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The Emergence and Early Evolution of Biological Carbon-Fixation

The fixation of [Image: see text] into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstru...

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Autores principales: Braakman, Rogier, Smith, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3334880/
https://www.ncbi.nlm.nih.gov/pubmed/22536150
http://dx.doi.org/10.1371/journal.pcbi.1002455
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author Braakman, Rogier
Smith, Eric
author_facet Braakman, Rogier
Smith, Eric
author_sort Braakman, Rogier
collection PubMed
description The fixation of [Image: see text] into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of [Image: see text] reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a “phylometabolic” tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form.
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spelling pubmed-33348802012-04-25 The Emergence and Early Evolution of Biological Carbon-Fixation Braakman, Rogier Smith, Eric PLoS Comput Biol Research Article The fixation of [Image: see text] into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of [Image: see text] reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a “phylometabolic” tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form. Public Library of Science 2012-04-19 /pmc/articles/PMC3334880/ /pubmed/22536150 http://dx.doi.org/10.1371/journal.pcbi.1002455 Text en Braakman, Smith. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Braakman, Rogier
Smith, Eric
The Emergence and Early Evolution of Biological Carbon-Fixation
title The Emergence and Early Evolution of Biological Carbon-Fixation
title_full The Emergence and Early Evolution of Biological Carbon-Fixation
title_fullStr The Emergence and Early Evolution of Biological Carbon-Fixation
title_full_unstemmed The Emergence and Early Evolution of Biological Carbon-Fixation
title_short The Emergence and Early Evolution of Biological Carbon-Fixation
title_sort emergence and early evolution of biological carbon-fixation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3334880/
https://www.ncbi.nlm.nih.gov/pubmed/22536150
http://dx.doi.org/10.1371/journal.pcbi.1002455
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