Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient

Salt tolerance in the γ-proteobacterium Halomonas elongata is linked to its ability to produce the compatible solute ectoine. The metabolism of ectoine production is of great interest since it can shed light on the biochemical basis of halotolerance as well as pave the way for the improvement of the...

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Autores: Hobmeier, Karina, Goëss, Marie C., Sehr, Christiana, Schwaminger, Sebastian, Berensmeier, Sonja, Kremling, Andreas, Kunte, Hans Jörg, Pflüger Grau, Katharina, Marin-Sanguino, Alberto
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Universitat de Lleida (UdL)
Repositorio:Repositori Obert UdL
OAI Identifier:oai:repositori.udl.cat:10459.1/467724
Acceso en línea:https://doi.org/10.3389/fmicb.2020.561800
https://hdl.handle.net/10459.1/467724
Access Level:acceso abierto
Palabra clave:Thermodynamics-based metabolic flux analysis
Halophilic bacteria
Metabolic modeling
Design principles
Biochemistry and metabolism
Halomonas elongata
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spelling Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium GradientHobmeier, KarinaGoëss, Marie C.Sehr, ChristianaSchwaminger, SebastianBerensmeier, SonjaKremling, AndreasKunte, Hans JörgPflüger Grau, KatharinaMarin-Sanguino, AlbertoThermodynamics-based metabolic flux analysisHalophilic bacteriaMetabolic modelingDesign principlesBiochemistry and metabolismHalomonas elongataSalt tolerance in the γ-proteobacterium Halomonas elongata is linked to its ability to produce the compatible solute ectoine. The metabolism of ectoine production is of great interest since it can shed light on the biochemical basis of halotolerance as well as pave the way for the improvement of the biotechnological production of such compatible solute. Ectoine belongs to the biosynthetic family of aspartate-derived amino-acids. Aspartate is formed from oxaloacetate, thereby connecting ectoine production to the anaplerotic reactions that refill carbon into the tricarboxylic acid cycle (TCA cycle). This places a high demand on these reactions and creates the need to regulate them not only in response to growth but also in response to extracellular salt concentration. In this work, we combine modeling and experiments to analyze how these different needs shape the anaplerotic reactions in H. elongata. First, the stoichiometric and thermodynamic factors that condition the flux distributions are analyzed, then the optimal patterns of operation for oxaloacetate production are calculated. Finally, the phenotype of two deletion mutants lacking potentially relevant anaplerotic enzymes: phosphoenolpyruvate carboxylase (Ppc) and oxaloacetate decarboxylase (Oad) are experimentally characterized. The results show that the anaplerotic reactions in H. elongata are indeed subject to evolutionary pressures that differ from those faced by other gram-negative bacteria. Ectoine producing halophiles must meet a higher metabolic demand for oxaloacetate and the reliance of many marine bacteria on the Entner-Doudoroff pathway compromises the anaplerotic efficiency of Ppc, which is usually one of the main enzymes fulfilling this role. The anaplerotic flux in H. elongata is contributed not only by Ppc but also by Oad, an enzyme that has not yet been shown to play this role in vivo. Ppc is necessary for H. elongata to grow normally at low salt concentrations but it is not required to achieve near maximal growth rates as long as there is a steep sodium gradient. On the other hand, the lack of Oad presents serious difficulties to grow at high salt concentrations. This points to a shared role of these two enzymes in guaranteeing the supply of oxaloacetate for biosynthetic reactions.Frontiers Media2020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://doi.org/10.3389/fmicb.2020.561800https://hdl.handle.net/10459.1/467724reponame:Repositori Obert UdL instname:Universitat de Lleida (UdL)InglésReproducció del document publicat a: https://doi.org/10.3389/fmicb.2020.561800Frontiers in Microbiology, 2020, vol. 11, Article 561800cc-by (c)The Authors, 2020Attribution 4.0 Internationalinfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/4.0/oai:repositori.udl.cat:10459.1/4677242026-06-24T12:42:17Z
dc.title.none.fl_str_mv Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
title Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
spellingShingle Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
Hobmeier, Karina
Thermodynamics-based metabolic flux analysis
Halophilic bacteria
Metabolic modeling
Design principles
Biochemistry and metabolism
Halomonas elongata
title_short Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
title_full Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
title_fullStr Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
title_full_unstemmed Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
title_sort Anaplerotic Pathways in Halomonas elongata: The Role of the Sodium Gradient
dc.creator.none.fl_str_mv Hobmeier, Karina
Goëss, Marie C.
Sehr, Christiana
Schwaminger, Sebastian
Berensmeier, Sonja
Kremling, Andreas
Kunte, Hans Jörg
Pflüger Grau, Katharina
Marin-Sanguino, Alberto
author Hobmeier, Karina
author_facet Hobmeier, Karina
Goëss, Marie C.
Sehr, Christiana
Schwaminger, Sebastian
Berensmeier, Sonja
Kremling, Andreas
Kunte, Hans Jörg
Pflüger Grau, Katharina
Marin-Sanguino, Alberto
author_role author
author2 Goëss, Marie C.
Sehr, Christiana
Schwaminger, Sebastian
Berensmeier, Sonja
Kremling, Andreas
Kunte, Hans Jörg
Pflüger Grau, Katharina
Marin-Sanguino, Alberto
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Thermodynamics-based metabolic flux analysis
Halophilic bacteria
Metabolic modeling
Design principles
Biochemistry and metabolism
Halomonas elongata
topic Thermodynamics-based metabolic flux analysis
Halophilic bacteria
Metabolic modeling
Design principles
Biochemistry and metabolism
Halomonas elongata
description Salt tolerance in the γ-proteobacterium Halomonas elongata is linked to its ability to produce the compatible solute ectoine. The metabolism of ectoine production is of great interest since it can shed light on the biochemical basis of halotolerance as well as pave the way for the improvement of the biotechnological production of such compatible solute. Ectoine belongs to the biosynthetic family of aspartate-derived amino-acids. Aspartate is formed from oxaloacetate, thereby connecting ectoine production to the anaplerotic reactions that refill carbon into the tricarboxylic acid cycle (TCA cycle). This places a high demand on these reactions and creates the need to regulate them not only in response to growth but also in response to extracellular salt concentration. In this work, we combine modeling and experiments to analyze how these different needs shape the anaplerotic reactions in H. elongata. First, the stoichiometric and thermodynamic factors that condition the flux distributions are analyzed, then the optimal patterns of operation for oxaloacetate production are calculated. Finally, the phenotype of two deletion mutants lacking potentially relevant anaplerotic enzymes: phosphoenolpyruvate carboxylase (Ppc) and oxaloacetate decarboxylase (Oad) are experimentally characterized. The results show that the anaplerotic reactions in H. elongata are indeed subject to evolutionary pressures that differ from those faced by other gram-negative bacteria. Ectoine producing halophiles must meet a higher metabolic demand for oxaloacetate and the reliance of many marine bacteria on the Entner-Doudoroff pathway compromises the anaplerotic efficiency of Ppc, which is usually one of the main enzymes fulfilling this role. The anaplerotic flux in H. elongata is contributed not only by Ppc but also by Oad, an enzyme that has not yet been shown to play this role in vivo. Ppc is necessary for H. elongata to grow normally at low salt concentrations but it is not required to achieve near maximal growth rates as long as there is a steep sodium gradient. On the other hand, the lack of Oad presents serious difficulties to grow at high salt concentrations. This points to a shared role of these two enzymes in guaranteeing the supply of oxaloacetate for biosynthetic reactions.
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.3389/fmicb.2020.561800
https://hdl.handle.net/10459.1/467724
url https://doi.org/10.3389/fmicb.2020.561800
https://hdl.handle.net/10459.1/467724
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.3389/fmicb.2020.561800
Frontiers in Microbiology, 2020, vol. 11, Article 561800
dc.rights.none.fl_str_mv cc-by (c)The Authors, 2020
Attribution 4.0 International
info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by/4.0/
rights_invalid_str_mv cc-by (c)The Authors, 2020
Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Repositori Obert UdL
instname:Universitat de Lleida (UdL)
instname_str Universitat de Lleida (UdL)
reponame_str Repositori Obert UdL
collection Repositori Obert UdL
repository.name.fl_str_mv
repository.mail.fl_str_mv
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