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The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis

BACKGROUND: Cyclodipeptides and their derivatives constitute a large class of peptide natural products with noteworthy biological activities. In some yeasts and bacterial species, pulcherriminic acid derived from cyclo-L-leucyl-L-leucyl is excreted and chelates free ferric ions to form the pulcherri...

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Autores principales: Randazzo, Paola, Aubert-Frambourg, Anne, Guillot, Alain, Auger, Sandrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992311/
https://www.ncbi.nlm.nih.gov/pubmed/27542896
http://dx.doi.org/10.1186/s12866-016-0807-3
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author Randazzo, Paola
Aubert-Frambourg, Anne
Guillot, Alain
Auger, Sandrine
author_facet Randazzo, Paola
Aubert-Frambourg, Anne
Guillot, Alain
Auger, Sandrine
author_sort Randazzo, Paola
collection PubMed
description BACKGROUND: Cyclodipeptides and their derivatives constitute a large class of peptide natural products with noteworthy biological activities. In some yeasts and bacterial species, pulcherriminic acid derived from cyclo-L-leucyl-L-leucyl is excreted and chelates free ferric ions to form the pulcherrimin. In Bacillus subtilis, the enzymes YvmC and CypX are known to be involved in pulcherriminic acid biosynthesis. However, the mechanisms controlling the transcription of the yvmC-cypX operon are still unknown. RESULTS: In this work, we demonstrated that the B. subtilis YvmB MarR-like regulator is the major transcription factor controlling yvmC-cypX expression. A comprehensive quantitative proteomic analysis revealed a wide and prominent effect of yvmB deletion on proteins involved in cellular processes depending on iron availability. In addition, expression of yvmB depends on iron availability. Further analysis with real-time in vivo transcriptional profiling allowed us to define the YvmB regulon. We identified yvmBA, yvmC-cypX and yvnB for negative regulation and yisI for positive regulation. In combination with genetic approaches, gel mobility shift assays indicated that a 14-bp palindromic motif constitutes the YvmB binding site. It was unexpected that YvmB controls expression of yisI, whose encoding protein plays a negative role in the regulation of the sporulation initiation pathway. YvmB appears as an additional regulatory element into the cell’s decision to grow or sporulate. CONCLUSION: Our findings reveal a possible role of the B. subtilis YvmB regulator in the regulatory networks connected to iron metabolism and to the control of proper timing of sporulation. YvmB was renamed as PchR controlling the pulcherriminic acid biosynthetic pathway of B. subtilis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0807-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-49923112016-08-21 The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis Randazzo, Paola Aubert-Frambourg, Anne Guillot, Alain Auger, Sandrine BMC Microbiol Research Article BACKGROUND: Cyclodipeptides and their derivatives constitute a large class of peptide natural products with noteworthy biological activities. In some yeasts and bacterial species, pulcherriminic acid derived from cyclo-L-leucyl-L-leucyl is excreted and chelates free ferric ions to form the pulcherrimin. In Bacillus subtilis, the enzymes YvmC and CypX are known to be involved in pulcherriminic acid biosynthesis. However, the mechanisms controlling the transcription of the yvmC-cypX operon are still unknown. RESULTS: In this work, we demonstrated that the B. subtilis YvmB MarR-like regulator is the major transcription factor controlling yvmC-cypX expression. A comprehensive quantitative proteomic analysis revealed a wide and prominent effect of yvmB deletion on proteins involved in cellular processes depending on iron availability. In addition, expression of yvmB depends on iron availability. Further analysis with real-time in vivo transcriptional profiling allowed us to define the YvmB regulon. We identified yvmBA, yvmC-cypX and yvnB for negative regulation and yisI for positive regulation. In combination with genetic approaches, gel mobility shift assays indicated that a 14-bp palindromic motif constitutes the YvmB binding site. It was unexpected that YvmB controls expression of yisI, whose encoding protein plays a negative role in the regulation of the sporulation initiation pathway. YvmB appears as an additional regulatory element into the cell’s decision to grow or sporulate. CONCLUSION: Our findings reveal a possible role of the B. subtilis YvmB regulator in the regulatory networks connected to iron metabolism and to the control of proper timing of sporulation. YvmB was renamed as PchR controlling the pulcherriminic acid biosynthetic pathway of B. subtilis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0807-3) contains supplementary material, which is available to authorized users. BioMed Central 2016-08-20 /pmc/articles/PMC4992311/ /pubmed/27542896 http://dx.doi.org/10.1186/s12866-016-0807-3 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Randazzo, Paola
Aubert-Frambourg, Anne
Guillot, Alain
Auger, Sandrine
The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title_full The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title_fullStr The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title_full_unstemmed The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title_short The MarR-like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis
title_sort marr-like protein pchr (yvmb) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in bacillus subtilis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992311/
https://www.ncbi.nlm.nih.gov/pubmed/27542896
http://dx.doi.org/10.1186/s12866-016-0807-3
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