Cargando…

Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145

The Streptomyces genus is well known for its ability to produce bio-active secondary metabolites of great medical interest. However, the metabolic features accompanying these bio-productions remain to be defined. In this study, the comparison of related model strains producing differing levels of ac...

Descripción completa

Detalles Bibliográficos
Autores principales: Esnault, Catherine, Dulermo, Thierry, Smirnov, Aleksey, Askora, Ahmed, David, Michelle, Deniset-Besseau, Ariane, Holland, Ian-Barry, Virolle, Marie-Joelle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5427975/
https://www.ncbi.nlm.nih.gov/pubmed/28298624
http://dx.doi.org/10.1038/s41598-017-00259-9
_version_ 1783235732957036544
author Esnault, Catherine
Dulermo, Thierry
Smirnov, Aleksey
Askora, Ahmed
David, Michelle
Deniset-Besseau, Ariane
Holland, Ian-Barry
Virolle, Marie-Joelle
author_facet Esnault, Catherine
Dulermo, Thierry
Smirnov, Aleksey
Askora, Ahmed
David, Michelle
Deniset-Besseau, Ariane
Holland, Ian-Barry
Virolle, Marie-Joelle
author_sort Esnault, Catherine
collection PubMed
description The Streptomyces genus is well known for its ability to produce bio-active secondary metabolites of great medical interest. However, the metabolic features accompanying these bio-productions remain to be defined. In this study, the comparison of related model strains producing differing levels of actinorhoddin (ACT), showed that S. lividans, a weak producer, had high TriAcylGlycerol (TAG) content indicative of a glycolytic metabolism. In contrast, the strong producer, S. coelicolor, was characterized by low TAG content, active consumption of its polyphosphate (PolyP) stores and extremely high ATP/ADP ratios. This indicated highly active oxidative metabolism that was correlated with induction of ACT biosynthesis. Interestingly, in conditions of phosphate limitation, the ppk mutant had TAG content and ACT production levels intermediary between those of S. lividans and S. coelicolor. This strain was characterized by high ADP levels indicating that Ppk was acting as an Adenosine Di Phosphate Kinase. Its absence resulted in energetic stress that is proposed to trigger an activation of oxidative metabolism to restore its energetic balance. This process, which is correlated with ACT biosynthesis, requires acetylCoA to fuel the Krebs cycle and phosphate for ATP generation by the ATP synthase coupled to the respiratory chain, resulting in low TAG and polyP content of the ACT producing strains.
format Online
Article
Text
id pubmed-5427975
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-54279752017-05-15 Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145 Esnault, Catherine Dulermo, Thierry Smirnov, Aleksey Askora, Ahmed David, Michelle Deniset-Besseau, Ariane Holland, Ian-Barry Virolle, Marie-Joelle Sci Rep Article The Streptomyces genus is well known for its ability to produce bio-active secondary metabolites of great medical interest. However, the metabolic features accompanying these bio-productions remain to be defined. In this study, the comparison of related model strains producing differing levels of actinorhoddin (ACT), showed that S. lividans, a weak producer, had high TriAcylGlycerol (TAG) content indicative of a glycolytic metabolism. In contrast, the strong producer, S. coelicolor, was characterized by low TAG content, active consumption of its polyphosphate (PolyP) stores and extremely high ATP/ADP ratios. This indicated highly active oxidative metabolism that was correlated with induction of ACT biosynthesis. Interestingly, in conditions of phosphate limitation, the ppk mutant had TAG content and ACT production levels intermediary between those of S. lividans and S. coelicolor. This strain was characterized by high ADP levels indicating that Ppk was acting as an Adenosine Di Phosphate Kinase. Its absence resulted in energetic stress that is proposed to trigger an activation of oxidative metabolism to restore its energetic balance. This process, which is correlated with ACT biosynthesis, requires acetylCoA to fuel the Krebs cycle and phosphate for ATP generation by the ATP synthase coupled to the respiratory chain, resulting in low TAG and polyP content of the ACT producing strains. Nature Publishing Group UK 2017-03-15 /pmc/articles/PMC5427975/ /pubmed/28298624 http://dx.doi.org/10.1038/s41598-017-00259-9 Text en © The Author(s) 2017 This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Esnault, Catherine
Dulermo, Thierry
Smirnov, Aleksey
Askora, Ahmed
David, Michelle
Deniset-Besseau, Ariane
Holland, Ian-Barry
Virolle, Marie-Joelle
Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title_full Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title_fullStr Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title_full_unstemmed Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title_short Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145
title_sort strong antibiotic production is correlated with highly active oxidative metabolism in streptomyces coelicolor m145
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5427975/
https://www.ncbi.nlm.nih.gov/pubmed/28298624
http://dx.doi.org/10.1038/s41598-017-00259-9
work_keys_str_mv AT esnaultcatherine strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT dulermothierry strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT smirnovaleksey strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT askoraahmed strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT davidmichelle strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT denisetbesseauariane strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT hollandianbarry strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145
AT virollemariejoelle strongantibioticproductioniscorrelatedwithhighlyactiveoxidativemetabolisminstreptomycescoelicolorm145