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On the potential roles of phosphorus in the early evolution of energy metabolism

Energy metabolism in extant life is centered around phosphate and the energy-dense phosphoanhydride bonds of adenosine triphosphate (ATP), a deeply conserved and ancient bioenergetic system. Yet, ATP synthesis relies on numerous complex enzymes and has an autocatalytic requirement for ATP itself. Th...

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Autores principales: Nicholls, Jack W. F., Chin, Jason P., Williams, Tom A., Lenton, Timothy M., O’Flaherty, Vincent, McGrath, John W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433651/
https://www.ncbi.nlm.nih.gov/pubmed/37601379
http://dx.doi.org/10.3389/fmicb.2023.1239189
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author Nicholls, Jack W. F.
Chin, Jason P.
Williams, Tom A.
Lenton, Timothy M.
O’Flaherty, Vincent
McGrath, John W.
author_facet Nicholls, Jack W. F.
Chin, Jason P.
Williams, Tom A.
Lenton, Timothy M.
O’Flaherty, Vincent
McGrath, John W.
author_sort Nicholls, Jack W. F.
collection PubMed
description Energy metabolism in extant life is centered around phosphate and the energy-dense phosphoanhydride bonds of adenosine triphosphate (ATP), a deeply conserved and ancient bioenergetic system. Yet, ATP synthesis relies on numerous complex enzymes and has an autocatalytic requirement for ATP itself. This implies the existence of evolutionarily simpler bioenergetic pathways and potentially primordial alternatives to ATP. The centrality of phosphate in modern bioenergetics, coupled with the energetic properties of phosphorylated compounds, may suggest that primordial precursors to ATP also utilized phosphate in compounds such as pyrophosphate, acetyl phosphate and polyphosphate. However, bioavailable phosphate may have been notably scarce on the early Earth, raising doubts about the roles that phosphorylated molecules might have played in the early evolution of life. A largely overlooked phosphorus redox cycle on the ancient Earth might have provided phosphorus and energy, with reduced phosphorus compounds potentially playing a key role in the early evolution of energy metabolism. Here, we speculate on the biological phosphorus compounds that may have acted as primordial energy currencies, sources of environmental energy, or sources of phosphorus for the synthesis of phosphorylated energy currencies. This review encompasses discussions on the evolutionary history of modern bioenergetics, and specifically those pathways with primordial relevance, and the geochemistry of bioavailable phosphorus on the ancient Earth. We highlight the importance of phosphorus, not only in the form of phosphate, to early biology and suggest future directions of study that may improve our understanding of the early evolution of bioenergetics.
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spelling pubmed-104336512023-08-18 On the potential roles of phosphorus in the early evolution of energy metabolism Nicholls, Jack W. F. Chin, Jason P. Williams, Tom A. Lenton, Timothy M. O’Flaherty, Vincent McGrath, John W. Front Microbiol Microbiology Energy metabolism in extant life is centered around phosphate and the energy-dense phosphoanhydride bonds of adenosine triphosphate (ATP), a deeply conserved and ancient bioenergetic system. Yet, ATP synthesis relies on numerous complex enzymes and has an autocatalytic requirement for ATP itself. This implies the existence of evolutionarily simpler bioenergetic pathways and potentially primordial alternatives to ATP. The centrality of phosphate in modern bioenergetics, coupled with the energetic properties of phosphorylated compounds, may suggest that primordial precursors to ATP also utilized phosphate in compounds such as pyrophosphate, acetyl phosphate and polyphosphate. However, bioavailable phosphate may have been notably scarce on the early Earth, raising doubts about the roles that phosphorylated molecules might have played in the early evolution of life. A largely overlooked phosphorus redox cycle on the ancient Earth might have provided phosphorus and energy, with reduced phosphorus compounds potentially playing a key role in the early evolution of energy metabolism. Here, we speculate on the biological phosphorus compounds that may have acted as primordial energy currencies, sources of environmental energy, or sources of phosphorus for the synthesis of phosphorylated energy currencies. This review encompasses discussions on the evolutionary history of modern bioenergetics, and specifically those pathways with primordial relevance, and the geochemistry of bioavailable phosphorus on the ancient Earth. We highlight the importance of phosphorus, not only in the form of phosphate, to early biology and suggest future directions of study that may improve our understanding of the early evolution of bioenergetics. Frontiers Media S.A. 2023-08-02 /pmc/articles/PMC10433651/ /pubmed/37601379 http://dx.doi.org/10.3389/fmicb.2023.1239189 Text en Copyright © 2023 Nicholls, Chin, Williams, Lenton, O’Flaherty and McGrath. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Nicholls, Jack W. F.
Chin, Jason P.
Williams, Tom A.
Lenton, Timothy M.
O’Flaherty, Vincent
McGrath, John W.
On the potential roles of phosphorus in the early evolution of energy metabolism
title On the potential roles of phosphorus in the early evolution of energy metabolism
title_full On the potential roles of phosphorus in the early evolution of energy metabolism
title_fullStr On the potential roles of phosphorus in the early evolution of energy metabolism
title_full_unstemmed On the potential roles of phosphorus in the early evolution of energy metabolism
title_short On the potential roles of phosphorus in the early evolution of energy metabolism
title_sort on the potential roles of phosphorus in the early evolution of energy metabolism
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433651/
https://www.ncbi.nlm.nih.gov/pubmed/37601379
http://dx.doi.org/10.3389/fmicb.2023.1239189
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