Gene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion.

2.50
Hdl Handle:
http://hdl.handle.net/10033/621020
Title:
Gene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion.
Authors:
Laass, Sebastian; Kleist, Sarah; Bill, Nelli; Drüppel, Katharina; Kossmehl, Sebastian; Wöhlbrand, Lars; Rabus, Ralf; Klein, Johannes; Rohde, Manfred; Bartsch, Annekathrin; Wittmann, Christoph; Schmidt-Hohagen, Kerstin; Tielen, Petra; Jahn, Dieter; Schomburg, Dietmar
Abstract:
Metabolic flexibility is the key to the ecological success of the marine Roseobacter clade bacteria. We investigated the metabolic adaptation and the underlying changes in gene expression of Dinoroseobacter shibae DFL12(T) to anoxic life by a combination of metabolome, proteome, and transcriptome analyses. Time-resolved studies during continuous oxygen depletion were performed in a chemostat using nitrate as the terminal electron acceptor. Formation of the denitrification machinery was found enhanced on the transcriptional and proteome level, indicating that D. shibae DFL12(T) established nitrate respiration to compensate for the depletion of the electron acceptor oxygen. In parallel, arginine fermentation was induced. During the transition state, growth and ATP concentration were found to be reduced, as reflected by a decrease of A578 values and viable cell counts. In parallel, the central metabolism, including gluconeogenesis, protein biosynthesis, and purine/pyrimidine synthesis was found transiently reduced in agreement with the decreased demand for cellular building blocks. Surprisingly, an accumulation of poly-3-hydroxybutanoate was observed during prolonged incubation under anoxic conditions. One possible explanation is the storage of accumulated metabolites and the regeneration of NADP(+) from NADPH during poly-3-hydroxybutanoate synthesis (NADPH sink). Although D. shibae DFL12(T) was cultivated in the dark, biosynthesis of bacteriochlorophyll was increased, possibly to prepare for additional energy generation via aerobic anoxygenic photophosphorylation. Overall, oxygen depletion led to a metabolic crisis with partly blocked pathways and the accumulation of metabolites. In response, major energy-consuming processes were reduced until the alternative respiratory denitrification machinery was operative.
Affiliation:
Helmholtz-Zentrum für Infektionsforschung, Inhoffenstr. 7, 38124 Braunschweig, Germany.
Citation:
Gene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion. 2014, 289 (19):13219-31 J. Biol. Chem.
Journal:
The Journal of biological chemistry
Issue Date:
9-May-2014
URI:
http://hdl.handle.net/10033/621020
DOI:
10.1074/jbc.M113.545004
PubMed ID:
24648520
Type:
Article
Language:
en
ISSN:
1083-351X
Appears in Collections:
publications of the central unit for microscopy (ZEIM)

Full metadata record

DC FieldValue Language
dc.contributor.authorLaass, Sebastianen
dc.contributor.authorKleist, Sarahen
dc.contributor.authorBill, Nellien
dc.contributor.authorDrüppel, Katharinaen
dc.contributor.authorKossmehl, Sebastianen
dc.contributor.authorWöhlbrand, Larsen
dc.contributor.authorRabus, Ralfen
dc.contributor.authorKlein, Johannesen
dc.contributor.authorRohde, Manfreden
dc.contributor.authorBartsch, Annekathrinen
dc.contributor.authorWittmann, Christophen
dc.contributor.authorSchmidt-Hohagen, Kerstinen
dc.contributor.authorTielen, Petraen
dc.contributor.authorJahn, Dieteren
dc.contributor.authorSchomburg, Dietmaren
dc.date.accessioned2017-07-25T14:37:36Z-
dc.date.available2017-07-25T14:37:36Z-
dc.date.issued2014-05-09-
dc.identifier.citationGene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion. 2014, 289 (19):13219-31 J. Biol. Chem.en
dc.identifier.issn1083-351X-
dc.identifier.pmid24648520-
dc.identifier.doi10.1074/jbc.M113.545004-
dc.identifier.urihttp://hdl.handle.net/10033/621020-
dc.description.abstractMetabolic flexibility is the key to the ecological success of the marine Roseobacter clade bacteria. We investigated the metabolic adaptation and the underlying changes in gene expression of Dinoroseobacter shibae DFL12(T) to anoxic life by a combination of metabolome, proteome, and transcriptome analyses. Time-resolved studies during continuous oxygen depletion were performed in a chemostat using nitrate as the terminal electron acceptor. Formation of the denitrification machinery was found enhanced on the transcriptional and proteome level, indicating that D. shibae DFL12(T) established nitrate respiration to compensate for the depletion of the electron acceptor oxygen. In parallel, arginine fermentation was induced. During the transition state, growth and ATP concentration were found to be reduced, as reflected by a decrease of A578 values and viable cell counts. In parallel, the central metabolism, including gluconeogenesis, protein biosynthesis, and purine/pyrimidine synthesis was found transiently reduced in agreement with the decreased demand for cellular building blocks. Surprisingly, an accumulation of poly-3-hydroxybutanoate was observed during prolonged incubation under anoxic conditions. One possible explanation is the storage of accumulated metabolites and the regeneration of NADP(+) from NADPH during poly-3-hydroxybutanoate synthesis (NADPH sink). Although D. shibae DFL12(T) was cultivated in the dark, biosynthesis of bacteriochlorophyll was increased, possibly to prepare for additional energy generation via aerobic anoxygenic photophosphorylation. Overall, oxygen depletion led to a metabolic crisis with partly blocked pathways and the accumulation of metabolites. In response, major energy-consuming processes were reduced until the alternative respiratory denitrification machinery was operative.en
dc.language.isoenen
dc.subject.meshAdaptation, Physiologicalen
dc.subject.meshBacterial Proteinsen
dc.subject.meshDenitrificationen
dc.subject.meshGene Expression Regulation, Bacterialen
dc.subject.meshOxygen Consumptionen
dc.subject.meshRhodobacteraceaeen
dc.titleGene regulatory and metabolic adaptation processes of Dinoroseobacter shibae DFL12T during oxygen depletion.en
dc.typeArticleen
dc.contributor.departmentHelmholtz-Zentrum für Infektionsforschung, Inhoffenstr. 7, 38124 Braunschweig, Germany.en
dc.identifier.journalThe Journal of biological chemistryen

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