Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>

Replacement of the <i>Lactobacillus</i> dominated vaginal microbiome by a mixed bacterial population including <i>Prevotella bivia</i> is associated with bacterial vaginosis (BV). To understand the impact of <i>P. bivia</i> on this microbiome, its growth requireme...

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Autores principales: Lena Schleicher, Sebastian Herdan, Günter Fritz, Andrej Trautmann, Jana Seifert, Julia Steuber
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Publicado: MDPI AG 2021
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Acceso en línea:https://doaj.org/article/174589f050bc489788c6e24cbb940c9b
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spelling oai:doaj.org-article:174589f050bc489788c6e24cbb940c9b2021-11-11T17:20:33ZCentral Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>10.3390/ijms2221119251422-00671661-6596https://doaj.org/article/174589f050bc489788c6e24cbb940c9b2021-11-01T00:00:00Zhttps://www.mdpi.com/1422-0067/22/21/11925https://doaj.org/toc/1661-6596https://doaj.org/toc/1422-0067Replacement of the <i>Lactobacillus</i> dominated vaginal microbiome by a mixed bacterial population including <i>Prevotella bivia</i> is associated with bacterial vaginosis (BV). To understand the impact of <i>P. bivia</i> on this microbiome, its growth requirements and mode of energy production were studied. Anoxic growth with glucose depended on CO<sub>2</sub> and resulted in succinate formation, indicating phosphoenolpyruvate carboxylation and fumarate reduction as critical steps. The reductive branch of fermentation relied on two highly active, membrane-bound enzymes, namely the quinol:fumarate reductase (QFR) and Na<sup>+</sup>-translocating NADH:quinone oxidoreductase (NQR). Both enzymes were characterized by activity measurements, in-gel fluorography, and VIS difference spectroscopy, and the Na<sup>+</sup>-dependent build-up of a transmembrane voltage was demonstrated. NQR is a potential drug target for BV treatment since it is neither found in humans nor in <i>Lactobacillus</i>. In <i>P. bivia</i>, the highly active enzymes L-asparaginase and aspartate ammonia lyase catalyze the conversion of asparagine to the electron acceptor fumarate. However, the by-product ammonium is highly toxic. It has been proposed that <i>P. bivia</i> depends on ammonium-utilizing <i>Gardnerella vaginalis</i>, another typical pathogen associated with BV, and provides key nutrients to it. The product pattern of <i>P. bivia</i> growing on glucose in the presence of mixed amino acids substantiates this notion.Lena SchleicherSebastian HerdanGünter FritzAndrej TrautmannJana SeifertJulia SteuberMDPI AGarticlebacterial vaginosis<i>Prevotella bivia</i>Na<sup>+</sup>-translocating NADH:quinone oxidoreductasefumarate reductaseamino acid degradationBiology (General)QH301-705.5ChemistryQD1-999ENInternational Journal of Molecular Sciences, Vol 22, Iss 11925, p 11925 (2021)
institution DOAJ
collection DOAJ
language EN
topic bacterial vaginosis
<i>Prevotella bivia</i>
Na<sup>+</sup>-translocating NADH:quinone oxidoreductase
fumarate reductase
amino acid degradation
Biology (General)
QH301-705.5
Chemistry
QD1-999
spellingShingle bacterial vaginosis
<i>Prevotella bivia</i>
Na<sup>+</sup>-translocating NADH:quinone oxidoreductase
fumarate reductase
amino acid degradation
Biology (General)
QH301-705.5
Chemistry
QD1-999
Lena Schleicher
Sebastian Herdan
Günter Fritz
Andrej Trautmann
Jana Seifert
Julia Steuber
Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
description Replacement of the <i>Lactobacillus</i> dominated vaginal microbiome by a mixed bacterial population including <i>Prevotella bivia</i> is associated with bacterial vaginosis (BV). To understand the impact of <i>P. bivia</i> on this microbiome, its growth requirements and mode of energy production were studied. Anoxic growth with glucose depended on CO<sub>2</sub> and resulted in succinate formation, indicating phosphoenolpyruvate carboxylation and fumarate reduction as critical steps. The reductive branch of fermentation relied on two highly active, membrane-bound enzymes, namely the quinol:fumarate reductase (QFR) and Na<sup>+</sup>-translocating NADH:quinone oxidoreductase (NQR). Both enzymes were characterized by activity measurements, in-gel fluorography, and VIS difference spectroscopy, and the Na<sup>+</sup>-dependent build-up of a transmembrane voltage was demonstrated. NQR is a potential drug target for BV treatment since it is neither found in humans nor in <i>Lactobacillus</i>. In <i>P. bivia</i>, the highly active enzymes L-asparaginase and aspartate ammonia lyase catalyze the conversion of asparagine to the electron acceptor fumarate. However, the by-product ammonium is highly toxic. It has been proposed that <i>P. bivia</i> depends on ammonium-utilizing <i>Gardnerella vaginalis</i>, another typical pathogen associated with BV, and provides key nutrients to it. The product pattern of <i>P. bivia</i> growing on glucose in the presence of mixed amino acids substantiates this notion.
format article
author Lena Schleicher
Sebastian Herdan
Günter Fritz
Andrej Trautmann
Jana Seifert
Julia Steuber
author_facet Lena Schleicher
Sebastian Herdan
Günter Fritz
Andrej Trautmann
Jana Seifert
Julia Steuber
author_sort Lena Schleicher
title Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
title_short Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
title_full Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
title_fullStr Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
title_full_unstemmed Central Carbon Metabolism, Sodium-Motive Electron Transfer, and Ammonium Formation by the Vaginal Pathogen <i>Prevotella bivia</i>
title_sort central carbon metabolism, sodium-motive electron transfer, and ammonium formation by the vaginal pathogen <i>prevotella bivia</i>
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/174589f050bc489788c6e24cbb940c9b
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