A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture

Streptomyces are mycelial bacteria adapted to grow in soil. They have become important producers of biomolecules with medical applications, but their growth in industrial fermenters is challenged by their peculiar morphology in liquid culture: the hyphae tend to clump and grow as large pellets, whic...

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Main Authors: Erick Eligio Arroyo-Pérez, Gabriela González-Cerón, Gloria Soberón-Chávez, Dimitris Georgellis, Luis Servín-González
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01568/full
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author Erick Eligio Arroyo-Pérez
Gabriela González-Cerón
Gloria Soberón-Chávez
Dimitris Georgellis
Luis Servín-González
author_facet Erick Eligio Arroyo-Pérez
Gabriela González-Cerón
Gloria Soberón-Chávez
Dimitris Georgellis
Luis Servín-González
author_sort Erick Eligio Arroyo-Pérez
collection DOAJ
description Streptomyces are mycelial bacteria adapted to grow in soil. They have become important producers of biomolecules with medical applications, but their growth in industrial fermenters is challenged by their peculiar morphology in liquid culture: the hyphae tend to clump and grow as large pellets, which are oxygen- and nutrient-limited, grow slowly and present diminished protein production. Here, by implementing an experimental evolution strategy, a S. coelicolor strain, 2L12, with dispersed morphology and reduced pellet size in liquid culture and no defects in either differentiation or secondary metabolism was selected. Genome sequencing revealed a single amino acid substitution in a sensor kinase, Sco5282, of unknown function to be responsible for the morphological changes. Moreover, genetic and biochemical scrutiny identified Sco5283 as the cognate response regulator and demonstrated that the acquired mutation activates this two-component system. Finally, transcriptomic analysis of the mutant strain revealed changes in expression of genes involved in central processes such as glycolysis, gluconeogenesis, stress-signaling pathways, proteins secretion and cell envelope metabolism. Thus a novel two-component system is proposed to play a key role in the control of Streptomyces extracellular metabolism.
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spelling doaj.art-5fbc19dae06340cea21217fc1814a82d2022-12-21T23:25:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-07-011010.3389/fmicb.2019.01568472631A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid CultureErick Eligio Arroyo-Pérez0Gabriela González-Cerón1Gloria Soberón-Chávez2Dimitris Georgellis3Luis Servín-González4Instituto de Investigaciones Biomédicas, Departamento de Biología Molecular y Biotecnología, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Investigaciones Biomédicas, Departamento de Biología Molecular y Biotecnología, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Investigaciones Biomédicas, Departamento de Biología Molecular y Biotecnología, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Fisiología Celular, Departamento de Genética Molecular, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Investigaciones Biomédicas, Departamento de Biología Molecular y Biotecnología, Universidad Nacional Autónoma de México, Mexico City, MexicoStreptomyces are mycelial bacteria adapted to grow in soil. They have become important producers of biomolecules with medical applications, but their growth in industrial fermenters is challenged by their peculiar morphology in liquid culture: the hyphae tend to clump and grow as large pellets, which are oxygen- and nutrient-limited, grow slowly and present diminished protein production. Here, by implementing an experimental evolution strategy, a S. coelicolor strain, 2L12, with dispersed morphology and reduced pellet size in liquid culture and no defects in either differentiation or secondary metabolism was selected. Genome sequencing revealed a single amino acid substitution in a sensor kinase, Sco5282, of unknown function to be responsible for the morphological changes. Moreover, genetic and biochemical scrutiny identified Sco5283 as the cognate response regulator and demonstrated that the acquired mutation activates this two-component system. Finally, transcriptomic analysis of the mutant strain revealed changes in expression of genes involved in central processes such as glycolysis, gluconeogenesis, stress-signaling pathways, proteins secretion and cell envelope metabolism. Thus a novel two-component system is proposed to play a key role in the control of Streptomyces extracellular metabolism.https://www.frontiersin.org/article/10.3389/fmicb.2019.01568/fullStreptomycesmorphologytwo-component systemsHAMP domainaggregationbiofilm
spellingShingle Erick Eligio Arroyo-Pérez
Gabriela González-Cerón
Gloria Soberón-Chávez
Dimitris Georgellis
Luis Servín-González
A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
Frontiers in Microbiology
Streptomyces
morphology
two-component systems
HAMP domain
aggregation
biofilm
title A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
title_full A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
title_fullStr A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
title_full_unstemmed A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
title_short A Novel Two-Component System, Encoded by the sco5282/sco5283 Genes, Affects Streptomyces coelicolor Morphology in Liquid Culture
title_sort novel two component system encoded by the sco5282 sco5283 genes affects streptomyces coelicolor morphology in liquid culture
topic Streptomyces
morphology
two-component systems
HAMP domain
aggregation
biofilm
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01568/full
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