Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple
Tyrian purple, mainly composed of 6, 6′-dibromoindigo, is a precious dye extracted from sea snails. In this study, we found Tyrian purple can be selectively produced by a bacterial strain GS-2 when fed with 6-bromotryptophan in the presence of tryptophan. This GS-2 strain was then identified as Prov...
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| Format: | Article |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Bioengineering and Biotechnology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fbioe.2022.1109929/full |
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| author | Feifei Li Feifei Li Feifei Li Feifei Li Huaxiang Deng Huaxiang Deng Huaxiang Deng Biming Zhong Biming Zhong Biming Zhong Banlai Ruan Banlai Ruan Banlai Ruan Xixi Zhao Xixi Zhao Xixi Zhao Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo |
| author_facet | Feifei Li Feifei Li Feifei Li Feifei Li Huaxiang Deng Huaxiang Deng Huaxiang Deng Biming Zhong Biming Zhong Biming Zhong Banlai Ruan Banlai Ruan Banlai Ruan Xixi Zhao Xixi Zhao Xixi Zhao Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo |
| author_sort | Feifei Li |
| collection | DOAJ |
| description | Tyrian purple, mainly composed of 6, 6′-dibromoindigo, is a precious dye extracted from sea snails. In this study, we found Tyrian purple can be selectively produced by a bacterial strain GS-2 when fed with 6-bromotryptophan in the presence of tryptophan. This GS-2 strain was then identified as Providencia rettgeri based on bacterial genome sequencing analysis. An indole degradation gene cluster for indole metabolism was identified from this GS-2 strain. The heterologous expression of the indole degradation gene cluster in Escherichia coli BL21 (DE3) and in vitro enzymatic reaction demonstrated that the indole biodegradation gene cluster may contribute to selectively biosynthesizing Tyrian purple. To further explore the underlying mechanism of the selectivity, we explored the intermediates in this indole biodegradation pathway using liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (LC-ESI-QTOF-MS/MS), which indicated that the indole biodegradation pathway in Providencia rettgeri is the catechol pathway. Interestingly, the monooxygenase GS-C co-expressed with its corresponding reductase GS-D in the cluster has better activity for the biosynthesis of Tyrian purple compared with the previously reported monooxygenase from Methylophaga aminisulfidivorans (MaFMO) or Streptomyces cattleya cytochrome P450 enzyme (CYP102G4). This is the first study to show the existence of an indole biodegradation pathway in Providencia rettgeri, and the indole biodegradation gene cluster can contribute to the selective production of Tyrian purple. |
| first_indexed | 2024-04-10T23:51:08Z |
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| id | doaj.art-40193e7f47c54713a5dc6461b4030035 |
| institution | Directory Open Access Journal |
| issn | 2296-4185 |
| language | English |
| last_indexed | 2024-04-10T23:51:08Z |
| publishDate | 2023-01-01 |
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| series | Frontiers in Bioengineering and Biotechnology |
| spelling | doaj.art-40193e7f47c54713a5dc6461b40300352023-01-10T18:14:25ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852023-01-011010.3389/fbioe.2022.11099291109929Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purpleFeifei Li0Feifei Li1Feifei Li2Feifei Li3Huaxiang Deng4Huaxiang Deng5Huaxiang Deng6Biming Zhong7Biming Zhong8Biming Zhong9Banlai Ruan10Banlai Ruan11Banlai Ruan12Xixi Zhao13Xixi Zhao14Xixi Zhao15Xiaozhou Luo16Xiaozhou Luo17Xiaozhou Luo18Xiaozhou Luo19School of Life Sciences, Inner Mongolia University, Hohhot, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaSchool of Life Sciences, Inner Mongolia University, Hohhot, ChinaShenzhen Key Laboratory for the Intelligent Microbial Manufacturing of Medicines, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaCenter for Synthetic Biochemistry, Shenzhen Institute of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaTyrian purple, mainly composed of 6, 6′-dibromoindigo, is a precious dye extracted from sea snails. In this study, we found Tyrian purple can be selectively produced by a bacterial strain GS-2 when fed with 6-bromotryptophan in the presence of tryptophan. This GS-2 strain was then identified as Providencia rettgeri based on bacterial genome sequencing analysis. An indole degradation gene cluster for indole metabolism was identified from this GS-2 strain. The heterologous expression of the indole degradation gene cluster in Escherichia coli BL21 (DE3) and in vitro enzymatic reaction demonstrated that the indole biodegradation gene cluster may contribute to selectively biosynthesizing Tyrian purple. To further explore the underlying mechanism of the selectivity, we explored the intermediates in this indole biodegradation pathway using liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (LC-ESI-QTOF-MS/MS), which indicated that the indole biodegradation pathway in Providencia rettgeri is the catechol pathway. Interestingly, the monooxygenase GS-C co-expressed with its corresponding reductase GS-D in the cluster has better activity for the biosynthesis of Tyrian purple compared with the previously reported monooxygenase from Methylophaga aminisulfidivorans (MaFMO) or Streptomyces cattleya cytochrome P450 enzyme (CYP102G4). This is the first study to show the existence of an indole biodegradation pathway in Providencia rettgeri, and the indole biodegradation gene cluster can contribute to the selective production of Tyrian purple.https://www.frontiersin.org/articles/10.3389/fbioe.2022.1109929/fullTyrian purpleProvidencia rettgeriindole biodegradation gene clusterselective Tyrian purple producingmonooxygenase |
| spellingShingle | Feifei Li Feifei Li Feifei Li Feifei Li Huaxiang Deng Huaxiang Deng Huaxiang Deng Biming Zhong Biming Zhong Biming Zhong Banlai Ruan Banlai Ruan Banlai Ruan Xixi Zhao Xixi Zhao Xixi Zhao Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo Xiaozhou Luo Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple Frontiers in Bioengineering and Biotechnology Tyrian purple Providencia rettgeri indole biodegradation gene cluster selective Tyrian purple producing monooxygenase |
| title | Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple |
| title_full | Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple |
| title_fullStr | Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple |
| title_full_unstemmed | Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple |
| title_short | Identification of an indole biodegradation gene cluster from Providencia rettgeri and its contribution in selectively biosynthesizing Tyrian purple |
| title_sort | identification of an indole biodegradation gene cluster from providencia rettgeri and its contribution in selectively biosynthesizing tyrian purple |
| topic | Tyrian purple Providencia rettgeri indole biodegradation gene cluster selective Tyrian purple producing monooxygenase |
| url | https://www.frontiersin.org/articles/10.3389/fbioe.2022.1109929/full |
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