The Small 6C RNA of Corynebacterium Glutamicum is Involved in the SOS Response

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2016 Jul 1

PMID 27362471

Citations 5

Authors

Jennifer Pahlke

Hana Dostalova

Jiri Holatko

Ursula Degner

Michael Bott

Miroslav Patek

Tino Polen

Affiliations

Soon will be listed here.

Abstract

The 6C RNA family is a class of small RNAs highly conserved in Actinobacteria, including the genera Mycobacterium, Streptomyces and Corynebacterium whose physiological function has not yet been elucidated. We found that strong transcription of the cgb_03605 gene, which encodes 6C RNA in C. glutamicum, was driven by the SigA- and SigB-dependent promoter Pcgb_03605. 6C RNA was detected at high level during exponential growth phase (180 to 240 molcules per cell) which even increased at the entry of the stationary phase. 6C RNA level did not decrease within 240 min after transcription had been stopped with rifampicin, which suggests high 6C RNA stability. The expression of cgb_03605 further increased approximately twofold in the presence of DNA-damaging mitomycin C (MMC) and nearly threefold in the absence of LexA. Deletion of the 6C RNA gene cgb_03605 resulted in a higher sensitivity of C. glutamicum toward MMC and UV radiation. These results indicate that 6C RNA is involved in the DNA damage response. Both 6C RNA level-dependent pausing of cell growth and branched cell morphology in response to MMC suggest that 6C RNA may also be involved in a control of cell division.

Citing Articles

Genomic, Phylogenetic and Physiological Characterization of the PAH-Degrading Strain 135.

Frantsuzova E, Bogun A, Kopylova O, Vetrova A, Solyanikova I, Streletskii R Biology (Basel). 2024; 13(5).

PMID: 38785821 PMC: 11117675. DOI: 10.3390/biology13050339.

Comparative genome analysis of mycobacteria focusing on tRNA and non-coding RNA.

Krishna Behra P, Pettersson B, Ramesh M, Das S, Dasgupta S, Kirsebom L BMC Genomics. 2022; 23(1):704.

PMID: 36243697 PMC: 9569102. DOI: 10.1186/s12864-022-08927-5.

Structure and functional implications of WYL domain-containing bacterial DNA damage response regulator PafBC.

Muller A, Leibundgut M, Ban N, Weber-Ban E Nat Commun. 2019; 10(1):4653.

PMID: 31604936 PMC: 6789036. DOI: 10.1038/s41467-019-12567-x.

Comparative genomics of Mycobacterium mucogenicum and Mycobacterium neoaurum clade members emphasizing tRNA and non-coding RNA.

Krishna Behra P, Pettersson B, Das S, Dasgupta S, Kirsebom L BMC Evol Biol. 2019; 19(1):124.

PMID: 31215393 PMC: 6582537. DOI: 10.1186/s12862-019-1447-7.

Mycobacterium tuberculosis 6C sRNA binds multiple mRNA targets via C-rich loops independent of RNA chaperones.

Mai J, Rao C, Watt J, Sun X, Lin C, Zhang L Nucleic Acids Res. 2019; 47(8):4292-4307.

PMID: 30820540 PMC: 6486639. DOI: 10.1093/nar/gkz149.

References

Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A . 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. Gene. 1994; 145(1):69-73. DOI: 10.1016/0378-1119(94)90324-7. View

Mentz A, Neshat A, Pfeifer-Sancar K, Puhler A, Ruckert C, Kalinowski J . Comprehensive discovery and characterization of small RNAs in Corynebacterium glutamicum ATCC 13032. BMC Genomics. 2013; 14:714. PMC: 4046766. DOI: 10.1186/1471-2164-14-714. View

Smollett K, Smith K, Kahramanoglou C, Arnvig K, Buxton R, Davis E . Global analysis of the regulon of the transcriptional repressor LexA, a key component of SOS response in Mycobacterium tuberculosis. J Biol Chem. 2012; 287(26):22004-14. PMC: 3381160. DOI: 10.1074/jbc.M112.357715. View

Knoppova M, Phensaijai M, Vesely M, Zemanova M, Nesvera J, Patek M . Plasmid vectors for testing in vivo promoter activities in Corynebacterium glutamicum and Rhodococcus erythropolis. Curr Microbiol. 2007; 55(3):234-9. DOI: 10.1007/s00284-007-0106-1. View

Schroder J, Tauch A . Transcriptional regulation of gene expression in Corynebacterium glutamicum: the role of global, master and local regulators in the modular and hierarchical gene regulatory network. FEMS Microbiol Rev. 2010; 34(5):685-737. DOI: 10.1111/j.1574-6976.2010.00228.x. View

Klug G, Cohen S . Combined actions of multiple hairpin loop structures and sites of rate-limiting endonucleolytic cleavage determine differential degradation rates of individual segments within polycistronic puf operon mRNA. J Bacteriol. 1990; 172(9):5140-6. PMC: 213173. DOI: 10.1128/jb.172.9.5140-5146.1990. View

Bentley S, Chater K, Challis G, Thomson N, James K, Harris D . Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature. 2002; 417(6885):141-7. DOI: 10.1038/417141a. View

Pfeifer-Sancar K, Mentz A, Ruckert C, Kalinowski J . Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique. BMC Genomics. 2013; 14:888. PMC: 3890552. DOI: 10.1186/1471-2164-14-888. View

Jungwirth B, Sala C, Kohl T, Uplekar S, Baumbach J, Cole S . High-resolution detection of DNA binding sites of the global transcriptional regulator GlxR in Corynebacterium glutamicum. Microbiology (Reading). 2012; 159(Pt 1):12-22. DOI: 10.1099/mic.0.062059-0. View

10.

Polen T, Rittmann D, Wendisch V, Sahm H . DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate. Appl Environ Microbiol. 2003; 69(3):1759-74. PMC: 150104. DOI: 10.1128/AEM.69.3.1759-1774.2003. View

11.

Holatko J, Silar R, Rabatinova A, Sanderova H, Halada P, Nesvera J . Construction of in vitro transcription system for Corynebacterium glutamicum and its use in the recognition of promoters of different classes. Appl Microbiol Biotechnol. 2012; 96(2):521-9. DOI: 10.1007/s00253-012-4336-1. View

12.

Weel-Sneve R, Kristiansen K, Odsbu I, Dalhus B, Booth J, Rognes T . Single transmembrane peptide DinQ modulates membrane-dependent activities. PLoS Genet. 2013; 9(2):e1003260. PMC: 3567139. DOI: 10.1371/journal.pgen.1003260. View

13.

Cramer A, Gerstmeir R, Schaffer S, Bott M, Eikmanns B . Identification of RamA, a novel LuxR-type transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol. 2006; 188(7):2554-67. PMC: 1428430. DOI: 10.1128/JB.188.7.2554-2567.2006. View

14.

Ogino H, Teramoto H, Inui M, Yukawa H . DivS, a novel SOS-inducible cell-division suppressor in Corynebacterium glutamicum. Mol Microbiol. 2007; 67(3):597-608. DOI: 10.1111/j.1365-2958.2007.06069.x. View

15.

Neumeyer A, Hubschmann T, Muller S, Frunzke J . Monitoring of population dynamics of Corynebacterium glutamicum by multiparameter flow cytometry. Microb Biotechnol. 2013; 6(2):157-67. PMC: 3917458. DOI: 10.1111/1751-7915.12018. View

16.

Masse E, Escorcia F, Gottesman S . Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 2003; 17(19):2374-83. PMC: 218075. DOI: 10.1101/gad.1127103. View

17.

Jochmann N, Kurze A, Czaja L, Brinkrolf K, Brune I, Huser A . Genetic makeup of the Corynebacterium glutamicum LexA regulon deduced from comparative transcriptomics and in vitro DNA band shift assays. Microbiology (Reading). 2009; 155(Pt 5):1459-1477. DOI: 10.1099/mic.0.025841-0. View

18.

Weiberg A, Bellinger M, Jin H . Conversations between kingdoms: small RNAs. Curr Opin Biotechnol. 2015; 32:207-215. PMC: 4387066. DOI: 10.1016/j.copbio.2014.12.025. View

19.

Ehira S, Shirai T, Teramoto H, Inui M, Yukawa H . Group 2 sigma factor SigB of Corynebacterium glutamicum positively regulates glucose metabolism under conditions of oxygen deprivation. Appl Environ Microbiol. 2008; 74(16):5146-52. PMC: 2519270. DOI: 10.1128/AEM.00944-08. View

20.

Kirchner O, Tauch A . Tools for genetic engineering in the amino acid-producing bacterium Corynebacterium glutamicum. J Biotechnol. 2003; 104(1-3):287-99. DOI: 10.1016/s0168-1656(03)00148-2. View