Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1

The facultative denitrifying alphaproteobacterium <i>Magnetospirillum</i> sp. strain 15-1 had been isolated from the hypoxic rhizosphere of a constructed wetland model fed with toluene. This bacterium can catabolize toluene anaerobically but not aerobically. Here, we used strain 15-1 to...

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Main Authors: Ingrid Meyer-Cifuentes, Sylvie Gruhl, Sven-Bastiaan Haange, Vanessa Lünsmann, Nico Jehmlich, Martin von Bergen, Hermann J. Heipieper, Jochen A. Müller
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/5/681
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author Ingrid Meyer-Cifuentes
Sylvie Gruhl
Sven-Bastiaan Haange
Vanessa Lünsmann
Nico Jehmlich
Martin von Bergen
Hermann J. Heipieper
Jochen A. Müller
author_facet Ingrid Meyer-Cifuentes
Sylvie Gruhl
Sven-Bastiaan Haange
Vanessa Lünsmann
Nico Jehmlich
Martin von Bergen
Hermann J. Heipieper
Jochen A. Müller
author_sort Ingrid Meyer-Cifuentes
collection DOAJ
description The facultative denitrifying alphaproteobacterium <i>Magnetospirillum</i> sp. strain 15-1 had been isolated from the hypoxic rhizosphere of a constructed wetland model fed with toluene. This bacterium can catabolize toluene anaerobically but not aerobically. Here, we used strain 15-1 to investigate regulation of expression of the highly oxygen-sensitive glycyl radical enzyme benzylsuccinate synthase, which catalyzes the first step in anaerobic toluene degradation. In cells growing aerobically with benzoate, the addition of toluene resulted in a ~20-fold increased transcription of <i>bssA</i>, encoding for the catalytically active subunit of the enzyme. Under anoxic conditions, <i>bssA</i> mRNA copy numbers were up to 129-fold higher in cells growing with toluene as compared to cells growing with benzoate. Proteomics showed that abundance of benzylsuccinate synthase increased in cells growing anaerobically with toluene. In contrast, peptides of this enzyme were never detected in oxic conditions. These findings show that synthesis of benzylsuccinate synthase was under stringent post-transcriptional control in the presence of oxygen, which is a novel level of regulation for glycyl radical enzymes.
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spelling doaj.art-d140e02713294464b40d845f2a2f1e7f2023-11-19T23:43:46ZengMDPI AGMicroorganisms2076-26072020-05-018568110.3390/microorganisms8050681Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1Ingrid Meyer-Cifuentes0Sylvie Gruhl1Sven-Bastiaan Haange2Vanessa Lünsmann3Nico Jehmlich4Martin von Bergen5Hermann J. Heipieper6Jochen A. Müller7Department of Environmental Biotechnology, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Environmental Biotechnology, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Molecular Systems Biology Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Molecular Systems Biology Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Molecular Systems Biology Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Molecular Systems Biology Helmholtz Centre for Environmental Research-UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Environmental Biotechnology, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, GermanyDepartment of Environmental Biotechnology, Helmholtz Centre for Environmental Research - UFZ, Permoserstr. 15, 04318 Leipzig, GermanyThe facultative denitrifying alphaproteobacterium <i>Magnetospirillum</i> sp. strain 15-1 had been isolated from the hypoxic rhizosphere of a constructed wetland model fed with toluene. This bacterium can catabolize toluene anaerobically but not aerobically. Here, we used strain 15-1 to investigate regulation of expression of the highly oxygen-sensitive glycyl radical enzyme benzylsuccinate synthase, which catalyzes the first step in anaerobic toluene degradation. In cells growing aerobically with benzoate, the addition of toluene resulted in a ~20-fold increased transcription of <i>bssA</i>, encoding for the catalytically active subunit of the enzyme. Under anoxic conditions, <i>bssA</i> mRNA copy numbers were up to 129-fold higher in cells growing with toluene as compared to cells growing with benzoate. Proteomics showed that abundance of benzylsuccinate synthase increased in cells growing anaerobically with toluene. In contrast, peptides of this enzyme were never detected in oxic conditions. These findings show that synthesis of benzylsuccinate synthase was under stringent post-transcriptional control in the presence of oxygen, which is a novel level of regulation for glycyl radical enzymes.https://www.mdpi.com/2076-2607/8/5/681toluenenitratebenzylsuccinate synthase<i>Magnetospirillum</i>rhizosphere
spellingShingle Ingrid Meyer-Cifuentes
Sylvie Gruhl
Sven-Bastiaan Haange
Vanessa Lünsmann
Nico Jehmlich
Martin von Bergen
Hermann J. Heipieper
Jochen A. Müller
Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
Microorganisms
toluene
nitrate
benzylsuccinate synthase
<i>Magnetospirillum</i>
rhizosphere
title Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
title_full Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
title_fullStr Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
title_full_unstemmed Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
title_short Benzylsuccinate Synthase is Post-Transcriptionally Regulated in the Toluene-Degrading Denitrifier <i>Magnetospirillum</i> sp. Strain 15-1
title_sort benzylsuccinate synthase is post transcriptionally regulated in the toluene degrading denitrifier i magnetospirillum i sp strain 15 1
topic toluene
nitrate
benzylsuccinate synthase
<i>Magnetospirillum</i>
rhizosphere
url https://www.mdpi.com/2076-2607/8/5/681
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