Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum
Busche T, Silar R, Picmanova M, Patek M, Kalinowski J (2012)
BMC Genomics 13(1): 445.
Zeitschriftenaufsatz
| Veröffentlicht | Englisch
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Autor*in
Busche, TobiasUniBi;
Silar, Radoslav;
Picmanova, Martina;
Patek, Miroslav;
Kalinowski, JörnUniBi
Abstract / Bemerkung
Background
The expression of genes in Corynebacterium glutamicum, a Gram-positive non-pathogenic bacterium used mainly for the industrial production of amino acids, is regulated by seven different sigma factors of RNA polymerase, including the stress-responsive ECF-sigma factor SigH. The sigH gene is located in a gene cluster together with the rshA gene, putatively encoding an anti-sigma factor. The aim of this study was to analyze the transcriptional regulation of the sigH and rshA gene cluster and the effects of RshA on the SigH regulon, in order to refine the model describing the role of SigH and RshA during stress response.
Results
Transcription analyses revealed that the sigH gene and rshA gene are cotranscribed from four sigH housekeeping promoters in C. glutamicum. In addition, a SigH-controlled rshA promoter was found to only drive the transcription of the rshA gene. To test the role of the putative anti-sigma factor gene rshA under normal growth conditions, a C. glutamicum rshA deletion strain was constructed and used for genome-wide transcription profiling with DNA microarrays. In total, 83 genes organized in 61 putative transcriptional units, including those previously detected using sigH mutant strains, exhibited increased transcript levels in the rshA deletion mutant compared to its parental strain. The genes encoding proteins related to disulphide stress response, heat stress proteins, components of the SOS-response to DNA damage and proteasome components were the most markedly upregulated gene groups. Altogether six SigH-dependent promoters upstream of the identified genes were determined by primer extension and a refined consensus promoter consisting of 45 original promoter sequences was constructed.
Conclusions
The rshA gene codes for an anti-sigma factor controlling the function of the stress-responsive sigma factor SigH in C. glutamicum. Transcription of rshA from a SigH-dependent promoter may serve to quickly shutdown the SigH-dependent stress response after the cells have overcome the stress condition. Here we propose a model of the regulation of oxidative and heat stress response including redox homeostasis by SigH, RshA and the thioredoxin system.
Stichworte
Anti-sigma factor;
Corynebacterium glutamicum;
ECF sigma factor;
Promoter;
Microarray analysis
Erscheinungsjahr
2012
Zeitschriftentitel
BMC Genomics
Band
13
Ausgabe
1
Art.-Nr.
445
ISSN
1471-2164
Finanzierungs-Informationen
Open-Access-Publikationskosten wurden durch die Deutsche Forschungsgemeinschaft und die Universität Bielefeld gefördert.
Page URI
https://pub.uni-bielefeld.de/record/2528277
Zitieren
Busche T, Silar R, Picmanova M, Patek M, Kalinowski J. Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics. 2012;13(1): 445.
Busche, T., Silar, R., Picmanova, M., Patek, M., & Kalinowski, J. (2012). Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics, 13(1), 445. doi:10.1186/1471-2164-13-445
Busche, Tobias, Silar, Radoslav, Picmanova, Martina, Patek, Miroslav, and Kalinowski, Jörn. 2012. “Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum”. BMC Genomics 13 (1): 445.
Busche, T., Silar, R., Picmanova, M., Patek, M., and Kalinowski, J. (2012). Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics 13:445.
Busche, T., et al., 2012. Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics, 13(1): 445.
T. Busche, et al., “Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum”, BMC Genomics, vol. 13, 2012, : 445.
Busche, T., Silar, R., Picmanova, M., Patek, M., Kalinowski, J.: Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum. BMC Genomics. 13, : 445 (2012).
Busche, Tobias, Silar, Radoslav, Picmanova, Martina, Patek, Miroslav, and Kalinowski, Jörn. “Transcriptional regulation of the operon encoding stress-responsive ECF sigma factor SigH and its anti-sigma factor RshA, and control of its regulatory network in Corynebacterium glutamicum”. BMC Genomics 13.1 (2012): 445.
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2019-09-06T09:18:06Z
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Daten bereitgestellt von European Bioinformatics Institute (EBI)
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The whcE gene of Corynebacterium glutamicum is important for survival following heat and oxidative stress.
Kim TH, Park JS, Kim HJ, Kim Y, Kim P, Lee HS., Biochem. Biophys. Res. Commun. 337(3), 2005
PMID: 16212936
Kim TH, Park JS, Kim HJ, Kim Y, Kim P, Lee HS., Biochem. Biophys. Res. Commun. 337(3), 2005
PMID: 16212936
Cloning and transcriptional characterization of two sigma factor genes, sigA and sigB, from Brevibacterium flavum.
Halgasova N, Bukovska G, Timko J, Kormanec J., Curr. Microbiol. 43(4), 2001
PMID: 11683358
Halgasova N, Bukovska G, Timko J, Kormanec J., Curr. Microbiol. 43(4), 2001
PMID: 11683358
Group 2 sigma factor SigB of Corynebacterium glutamicum positively regulates glucose metabolism under conditions of oxygen deprivation.
Ehira S, Shirai T, Teramoto H, Inui M, Yukawa H., Appl. Environ. Microbiol. 74(16), 2008
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Ehira S, Shirai T, Teramoto H, Inui M, Yukawa H., Appl. Environ. Microbiol. 74(16), 2008
PMID: 18567683
The extracytoplasmic function-type sigma factor SigM of Corynebacterium glutamicum ATCC 13032 is involved in transcription of disulfide stress-related genes.
Nakunst D, Larisch C, Huser AT, Tauch A, Puhler A, Kalinowski J., J. Bacteriol. 189(13), 2007
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Positive and negative feedback regulatory loops of thiol-oxidative stress response mediated by an unstable isoform of sigmaR in actinomycetes.
Kim MS, Hahn MY, Cho Y, Cho SN, Roe JH., Mol. Microbiol. 73(5), 2009
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Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora.
Tauch A, Kaiser O, Hain T, Goesmann A, Weisshaar B, Albersmeier A, Bekel T, Bischoff N, Brune I, Chakraborty T, Kalinowski J, Meyer F, Rupp O, Schneiker S, Viehoever P, Puhler A., J. Bacteriol. 187(13), 2005
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Tauch A, Kaiser O, Hain T, Goesmann A, Weisshaar B, Albersmeier A, Bekel T, Bischoff N, Brune I, Chakraborty T, Kalinowski J, Meyer F, Rupp O, Schneiker S, Viehoever P, Puhler A., J. Bacteriol. 187(13), 2005
PMID: 15968079
Genetic makeup of the Corynebacterium glutamicum LexA regulon deduced from comparative transcriptomics and in vitro DNA band shift assays.
Jochmann N, Kurze AK, Czaja LF, Brinkrolf K, Brune I, Huser AT, Hansmeier N, Puhler A, Borovok I, Tauch A., Microbiology (Reading, Engl.) 155(Pt 5), 2009
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Jochmann N, Kurze AK, Czaja LF, Brinkrolf K, Brune I, Huser AT, Hansmeier N, Puhler A, Borovok I, Tauch A., Microbiology (Reading, Engl.) 155(Pt 5), 2009
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The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis.
Raman S, Song T, Puyang X, Bardarov S, Jacobs WR Jr, Husson RN., J. Bacteriol. 183(20), 2001
PMID: 11567012
Raman S, Song T, Puyang X, Bardarov S, Jacobs WR Jr, Husson RN., J. Bacteriol. 183(20), 2001
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Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon.
Paget MS, Molle V, Cohen G, Aharonowitz Y, Buttner MJ., Mol. Microbiol. 42(4), 2001
PMID: 11737643
Paget MS, Molle V, Cohen G, Aharonowitz Y, Buttner MJ., Mol. Microbiol. 42(4), 2001
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Regulation of mycothiol metabolism by sigma(R) and the thiol redox sensor anti-sigma factor RsrA.
Newton GL, Fahey RC., Mol. Microbiol. 68(4), 2008
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Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria.
Newton GL, Buchmeier N, Fahey RC., Microbiol. Mol. Biol. Rev. 72(3), 2008
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Newton GL, Buchmeier N, Fahey RC., Microbiol. Mol. Biol. Rev. 72(3), 2008
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Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein.
Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry CE 3rd., J. Biol. Chem. 284(5), 2008
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Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry CE 3rd., J. Biol. Chem. 284(5), 2008
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Chromosomally encoded small antisense RNA in Corynebacterium glutamicum.
Zemanova M, Kaderabkova P, Patek M, Knoppova M, Silar R, Nesvera J., FEMS Microbiol. Lett. 279(2), 2007
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Development of a Corynebacterium glutamicum DNA microarray and validation by genome-wide expression profiling during growth with propionate as carbon source.
Huser AT, Becker A, Brune I, Dondrup M, Kalinowski J, Plassmeier J, Puhler A, Wiegrabe I, Tauch A., J. Biotechnol. 106(2-3), 2003
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Huser AT, Becker A, Brune I, Dondrup M, Kalinowski J, Plassmeier J, Puhler A, Wiegrabe I, Tauch A., J. Biotechnol. 106(2-3), 2003
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BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes.
Liu X, Brutlag DL, Liu JS., Pac Symp Biocomput (), 2001
PMID: 11262934
Liu X, Brutlag DL, Liu JS., Pac Symp Biocomput (), 2001
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Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes.
Newton GL, Arnold K, Price MS, Sherrill C, Delcardayre SB, Aharonowitz Y, Cohen G, Davies J, Fahey RC, Davis C., J. Bacteriol. 178(7), 1996
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The gene ncgl2918 encodes a novel maleylpyruvate isomerase that needs mycothiol as cofactor and links mycothiol biosynthesis and gentisate assimilation in Corynebacterium glutamicum.
Feng J, Che Y, Milse J, Yin YJ, Liu L, Ruckert C, Shen XH, Qi SW, Kalinowski J, Liu SJ., J. Biol. Chem. 281(16), 2006
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Park JH, Roe JH., Mol. Microbiol. 68(4), 2008
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The SOS response of Escherichia coli
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AUTHOR UNKNOWN, 2005
DNA binding properties of the LexA repressor.
Schnarr M, Oertel-Buchheit P, Kazmaier M, Granger-Schnarr M., Biochimie 73(4), 1991
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Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon.
Keilhauer C, Eggeling L, Sahm H., J. Bacteriol. 175(17), 1993
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Keilhauer C, Eggeling L, Sahm H., J. Bacteriol. 175(17), 1993
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The Corynebacterium xerosis composite transposon Tn5432 consists of two identical insertion sequences, designated IS1249, flanking the erythromycin resistance gene ermCX.
Tauch A, Kassing F, Kalinowski J, Puhler A., Plasmid 34(2), 1995
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Tauch A, Kassing F, Kalinowski J, Puhler A., Plasmid 34(2), 1995
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Techniques for transformation of E. coli
AUTHOR UNKNOWN, 1985
AUTHOR UNKNOWN, 1985
Corynebacterium glutamicum DNA is subjected to methylation-restriction in Escherichia coli.
Tauch A, Kirchner O, Wehmeier L, Kalinowski J, Puhler A., FEMS Microbiol. Lett. 123(3), 1994
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Efficient electrotransformation of corynebacterium diphtheriae with a mini-replicon derived from the Corynebacterium glutamicum plasmid pGA1.
Tauch A, Kirchner O, Loffler B, Gotker S, Puhler A, Kalinowski J., Curr. Microbiol. 45(5), 2002
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PMID: 12232668
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension.
Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR., Gene 77(1), 1989
PMID: 2744488
Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR., Gene 77(1), 1989
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Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum.
Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A., Gene 145(1), 1994
PMID: 8045426
Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A., Gene 145(1), 1994
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Genome-wide analysis of the L-methionine biosynthetic pathway in Corynebacterium glutamicum by targeted gene deletion and homologous complementation.
Ruckert C, Puhler A, Kalinowski J., J. Biotechnol. 104(1-3), 2003
PMID: 12948640
Ruckert C, Puhler A, Kalinowski J., J. Biotechnol. 104(1-3), 2003
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The dual transcriptional regulator CysR in Corynebacterium glutamicum ATCC 13032 controls a subset of genes of the McbR regulon in response to the availability of sulphide acceptor molecules.
Ruckert C, Milse J, Albersmeier A, Koch DJ, Puhler A, Kalinowski J., BMC Genomics 9(), 2008
PMID: 18854009
Ruckert C, Milse J, Albersmeier A, Koch DJ, Puhler A, Kalinowski J., BMC Genomics 9(), 2008
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EMMA 2--a MAGE-compliant system for the collaborative analysis and integration of microarray data.
Dondrup M, Albaum SP, Griebel T, Henckel K, Junemann S, Kahlke T, Kleindt CK, Kuster H, Linke B, Mertens D, Mittard-Runte V, Neuweger H, Runte KJ, Tauch A, Tille F, Puhler A, Goesmann A., BMC Bioinformatics 10(), 2009
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The genes of lepA and hemN form a bicistronic operon in Bacillus subtilis.
Homuth G, Heinemann M, Zuber U, Schumann W., Microbiology (Reading, Engl.) 142 ( Pt 7)(), 1996
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Homuth G, Heinemann M, Zuber U, Schumann W., Microbiology (Reading, Engl.) 142 ( Pt 7)(), 1996
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Function of Corynebacterium glutamicum promoters in Escherichia coli, Streptomyces lividans, and Bacillus subtilis.
Patek M, Muth G, Wohlleben W., J. Biotechnol. 104(1-3), 2003
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Metabolic engineering of the L-valine biosynthesis pathway in Corynebacterium glutamicum using promoter activity modulation.
Holatko J, Elisakova V, Prouza M, Sobotka M, Nesvera J, Patek M., J. Biotechnol. 139(3), 2008
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Holatko J, Elisakova V, Prouza M, Sobotka M, Nesvera J, Patek M., J. Biotechnol. 139(3), 2008
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Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria.
Shaw WV., Meth. Enzymol. 43(), 1975
PMID: 1094240
Shaw WV., Meth. Enzymol. 43(), 1975
PMID: 1094240
WebLogo: a sequence logo generator.
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120
Integrative and autonomously replicating vectors for analysis of promoters in Corynebacterium glutamicum
AUTHOR UNKNOWN, 1998
AUTHOR UNKNOWN, 1998
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
Yanisch-Perron C, Vieira J, Messing J., Gene 33(1), 1985
PMID: 2985470
Yanisch-Perron C, Vieira J, Messing J., Gene 33(1), 1985
PMID: 2985470
Clustal W and Clustal X version 2.0.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG., Bioinformatics 23(21), 2007
PMID: 17846036
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG., Bioinformatics 23(21), 2007
PMID: 17846036
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