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Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway

Little is known about the evolutionary origins of metabolism. However, key biochemical reactions of glycolysis and the pentose phosphate pathway (PPP), ancient metabolic pathways central to the metabolic network, have non-enzymatic pendants that occur in a prebiotically plausible reaction milieu rec...

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Autores principales: Keller, Markus A., Zylstra, Andre, Castro, Cecilia, Turchyn, Alexandra V., Griffin, Julian L., Ralser, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4730858/
https://www.ncbi.nlm.nih.gov/pubmed/26824074
http://dx.doi.org/10.1126/sciadv.1501235
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author Keller, Markus A.
Zylstra, Andre
Castro, Cecilia
Turchyn, Alexandra V.
Griffin, Julian L.
Ralser, Markus
author_facet Keller, Markus A.
Zylstra, Andre
Castro, Cecilia
Turchyn, Alexandra V.
Griffin, Julian L.
Ralser, Markus
author_sort Keller, Markus A.
collection PubMed
description Little is known about the evolutionary origins of metabolism. However, key biochemical reactions of glycolysis and the pentose phosphate pathway (PPP), ancient metabolic pathways central to the metabolic network, have non-enzymatic pendants that occur in a prebiotically plausible reaction milieu reconstituted to contain Archean sediment metal components. These non-enzymatic reactions could have given rise to the origin of glycolysis and the PPP during early evolution. Using nuclear magnetic resonance spectroscopy and high-content metabolomics that allowed us to measure several thousand reaction mixtures, we experimentally address the chemical logic of a metabolism-like network constituted from these non-enzymatic reactions. Fe(II), the dominant transition metal component of Archean oceanic sediments, has binding affinity toward metabolic sugar phosphates and drives metabolism-like reactivity acting as both catalyst and cosubstrate. Iron and pH dependencies determine a metabolism-like network topology and comediate reaction rates over several orders of magnitude so that the network adopts conditional activity. Alkaline pH triggered the activity of the non-enzymatic PPP pendant, whereas gentle acidic or neutral conditions favored non-enzymatic glycolytic reactions. Fe(II)-sensitive glycolytic and PPP-like reactions thus form a chemical network mimicking structural features of extant carbon metabolism, including topology, pH dependency, and conditional reactivity. Chemical networks that obtain structure and catalysis on the basis of transition metals found in Archean sediments are hence plausible direct precursors of cellular metabolic networks.
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spelling pubmed-47308582016-01-28 Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway Keller, Markus A. Zylstra, Andre Castro, Cecilia Turchyn, Alexandra V. Griffin, Julian L. Ralser, Markus Sci Adv Research Articles Little is known about the evolutionary origins of metabolism. However, key biochemical reactions of glycolysis and the pentose phosphate pathway (PPP), ancient metabolic pathways central to the metabolic network, have non-enzymatic pendants that occur in a prebiotically plausible reaction milieu reconstituted to contain Archean sediment metal components. These non-enzymatic reactions could have given rise to the origin of glycolysis and the PPP during early evolution. Using nuclear magnetic resonance spectroscopy and high-content metabolomics that allowed us to measure several thousand reaction mixtures, we experimentally address the chemical logic of a metabolism-like network constituted from these non-enzymatic reactions. Fe(II), the dominant transition metal component of Archean oceanic sediments, has binding affinity toward metabolic sugar phosphates and drives metabolism-like reactivity acting as both catalyst and cosubstrate. Iron and pH dependencies determine a metabolism-like network topology and comediate reaction rates over several orders of magnitude so that the network adopts conditional activity. Alkaline pH triggered the activity of the non-enzymatic PPP pendant, whereas gentle acidic or neutral conditions favored non-enzymatic glycolytic reactions. Fe(II)-sensitive glycolytic and PPP-like reactions thus form a chemical network mimicking structural features of extant carbon metabolism, including topology, pH dependency, and conditional reactivity. Chemical networks that obtain structure and catalysis on the basis of transition metals found in Archean sediments are hence plausible direct precursors of cellular metabolic networks. American Association for the Advancement of Science 2016-01-15 /pmc/articles/PMC4730858/ /pubmed/26824074 http://dx.doi.org/10.1126/sciadv.1501235 Text en Copyright © 2016, The Authors http://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Research Articles
Keller, Markus A.
Zylstra, Andre
Castro, Cecilia
Turchyn, Alexandra V.
Griffin, Julian L.
Ralser, Markus
Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title_full Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title_fullStr Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title_full_unstemmed Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title_short Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
title_sort conditional iron and ph-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4730858/
https://www.ncbi.nlm.nih.gov/pubmed/26824074
http://dx.doi.org/10.1126/sciadv.1501235
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