Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics

<i>Streptomyces coelicolor</i> M145 is a model strain extensively studied to elucidate the regulation of antibiotic biosynthesis in <i>Streptomyces</i> species. This strain abundantly produces the blue polyketide antibiotic, actinorhodin (ACT), and has a low lipid content. In...

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Main Authors: Thierry Dulermo, Clara Lejeune, Ece Aybeke, Sonia Abreu, Jean Bleton, Michelle David, Ariane Deniset-Besseau, Pierre Chaminade, Annabelle Thibessard, Pierre Leblond, Marie-Joelle Virolle
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Language:English
Published: MDPI AG 2023-05-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/6/1470
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author Thierry Dulermo
Clara Lejeune
Ece Aybeke
Sonia Abreu
Jean Bleton
Michelle David
Ariane Deniset-Besseau
Pierre Chaminade
Annabelle Thibessard
Pierre Leblond
Marie-Joelle Virolle
author_facet Thierry Dulermo
Clara Lejeune
Ece Aybeke
Sonia Abreu
Jean Bleton
Michelle David
Ariane Deniset-Besseau
Pierre Chaminade
Annabelle Thibessard
Pierre Leblond
Marie-Joelle Virolle
author_sort Thierry Dulermo
collection DOAJ
description <i>Streptomyces coelicolor</i> M145 is a model strain extensively studied to elucidate the regulation of antibiotic biosynthesis in <i>Streptomyces</i> species. This strain abundantly produces the blue polyketide antibiotic, actinorhodin (ACT), and has a low lipid content. In a process designed to delete the gene encoding the isocitrate lyase (<i>sco0982</i>) of the glyoxylate cycle, an unexpected variant of <i>S. coelicolor</i> was obtained besides <i>bona fide sco0982</i> deletion mutants. This variant produces 7- to 15-fold less ACT and has a 3-fold higher triacylglycerol and phosphatidylethanolamine content than the original strain. The genome of this variant was sequenced and revealed that 704 genes were deleted (9% of total number of genes) through deletions of various sizes accompanied by the massive loss of mobile genetic elements. Some deletions include genes whose absence could be related to the high total lipid content of this variant such as those encoding enzymes of the TCA and glyoxylate cycles, enzymes involved in nitrogen assimilation as well as enzymes belonging to some polyketide and possibly trehalose biosynthetic pathways. The characteristics of this deleted variant of <i>S. coelicolor</i> are consistent with the existence of the previously reported negative correlation existing between lipid content and antibiotic production in <i>Streptomyces</i> species.
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spelling doaj.art-bbe276df92374be089ca44dbaebd48792023-11-18T11:42:20ZengMDPI AGMicroorganisms2076-26072023-05-01116147010.3390/microorganisms11061470Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize AntibioticsThierry Dulermo0Clara Lejeune1Ece Aybeke2Sonia Abreu3Jean Bleton4Michelle David5Ariane Deniset-Besseau6Pierre Chaminade7Annabelle Thibessard8Pierre Leblond9Marie-Joelle Virolle10Université Paris-Saclay, CNRS, CEA, Institute for Integrative Biology of the Cell (I2BC), Department of Microbiology, Group “Energetic Metabolism of <i>Streptomyces</i>”, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, FranceUniversité Paris-Saclay, CNRS, CEA, Institute for Integrative Biology of the Cell (I2BC), Department of Microbiology, Group “Energetic Metabolism of <i>Streptomyces</i>”, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, FranceUniversité Paris-Saclay, CNRS, CEA, Institut de Chimie Physique, UMR 8000, 91405 Orsay, FranceUniversité Paris-Saclay, CNRS, CEA, Lip(Sys)2 (Lipides Systèmes Analytiques et Biologiques), UFR Pharmacie—Bâtiment Henri Moissan, 17 Avenue des Sciences, 91400 Orsay, FranceUniversité Paris-Saclay, CNRS, CEA, Lip(Sys)2 (Lipides Systèmes Analytiques et Biologiques), UFR Pharmacie—Bâtiment Henri Moissan, 17 Avenue des Sciences, 91400 Orsay, FranceUniversité Paris-Saclay, CNRS, CEA, Institute for Integrative Biology of the Cell (I2BC), Department of Microbiology, Group “Energetic Metabolism of <i>Streptomyces</i>”, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, FranceUniversité Paris-Saclay, CNRS, CEA, Institut de Chimie Physique, UMR 8000, 91405 Orsay, FranceUniversité Paris-Saclay, CNRS, CEA, Lip(Sys)2 (Lipides Systèmes Analytiques et Biologiques), UFR Pharmacie—Bâtiment Henri Moissan, 17 Avenue des Sciences, 91400 Orsay, FranceUniversité de Lorraine, INRAE, DynAMic, F-54000 Nancy, FranceUniversité de Lorraine, INRAE, DynAMic, F-54000 Nancy, FranceUniversité Paris-Saclay, CNRS, CEA, Institute for Integrative Biology of the Cell (I2BC), Department of Microbiology, Group “Energetic Metabolism of <i>Streptomyces</i>”, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, France<i>Streptomyces coelicolor</i> M145 is a model strain extensively studied to elucidate the regulation of antibiotic biosynthesis in <i>Streptomyces</i> species. This strain abundantly produces the blue polyketide antibiotic, actinorhodin (ACT), and has a low lipid content. In a process designed to delete the gene encoding the isocitrate lyase (<i>sco0982</i>) of the glyoxylate cycle, an unexpected variant of <i>S. coelicolor</i> was obtained besides <i>bona fide sco0982</i> deletion mutants. This variant produces 7- to 15-fold less ACT and has a 3-fold higher triacylglycerol and phosphatidylethanolamine content than the original strain. The genome of this variant was sequenced and revealed that 704 genes were deleted (9% of total number of genes) through deletions of various sizes accompanied by the massive loss of mobile genetic elements. Some deletions include genes whose absence could be related to the high total lipid content of this variant such as those encoding enzymes of the TCA and glyoxylate cycles, enzymes involved in nitrogen assimilation as well as enzymes belonging to some polyketide and possibly trehalose biosynthetic pathways. The characteristics of this deleted variant of <i>S. coelicolor</i> are consistent with the existence of the previously reported negative correlation existing between lipid content and antibiotic production in <i>Streptomyces</i> species.https://www.mdpi.com/2076-2607/11/6/1470fatty acids/lipid biosynthesis/degradationtriacylglycerolphosphatidylethanolamineantibioticsgenome comparative analysisgenomic deletion
spellingShingle Thierry Dulermo
Clara Lejeune
Ece Aybeke
Sonia Abreu
Jean Bleton
Michelle David
Ariane Deniset-Besseau
Pierre Chaminade
Annabelle Thibessard
Pierre Leblond
Marie-Joelle Virolle
Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
Microorganisms
fatty acids/lipid biosynthesis/degradation
triacylglycerol
phosphatidylethanolamine
antibiotics
genome comparative analysis
genomic deletion
title Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
title_full Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
title_fullStr Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
title_full_unstemmed Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
title_short Genome Analysis of a Variant of <i>Streptomyces coelicolor</i> M145 with High Lipid Content and Poor Ability to Synthetize Antibiotics
title_sort genome analysis of a variant of i streptomyces coelicolor i m145 with high lipid content and poor ability to synthetize antibiotics
topic fatty acids/lipid biosynthesis/degradation
triacylglycerol
phosphatidylethanolamine
antibiotics
genome comparative analysis
genomic deletion
url https://www.mdpi.com/2076-2607/11/6/1470
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