backup resulting decisions. Missing in negotiations is a biologically-based currency for estimating sufficiency of offsets and a framework for applying proceeds to maximize conservation benefits.Methodology/principal findingsHere we quantify a common currency for offsets for greater sage-grouse (Centrocercus urophasianus) by estimating number of impacted birds at 4 levels of development commonly permitted. Impacts were indiscernible at 1-12 wells per 32.2 km(2). Above this threshold lek losses were 2-5 times greater inside than outside of development and bird abundance at remaining leks declined by -32 to -77%. Findings reiterated the importance of time-lags as evidenced by greater impacts 4 years after initial development. Clustering well locations enabled a few small leks to remain active inside of developments.Conclusions/significanceDocumented impacts relative to development intensity can be used to forecast biological trade-offs of newly proposed or ongoing developments, and when drilling is approved, anticipated bird declines form the biological currency for negotiating offsets. Monetary costs for offsets will be determined by true conservation cost to mitigate risks such as sagebrush tillage to other populations of equal or greater number. If this information is blended with landscape level conservation planning, the mitigation hierarchy can be improved by steering planned developments away from conservation priorities, ensuring compensatory mitigation projects deliver a higher return for conservation that equate to an equal number of birds in the highest priority areas, provide on-site mitigation recommendations, and provide a biologically based cost for mitigating unavoidable impacts.

Project description:BACKGROUND:With approximately one-third of their genomes consisting of linear and circular plasmids, the Lyme disease agent cluster of species has the most complex genomes among known bacteria. We report here a comparative analysis of plasmids in eleven Borreliella (also known as Borrelia burgdorferi sensu lato) species. RESULTS:We sequenced the complete genomes of two B. afzelii, two B. garinii, and individual B. spielmanii, B. bissettiae, B. valaisiana and B. finlandensis isolates. These individual isolates carry between seven and sixteen plasmids, and together harbor 99 plasmids. We report here a comparative analysis of these plasmids, along with 70 additional Borreliella plasmids available in the public sequence databases. We identify only one new putative plasmid compatibility type (the 30th) among these 169 plasmid sequences, suggesting that all or nearly all such types have now been discovered. We find that the linear plasmids in the non-B. burgdorferi species have undergone the same kinds of apparently random, chaotic rearrangements mediated by non-homologous recombination that we previously discovered in B. burgdorferi. These rearrangements occurred independently in the different species lineages, and they, along with an expanded chromosomal phylogeny reported here, allow the identification of several whole plasmid transfer events among these species. Phylogenetic analyses of the plasmid partition genes show that a majority of the plasmid compatibility types arose early, most likely before separation of the Lyme agent Borreliella and relapsing fever Borrelia clades, and this, with occasional cross species plasmid transfers, has resulted in few if any species-specific or geographic region-specific Borreliella plasmid types. CONCLUSIONS:The primordial origin and persistent maintenance of the Borreliella plasmid types support their functional indispensability as well as evolutionary roles in facilitating genome diversity. The improved resolution of Borreliella plasmid phylogeny based on conserved partition-gene clusters will lead to better determination of gene orthology which is essential for prediction of biological function, and it will provide a basis for inferring detailed evolutionary mechanisms of Borreliella genomic variability including homologous gene and plasmid exchanges as well as non-homologous rearrangements.

Dataset Information

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

Publications

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

Similar Datasets

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