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Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona

BACKGROUND: Butenyl-spinosyn, produced by Saccharopolyspora pogona, is a promising biopesticide due to excellent insecticidal activity and broad pesticidal spectrum. Bacterioferritin (Bfr, encoded by bfr) regulates the storage and utilization of iron, which is essential for the growth and metabolism...

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Autores principales: Tang, Jianli, Zhu, Zirong, He, Haocheng, Liu, Zhudong, Xia, Ziyuan, Chen, Jianming, Hu, Jinjuan, Cao, Li, Rang, Jie, Shuai, Ling, Liu, Yang, Sun, Yunjun, Ding, Xuezhi, Hu, Shengbiao, Xia, Liqiu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8364703/
https://www.ncbi.nlm.nih.gov/pubmed/34391414
http://dx.doi.org/10.1186/s12934-021-01651-x
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author Tang, Jianli
Zhu, Zirong
He, Haocheng
Liu, Zhudong
Xia, Ziyuan
Chen, Jianming
Hu, Jinjuan
Cao, Li
Rang, Jie
Shuai, Ling
Liu, Yang
Sun, Yunjun
Ding, Xuezhi
Hu, Shengbiao
Xia, Liqiu
author_facet Tang, Jianli
Zhu, Zirong
He, Haocheng
Liu, Zhudong
Xia, Ziyuan
Chen, Jianming
Hu, Jinjuan
Cao, Li
Rang, Jie
Shuai, Ling
Liu, Yang
Sun, Yunjun
Ding, Xuezhi
Hu, Shengbiao
Xia, Liqiu
author_sort Tang, Jianli
collection PubMed
description BACKGROUND: Butenyl-spinosyn, produced by Saccharopolyspora pogona, is a promising biopesticide due to excellent insecticidal activity and broad pesticidal spectrum. Bacterioferritin (Bfr, encoded by bfr) regulates the storage and utilization of iron, which is essential for the growth and metabolism of microorganisms. However, the effect of Bfr on the growth and butenyl-spinosyn biosynthesis in S. pogona has not been explored. RESULTS: Here, we found that the storage of intracellular iron influenced butenyl-spinosyn biosynthesis and the stress resistance of S. pogona, which was regulated by Bfr. The overexpression of bfr increased the production of butenyl-spinosyn by 3.14-fold and enhanced the tolerance of S. pogona to iron toxicity and oxidative damage, while the knockout of bfr had the opposite effects. Based on the quantitative proteomics analysis and experimental verification, the inner mechanism of these phenomena was explored. Overexpression of bfr enhanced the iron storage capacity of the strain, which activated polyketide synthase genes and enhanced the supply of acyl-CoA precursors to improve butenyl-spinosyn biosynthesis. In addition, it induced the oxidative stress response to improve the stress resistance of S. pogona. CONCLUSION: Our work reveals the role of Bfr in increasing the yield of butenyl-spinosyn and enhancing the stress resistance of S. pogona, and provides insights into its enhancement on secondary metabolism, which provides a reference for optimizing the production of secondary metabolites in actinomycetes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12934-021-01651-x.
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spelling pubmed-83647032021-08-17 Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona Tang, Jianli Zhu, Zirong He, Haocheng Liu, Zhudong Xia, Ziyuan Chen, Jianming Hu, Jinjuan Cao, Li Rang, Jie Shuai, Ling Liu, Yang Sun, Yunjun Ding, Xuezhi Hu, Shengbiao Xia, Liqiu Microb Cell Fact Research BACKGROUND: Butenyl-spinosyn, produced by Saccharopolyspora pogona, is a promising biopesticide due to excellent insecticidal activity and broad pesticidal spectrum. Bacterioferritin (Bfr, encoded by bfr) regulates the storage and utilization of iron, which is essential for the growth and metabolism of microorganisms. However, the effect of Bfr on the growth and butenyl-spinosyn biosynthesis in S. pogona has not been explored. RESULTS: Here, we found that the storage of intracellular iron influenced butenyl-spinosyn biosynthesis and the stress resistance of S. pogona, which was regulated by Bfr. The overexpression of bfr increased the production of butenyl-spinosyn by 3.14-fold and enhanced the tolerance of S. pogona to iron toxicity and oxidative damage, while the knockout of bfr had the opposite effects. Based on the quantitative proteomics analysis and experimental verification, the inner mechanism of these phenomena was explored. Overexpression of bfr enhanced the iron storage capacity of the strain, which activated polyketide synthase genes and enhanced the supply of acyl-CoA precursors to improve butenyl-spinosyn biosynthesis. In addition, it induced the oxidative stress response to improve the stress resistance of S. pogona. CONCLUSION: Our work reveals the role of Bfr in increasing the yield of butenyl-spinosyn and enhancing the stress resistance of S. pogona, and provides insights into its enhancement on secondary metabolism, which provides a reference for optimizing the production of secondary metabolites in actinomycetes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12934-021-01651-x. BioMed Central 2021-08-14 /pmc/articles/PMC8364703/ /pubmed/34391414 http://dx.doi.org/10.1186/s12934-021-01651-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Tang, Jianli
Zhu, Zirong
He, Haocheng
Liu, Zhudong
Xia, Ziyuan
Chen, Jianming
Hu, Jinjuan
Cao, Li
Rang, Jie
Shuai, Ling
Liu, Yang
Sun, Yunjun
Ding, Xuezhi
Hu, Shengbiao
Xia, Liqiu
Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title_full Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title_fullStr Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title_full_unstemmed Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title_short Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona
title_sort bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in saccharopolyspora pogona
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8364703/
https://www.ncbi.nlm.nih.gov/pubmed/34391414
http://dx.doi.org/10.1186/s12934-021-01651-x
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