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Basic regulatory principles of Escherichia coli's electron transport chain for varying oxygen conditions
For adaptation between anaerobic, micro-aerobic and aerobic conditions Escherichia coli's metabolism and in particular its electron transport chain (ETC) is highly regulated. Although it is known that the global transcriptional regulators FNR and ArcA are involved in oxygen response it is uncle...
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Published in: | PloS one 2014-09, Vol.9 (9), p.e107640-e107640 |
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description | For adaptation between anaerobic, micro-aerobic and aerobic conditions Escherichia coli's metabolism and in particular its electron transport chain (ETC) is highly regulated. Although it is known that the global transcriptional regulators FNR and ArcA are involved in oxygen response it is unclear how they interplay in the regulation of ETC enzymes under micro-aerobic chemostat conditions. Also, there are diverse results which and how quinones (oxidised/reduced, ubiquinone/other quinones) are controlling the ArcBA two-component system. In the following a mathematical model of the E. coli ETC linked to basic modules for substrate uptake, fermentation product excretion and biomass formation is introduced. The kinetic modelling focusses on regulatory principles of the ETC for varying oxygen conditions in glucose-limited continuous cultures. The model is based on the balance of electron donation (glucose) and acceptance (oxygen or other acceptors). Also, it is able to account for different chemostat conditions due to changed substrate concentrations and dilution rates. The parameter identification process is divided into an estimation and a validation step based on previously published and new experimental data. The model shows that experimentally observed, qualitatively different behaviour of the ubiquinone redox state and the ArcA activity profile in the micro-aerobic range for different experimental conditions can emerge from a single network structure. The network structure features a strong feed-forward effect from the FNR regulatory system to the ArcBA regulatory system via a common control of the dehydrogenases of the ETC. The model supports the hypothesis that ubiquinone but not ubiquinol plays a key role in determining the activity of ArcBA in a glucose-limited chemostat at micro-aerobic conditions. |
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Although it is known that the global transcriptional regulators FNR and ArcA are involved in oxygen response it is unclear how they interplay in the regulation of ETC enzymes under micro-aerobic chemostat conditions. Also, there are diverse results which and how quinones (oxidised/reduced, ubiquinone/other quinones) are controlling the ArcBA two-component system. In the following a mathematical model of the E. coli ETC linked to basic modules for substrate uptake, fermentation product excretion and biomass formation is introduced. The kinetic modelling focusses on regulatory principles of the ETC for varying oxygen conditions in glucose-limited continuous cultures. The model is based on the balance of electron donation (glucose) and acceptance (oxygen or other acceptors). Also, it is able to account for different chemostat conditions due to changed substrate concentrations and dilution rates. The parameter identification process is divided into an estimation and a validation step based on previously published and new experimental data. The model shows that experimentally observed, qualitatively different behaviour of the ubiquinone redox state and the ArcA activity profile in the micro-aerobic range for different experimental conditions can emerge from a single network structure. The network structure features a strong feed-forward effect from the FNR regulatory system to the ArcBA regulatory system via a common control of the dehydrogenases of the ETC. The model supports the hypothesis that ubiquinone but not ubiquinol plays a key role in determining the activity of ArcBA in a glucose-limited chemostat at micro-aerobic conditions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0107640</identifier><identifier>PMID: 25268772</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Aerobic conditions ; Aerobiosis ; Anaerobic conditions ; Anaerobiosis ; Bacterial Outer Membrane Proteins - genetics ; Bacterial Outer Membrane Proteins - metabolism ; Biology ; Biology and Life Sciences ; Computer and Information Sciences ; Cytochrome ; Dehydrogenases ; Dilution ; E coli ; Electron Transport ; Electron transport chain ; Electron Transport Chain Complex Proteins - genetics ; Electron Transport Chain Complex Proteins - metabolism ; Electrons ; Enzymes ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - metabolism ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Excretion ; Fermentation ; Gene expression ; Glucose ; Kinases ; Kinetics ; Life sciences ; Mathematical models ; Metabolism ; Models, Biological ; Oxygen ; Oxygen - physiology ; Parameter identification ; Physiology ; Process parameters ; Quinones ; Redox properties ; Regulators ; Research and Analysis Methods ; Substrates ; Transcription ; Ubiquinol ; Ubiquinone</subject><ispartof>PloS one, 2014-09, Vol.9 (9), p.e107640-e107640</ispartof><rights>2014 Henkel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Henkel, Sebastian G</au><au>Ter Beek, Alexander</au><au>Steinsiek, Sonja</au><au>Stagge, Stefan</au><au>Bettenbrock, Katja</au><au>de Mattos, M Joost Teixeira</au><au>Sauter, Thomas</au><au>Sawodny, Oliver</au><au>Ederer, Michael</au><au>Torres, Néstor V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Basic regulatory principles of Escherichia coli's electron transport chain for varying oxygen conditions</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-09-30</date><risdate>2014</risdate><volume>9</volume><issue>9</issue><spage>e107640</spage><epage>e107640</epage><pages>e107640-e107640</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>For adaptation between anaerobic, micro-aerobic and aerobic conditions Escherichia coli's metabolism and in particular its electron transport chain (ETC) is highly regulated. Although it is known that the global transcriptional regulators FNR and ArcA are involved in oxygen response it is unclear how they interplay in the regulation of ETC enzymes under micro-aerobic chemostat conditions. Also, there are diverse results which and how quinones (oxidised/reduced, ubiquinone/other quinones) are controlling the ArcBA two-component system. In the following a mathematical model of the E. coli ETC linked to basic modules for substrate uptake, fermentation product excretion and biomass formation is introduced. The kinetic modelling focusses on regulatory principles of the ETC for varying oxygen conditions in glucose-limited continuous cultures. The model is based on the balance of electron donation (glucose) and acceptance (oxygen or other acceptors). Also, it is able to account for different chemostat conditions due to changed substrate concentrations and dilution rates. The parameter identification process is divided into an estimation and a validation step based on previously published and new experimental data. The model shows that experimentally observed, qualitatively different behaviour of the ubiquinone redox state and the ArcA activity profile in the micro-aerobic range for different experimental conditions can emerge from a single network structure. The network structure features a strong feed-forward effect from the FNR regulatory system to the ArcBA regulatory system via a common control of the dehydrogenases of the ETC. The model supports the hypothesis that ubiquinone but not ubiquinol plays a key role in determining the activity of ArcBA in a glucose-limited chemostat at micro-aerobic conditions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25268772</pmid><doi>10.1371/journal.pone.0107640</doi><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation Aerobic conditions Aerobiosis Anaerobic conditions Anaerobiosis Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Biology Biology and Life Sciences Computer and Information Sciences Cytochrome Dehydrogenases Dilution E coli Electron Transport Electron transport chain Electron Transport Chain Complex Proteins - genetics Electron Transport Chain Complex Proteins - metabolism Electrons Enzymes Escherichia coli Escherichia coli - genetics Escherichia coli - metabolism Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Excretion Fermentation Gene expression Glucose Kinases Kinetics Life sciences Mathematical models Metabolism Models, Biological Oxygen Oxygen - physiology Parameter identification Physiology Process parameters Quinones Redox properties Regulators Research and Analysis Methods Substrates Transcription Ubiquinol Ubiquinone |
title | Basic regulatory principles of Escherichia coli's electron transport chain for varying oxygen conditions |
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