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 sustain...

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Main Authors:	Reyes-Prieto, Adrian, Barquera, Blanca, Juárez, Oscar
Format:	Online
Language:	English
Published:	Public Library of Science 2014
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4014512/

id	pubmed-4014512
recordtype	oai_dc
spelling	pubmed-40145122014-05-14 Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase Reyes-Prieto, Adrian Barquera, Blanca Juárez, Oscar 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.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Reyes-Prieto, Adrian Barquera, Blanca Juárez, Oscar
spellingShingle	Reyes-Prieto, Adrian Barquera, Blanca Juárez, Oscar Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
author_facet	Reyes-Prieto, Adrian Barquera, Blanca Juárez, Oscar
author_sort	Reyes-Prieto, Adrian
title	Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase
title_short	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_sort	origin and evolution of the sodium -pumping nadh: ubiquinone oxidoreductase
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.
publisher	Public Library of Science
publishDate	2014
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4014512/
_version_	1612086754111651840

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

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