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Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase

The sodium -pumping NADH: ubiquinone oxidoreductase (Na(+)-NQR) is the main ion pump and the primary entry site for electrons into the respiratory chain of many different types of pathogenic bacteria. This enzymatic complex creates a transmembrane gradient of sodium that is used by the cell to susta...

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Autores principales: Reyes-Prieto, Adrian, Barquera, Blanca, Juárez, Oscar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4014512/
https://www.ncbi.nlm.nih.gov/pubmed/24809444
http://dx.doi.org/10.1371/journal.pone.0096696
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author Reyes-Prieto, Adrian
Barquera, Blanca
Juárez, Oscar
author_facet Reyes-Prieto, Adrian
Barquera, Blanca
Juárez, Oscar
author_sort Reyes-Prieto, Adrian
collection PubMed
description The sodium -pumping NADH: ubiquinone oxidoreductase (Na(+)-NQR) is the main ion pump and the primary entry site for electrons into the respiratory chain of many different types of pathogenic bacteria. This enzymatic complex creates a transmembrane gradient of sodium that is used by the cell to sustain ionic homeostasis, nutrient transport, ATP synthesis, flagellum rotation and other essential processes. Comparative genomics data demonstrate that the nqr operon, which encodes all Na(+)-NQR subunits, is found in a large variety of bacterial lineages with different habitats and metabolic strategies. Here we studied the distribution, origin and evolution of this enzymatic complex. The molecular phylogenetic analyses and the organizations of the nqr operon indicate that Na(+)-NQR evolved within the Chlorobi/Bacteroidetes group, after the duplication and subsequent neofunctionalization of the operon that encodes the homolog RNF complex. Subsequently, the nqr operon dispersed through multiple horizontal transfer events to other bacterial lineages such as Chlamydiae, Planctomyces and α, β, γ and δ -proteobacteria. Considering the biochemical properties of the Na(+)-NQR complex and its physiological role in different bacteria, we propose a detailed scenario to explain the molecular mechanisms that gave rise to its novel redox- dependent sodium -pumping activity. Our model postulates that the evolution of the Na(+)-NQR complex involved a functional divergence from its RNF homolog, following the duplication of the rnf operon, the loss of the rnfB gene and the recruitment of the reductase subunit of an aromatic monooxygenase.
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spelling pubmed-40145122014-05-14 Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase Reyes-Prieto, Adrian Barquera, Blanca Juárez, Oscar PLoS One Research Article The sodium -pumping NADH: ubiquinone oxidoreductase (Na(+)-NQR) is the main ion pump and the primary entry site for electrons into the respiratory chain of many different types of pathogenic bacteria. This enzymatic complex creates a transmembrane gradient of sodium that is used by the cell to sustain ionic homeostasis, nutrient transport, ATP synthesis, flagellum rotation and other essential processes. Comparative genomics data demonstrate that the nqr operon, which encodes all Na(+)-NQR subunits, is found in a large variety of bacterial lineages with different habitats and metabolic strategies. Here we studied the distribution, origin and evolution of this enzymatic complex. The molecular phylogenetic analyses and the organizations of the nqr operon indicate that Na(+)-NQR evolved within the Chlorobi/Bacteroidetes group, after the duplication and subsequent neofunctionalization of the operon that encodes the homolog RNF complex. Subsequently, the nqr operon dispersed through multiple horizontal transfer events to other bacterial lineages such as Chlamydiae, Planctomyces and α, β, γ and δ -proteobacteria. Considering the biochemical properties of the Na(+)-NQR complex and its physiological role in different bacteria, we propose a detailed scenario to explain the molecular mechanisms that gave rise to its novel redox- dependent sodium -pumping activity. Our model postulates that the evolution of the Na(+)-NQR complex involved a functional divergence from its RNF homolog, following the duplication of the rnf operon, the loss of the rnfB gene and the recruitment of the reductase subunit of an aromatic monooxygenase. Public Library of Science 2014-05-08 /pmc/articles/PMC4014512/ /pubmed/24809444 http://dx.doi.org/10.1371/journal.pone.0096696 Text en © 2014 Reyes-Prieto et al 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
Reyes-Prieto, Adrian
Barquera, Blanca
Juárez, Oscar
Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_full Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_fullStr Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_full_unstemmed Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_short Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_sort origin and evolution of the sodium -pumping nadh: ubiquinone oxidoreductase
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4014512/
https://www.ncbi.nlm.nih.gov/pubmed/24809444
http://dx.doi.org/10.1371/journal.pone.0096696
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