The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain
In condition of over-expression, SCO3201, a regulator of the TetR family was previously shown to strongly inhibit antibiotic production and morphological differentiation in Streptomyces coelicolor M145. In order to elucidate the molecular processes underlying this interesting, but poorly understood...
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Frontiers Media S.A.
2020-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01399/full |
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| author | Jun Zhang Qiting Liang Zhongheng Xu Miao Cui Qizhong Zhang Sonia Abreu Michelle David Clara Lejeune Pierre Chaminade Marie-Joelle Virolle Delin Xu |
| author_facet | Jun Zhang Qiting Liang Zhongheng Xu Miao Cui Qizhong Zhang Sonia Abreu Michelle David Clara Lejeune Pierre Chaminade Marie-Joelle Virolle Delin Xu |
| author_sort | Jun Zhang |
| collection | DOAJ |
| description | In condition of over-expression, SCO3201, a regulator of the TetR family was previously shown to strongly inhibit antibiotic production and morphological differentiation in Streptomyces coelicolor M145. In order to elucidate the molecular processes underlying this interesting, but poorly understood phenomenon, a comparative analysis of the lipidomes and transcriptomes of the strain over-expressing sco3201 and of the control strain containing the empty plasmid, was carried out. This study revealed that the strain over-expressing sco3201 had a higher triacylglycerol content and a lower phospholipids content than the control strain. This was correlated with up- and down- regulation of some genes involved in fatty acids biosynthesis (fab) and degradation (fad) respectively, indicating a direct or indirect control of the expression of these genes by SCO3201. In some instances, indirect control might involve TetR regulators, whose encoding genes present in close vicinity of genes involved in lipid metabolism, were shown to be differentially expressed in the two strains. Direct interaction of purified His6-SCO3201 with the promoter regions of four of such TetR regulators encoding genes (sco0116, sco0430, sco4167, and sco6792) was demonstrated. Furthermore, fasR (sco2386), encoding the activator of the main fatty acid biosynthetic operon, sco2386-sco2390, has been shown to be an illegitimate positive regulatory target of SCO3201. Altogether our data demonstrated that the sco3201 over-expressing strain accumulates TAG and suggested that degradation of fatty acids was reduced in this strain. This is expected to result into a reduced acetyl-CoA availability that would impair antibiotic biosynthesis either directly or indirectly. |
| first_indexed | 2024-12-10T20:50:08Z |
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| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-12-10T20:50:08Z |
| publishDate | 2020-06-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-4f5cd476515847ba8f91be1dcb0787352022-12-22T01:34:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.01399551002The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the StrainJun Zhang0Qiting Liang1Zhongheng Xu2Miao Cui3Qizhong Zhang4Sonia Abreu5Michelle David6Clara Lejeune7Pierre Chaminade8Marie-Joelle Virolle9Delin Xu10Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaKey Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaKey Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaKey Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaKey Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaUniversité Paris-Saclay, Lipides, Systèmes Analytiques et Biologiques, Châtenay-Malabry, FranceGroup “Energetic Metabolism of Streptomyces”, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, INRA, University Paris-Saclay, Gif-sur-Yvette, FranceGroup “Energetic Metabolism of Streptomyces”, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, INRA, University Paris-Saclay, Gif-sur-Yvette, FranceUniversité Paris-Saclay, Lipides, Systèmes Analytiques et Biologiques, Châtenay-Malabry, FranceGroup “Energetic Metabolism of Streptomyces”, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris-Sud, INRA, University Paris-Saclay, Gif-sur-Yvette, FranceKey Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Department of Ecology, School of Life Sciences and Technology, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Institute of Hydrobiology, Jinan University, Guangzhou, ChinaIn condition of over-expression, SCO3201, a regulator of the TetR family was previously shown to strongly inhibit antibiotic production and morphological differentiation in Streptomyces coelicolor M145. In order to elucidate the molecular processes underlying this interesting, but poorly understood phenomenon, a comparative analysis of the lipidomes and transcriptomes of the strain over-expressing sco3201 and of the control strain containing the empty plasmid, was carried out. This study revealed that the strain over-expressing sco3201 had a higher triacylglycerol content and a lower phospholipids content than the control strain. This was correlated with up- and down- regulation of some genes involved in fatty acids biosynthesis (fab) and degradation (fad) respectively, indicating a direct or indirect control of the expression of these genes by SCO3201. In some instances, indirect control might involve TetR regulators, whose encoding genes present in close vicinity of genes involved in lipid metabolism, were shown to be differentially expressed in the two strains. Direct interaction of purified His6-SCO3201 with the promoter regions of four of such TetR regulators encoding genes (sco0116, sco0430, sco4167, and sco6792) was demonstrated. Furthermore, fasR (sco2386), encoding the activator of the main fatty acid biosynthetic operon, sco2386-sco2390, has been shown to be an illegitimate positive regulatory target of SCO3201. Altogether our data demonstrated that the sco3201 over-expressing strain accumulates TAG and suggested that degradation of fatty acids was reduced in this strain. This is expected to result into a reduced acetyl-CoA availability that would impair antibiotic biosynthesis either directly or indirectly.https://www.frontiersin.org/article/10.3389/fmicb.2020.01399/fullStreptomyces coelicolorantibioticsTetR regulatorfatty acid metabolismRNA-seq |
| spellingShingle | Jun Zhang Qiting Liang Zhongheng Xu Miao Cui Qizhong Zhang Sonia Abreu Michelle David Clara Lejeune Pierre Chaminade Marie-Joelle Virolle Delin Xu The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain Frontiers in Microbiology Streptomyces coelicolor antibiotics TetR regulator fatty acid metabolism RNA-seq |
| title | The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain |
| title_full | The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain |
| title_fullStr | The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain |
| title_full_unstemmed | The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain |
| title_short | The Inhibition of Antibiotic Production in Streptomyces coelicolor Over-Expressing the TetR Regulator SCO3201 IS Correlated With Changes in the Lipidome of the Strain |
| title_sort | inhibition of antibiotic production in streptomyces coelicolor over expressing the tetr regulator sco3201 is correlated with changes in the lipidome of the strain |
| topic | Streptomyces coelicolor antibiotics TetR regulator fatty acid metabolism RNA-seq |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.01399/full |
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