The small 6C RNA of Corynebacterium glutamicum is involved in the SOS response

. 2016 Sep ; 13 (9) : 848-60. [epub] 20160630

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27362471

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.

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Weiberg A, Bellinger M, Jin H. Conversations between kingdoms: small RNAs. Curr Opin Biotechnol 2015; 32:207-15; PMID:25622136; http://dx.doi.org/10.1016/j.copbio.2014.12.025 PubMed DOI PMC

Updegrove TB, Shabalina SA, Storz G. How do base-pairing small RNAs evolve? FEMS Microbiol Rev 2015; 39:379-91; PMID:25934120; http://dx.doi.org/10.1093/femsre/fuv014 PubMed DOI PMC

Miyakoshi M, Chao Y, Vogel J. Regulatory small RNAs from the 3′ regions of bacterial mRNAs. Curr Opin Microbiol 2015; 24:132-9; PMID:25677420; http://dx.doi.org/10.1016/j.mib.2015.01.013 PubMed DOI

Daub J, Eberhardt RY, Tate JG, Burge SW. Rfam: annotating families of non-coding RNA sequences. Methods Mol Biol 2015; 1269:349-63; PMID:25577390; http://dx.doi.org/10.1007/978-1-4939-2291-8_22 PubMed DOI

Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, et al.. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 2007; 35:4809-19; PMID:17621584; http://dx.doi.org/10.1093/nar/gkm487 PubMed DOI PMC

Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, et al.. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002; 417:141-7; PMID:12000953; http://dx.doi.org/10.1038/417141a PubMed DOI

Swiercz JP, Hindra Bobek J, Bobek J, Haiser HJ, Di Berardo C, Tjaden B, Elliot MA. Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res 2008; 36:7240-51; PMID:19008244; http://dx.doi.org/10.1093/nar/gkn898 PubMed DOI PMC

Arnvig KB, Young DB. Identification of small RNAs in Mycobacterium tuberculosis. Mol Microbiol 2009; 73:397-408; PMID:19555452; http://dx.doi.org/10.1111/j.1365-2958.2009.06777.x PubMed DOI PMC

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; PMID:24341750; http://dx.doi.org/10.1186/1471-2164-14-888 PubMed DOI PMC

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; PMID:24138339; http://dx.doi.org/10.1186/1471-2164-14-714 PubMed DOI PMC

Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2010; 329:533-8; PMID:20671182; http://dx.doi.org/10.1126/science.1188308 PubMed DOI PMC

Heidrich N, Moll I, Brantl S. In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res 2007; 35:4331-46; PMID:17576690; http://dx.doi.org/10.1093/nar/gkm439 PubMed DOI PMC

Pátek M, Nešvera J. Sigma factors and promoters in Corynebacterium glutamicum. J Biotechnol 2011; 154:101-13; http://dx.doi.org/10.1016/j.jbiotec.2011.01.017 PubMed DOI

Larisch C, Nakunst D, Hüser AT, Tauch A, Kalinowski J. The alternative sigma factor SigB of Corynebacterium glutamicum modulates global gene expression during transition from exponential growth to stationary phase. BMC Genomics 2007; 8:4; PMID:17204139; http://dx.doi.org/; http://dx.doi.org/10.1186/1471-2164-8-4 PubMed DOI PMC

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; 74:5146-52; PMID:18567683; http://dx.doi.org/10.1128/AEM.00944-08 PubMed DOI PMC

Holátko J, Silar R, Rabatinová A, Sanderová H, Halada P, Nešvera J, Krásný L, Pátek M. Construction of in vitro transcription system for Corynebacterium glutamicum and its use in the recognition of promoters of different classes. Appl Microbiol Biotechnol 2012; 96:521-9; http://dx.doi.org/10.1007/s00253-012-4336-1 PubMed DOI

Jungwirth B, Sala C, Kohl TA, Uplekar S, Baumbach J, Cole ST, Pühler A, Tauch A. High-resolution detection of DNA binding sites of the global transcriptional regulator GlxR in Corynebacterium glutamicum. Microbiology 2013; 159:12-22; PMID:23103979; http://dx.doi.org/10.1099/mic.0.062059-0 PubMed DOI

Cramer A, Gerstmeir R, Schaffer S, Bott M, Eikmanns BJ. Identification of RamA, a novel LuxR-type transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 2006; 188:2554-67; PMID:16547043; http://dx.doi.org/10.1128/JB.188.7.2554-2567.2006 PubMed DOI PMC

Auchter M, Cramer A, Huser A, Ruckert C, Emer D, Schwarz P, Arndt A, Lange C, Kalinowski J, Wendisch VF, et al.. RamA and RamB are global transcriptional regulators in Corynebacterium glutamicum and control genes for enzymes of the central metabolism. J Biotechnol 2011; 154:126-39; PMID:20620178; http://dx.doi.org/10.1016/j.jbiotec.2010.07.001 PubMed DOI

Jochmann N, Kurze AK, Czaja LF, Brinkrolf K, Brune I, Huser AT, Hansmeier N, Pühler A, Borovok I, Tauch A. Genetic makeup of the Corynebacterium glutamicum LexA regulon deduced from comparative transcriptomics and in vitro DNA band shift assays. Microbiology 2009; 155:1459-77; PMID:19372162; http://dx.doi.org/10.1099/mic.0.025841-0 PubMed DOI

Klug G, Cohen SN. 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; 172:5140-6; PMID:2394682 PubMed PMC

Richards J, Sundermeier T, Svetlanov A, Karzai AW. Quality control of bacterial mRNA decoding and decay. Biochim Biophys Acta 2008; 1779:574-82; PMID:18342642; http://dx.doi.org/10.1016/j.bbagrm.2008.02.008 PubMed DOI PMC

Massé E, Escorcia FE, Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 2003; 17:2374-83; http://dx.doi.org/10.1101/gad.1127103 PubMed DOI PMC

Wakaki S, Marumo H, Tomioka K, Shimizu G, Kato E, Kamada H, Kudo S, Fujimoto Y. Isolation of new fractions of antitumor mitomycins. Antibiot Chemother (Northfield) 1958; 8:228-40; PMID:24544727 PubMed

Smollett KL, Smith KM, Kahramanoglou C, Arnvig KB, Buxton RS, Davis EO. Global analysis of the regulon of the transcriptional repressor LexA, a key component of SOS response in Mycobacterium tuberculosis. J Biol Chem 2012; 287:22004-14; PMID:22528497; http://dx.doi.org/10.1074/jbc.M112.357715 PubMed DOI PMC

Seow HA, Penketh PG, Baumann RP, Sartorelli AC. Bioactivation and resistance to mitomycin C. Methods Enzymol 2004; 382:221-33; PMID:15047104; http://dx.doi.org/10.1016/S0076-6879(04)82012-3 PubMed DOI

Weel-Sneve R, Kristiansen KI, Odsbu I, Dalhus B, Booth J, Rognes T, Skarstad K, Bjørås M. Single transmembrane peptide DinQ modulates membrane-dependent activities. PLoS Genet 2013; 9:e1003260; PMID:23408903; http://dx.doi.org/10.1371/journal.pgen.1003260 PubMed DOI PMC

Vogel J, Argaman L, Wagner EG, Altuvia S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 2004; 14:2271-6; PMID:15620655; http://dx.doi.org/10.1016/j.cub.2004.12.003 PubMed DOI

Unoson C, Wagner EG. A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol Microbiol 2008; 70:258-70; PMID:18761622; http://dx.doi.org/10.1111/j.1365-2958.2008.06416.x PubMed DOI

Donovan C, Bramkamp M. Cell division in Corynebacterineae. Front Microbiol 2014; 5:132; PMID:24782835; http://dx.doi.org/10.3389/fmicb.2014.00132 PubMed DOI PMC

Jonas K. To divide or not to divide: control of the bacterial cell cycle by environmental cues. Curr Opin Microbiol 2014; 18:54-60; PMID:24631929; http://dx.doi.org/10.1016/j.mib.2014.02.006 PubMed DOI

Ogino H, Teramoto H, Inui M, Yukawa H. DivS, a novel SOS-inducible cell-division suppressor in Corynebacterium glutamicum. Mol Microbiol 2008; 67:597-608; PMID:18086211; http://dx.doi.org/10.1111/j.1365-2958.2007.06069.x PubMed DOI

Ramos A, Letek M, Campelo AB, Vaquera J, Mateos LM, Gil JA. Altered morphology produced by ftsZ expression in Corynebacterium glutamicum ATCC 13869. Microbiology 2005; 151:2563-72; PMID:16079335; http://dx.doi.org/10.1099/mic.0.28036-0 PubMed DOI

Maeda T, Tanaka Y, Takemoto N, Hamamoto N, Inui M. RNase III mediated cleavage of the coding region of mraZ mRNA is required for efficient cell division in Corynebacterium glutamicum. Mol Microbiol 2016; 99:1149-66; PMID:26713407; http://dx.doi.org/10.1111/mmi.13295 PubMed DOI

Keilhauer C, Eggeling L, Sahm H. Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon. J Bacteriol 1993; 175:5595-603; PMID:8366043 PubMed PMC

Sambrook J, Russell DW. Molecular cloning: a laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, 2001.

Niebisch A, Bott M. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Arch Microbiol 2001; 175:282-94; PMID:11382224; http://dx.doi.org/10.1007/s002030100262 PubMed DOI

Taniguchi H, Wendisch VF. Exploring the role of sigma factor gene expression on production by Corynebacterium glutamicum: sigma factor H and FMN as example. Front Microbiol 2015; 6:740; PMID:26257719; http://dx.doi.org/10.3389/fmicb.2015.00740 PubMed DOI PMC

van Ooyen J, Emer D, Bussmann M, Bott M, Eikmanns BJ, Eggeling L. Citrate synthase in Corynebacterium glutamicum is encoded by two gltA transcripts which are controlled by RamA, RamB, and GlxR. J Biotechnol 2011; 154:140-8; PMID:20630483; http://dx.doi.org/10.1016/j.jbiotec.2010.07.004 PubMed DOI

Polen T, Rittmann D, Wendisch VF, Sahm H. DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate. Appl Environ Microbiol 2003; 69:1759-74; PMID:12620868; http://dx.doi.org/10.1128/AEM.69.3.1759-1774.2003 PubMed DOI PMC

Krause JP, Polen T, Youn JW, Emer D, Eikmanns BJ, Wendisch VF. Regulation of the malic enzyme gene malE by the transcriptional regulator MalR in Corynebacterium glutamicum. J Biotechnol 2012; 159:204-15; PMID:22261175; http://dx.doi.org/10.1016/j.jbiotec.2012.01.003 PubMed DOI

Polen T, Schluesener D, Poetsch A, Bott M, Wendisch VF. Characterization of citrate utilization in Corynebacterium glutamicum by transcriptome and proteome analysis. FEMS Microbiol Lett 2007; 273:109-19; PMID:17559405; http://dx.doi.org/10.1111/j.1574-6968.2007.00793.x PubMed DOI

Knoppová M, Phensaijai M, Veselý M, Zemanová M, Nešvera J, Pátek M. Plasmid vectors for testing in vivo promoter activities in Corynebacterium glutamicum and Rhodococcus erythropolis. Curr Microbiol 2007; 55:234-9; http://dx.doi.org/10.1007/s00284-007-0106-1 PubMed DOI

Neumeyer A, Hubschmann T, Muller S, Frunzke J. Monitoring of population dynamics of Corynebacterium glutamicum by multiparameter flow cytometry. Microb Biotechnol 2013; 6:157-67; PMID:23279937; http://dx.doi.org/10.1111/1751-7915.12018 PubMed DOI PMC

Larisch C, Nakunst D, Huser AT, Tauch A, Kalinowski J. The alternative sigma factor SigB of Corynebacterium glutamicum modulates global gene expression during transition from exponential growth to stationary phase. BMC Genomics 2007; 8:4; PMID:17204139; http://dx.doi.org/10.1186/1471-2164-8-4 PubMed DOI PMC

Hanahan D. Techniques for transformation of E. coli In DNA-cloning. Vol1 Glover DM. (ed) Oxford: IRL-Press, pp 109-135 1985.

Dubendorff JW, Studier FW. Controlling basal expression in an inducible T7 expression system by blocking the target T7 promoter with lac repressor. J Mol Biol 1991; 219:45-59; PMID:1902522; http://dx.doi.org/10.1016/0022-2836(91)90856-2 PubMed DOI

Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985; 33:103-19; PMID:2985470; http://dx.doi.org/10.1016/0378-1119(85)90120-9 PubMed DOI

Schäfer 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; 145:69-73; http://dx.doi.org/10.1016/0378-1119(94)90324-7 PubMed DOI

Cremer J, Eggeling L, Sahm H. Control of the lysine biosynthesis sequence in Corynebacterium glutamicum as analyzed by overexpression of the individual corresponding genes. Appl Environ Microbiol 1991; 57:1746-52; PMID:16348510 PubMed PMC

Kirchner O, Tauch A. Tools for genetic engineering in the amino acid-producing bacterium Corynebacterium glutamicum. J Biotechnol 2003; 104:287-99; PMID:12948646; http://dx.doi.org/10.1016/S0168-1656(03)00148-2 PubMed DOI

Schröder 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; 34:685-737; PMID:20491930; http://dx.doi.org/10.1111/j.1574-6976.2010.00228.x PubMed DOI

Wennerhold J, Krug A, Bott M. The AraC-type regulator RipA represses aconitase and other iron proteins from Corynebacterium under iron limitation and is itself repressed by DtxR. J Biol Chem 2005; 280:40500-8; PMID:16179344; http://dx.doi.org/10.1074/jbc.M508693200 PubMed DOI

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