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Corynebacterium glutamicum RNase E/G-type endoribonuclease encoded by NCgl2281 is involved in the 5′ maturation of 5S rRNA

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Abstract

Corynebacterium glutamicum has one RNase E/G ortholog and one RNase J ortholog but no RNase Y. We previously reported that the C. glutamicum NCgl2281 gene encoding the RNase E/G ortholog complemented the rng::cat mutation in Escherichia coli but not the rne-1 mutation. In this study, we constructed an NCgl2281 knockout mutant and found that the mutant cells accumulated 5S rRNA precursor molecules. The processing of 16S and 23S rRNA, tRNA, and tmRNA was normal. Primer extension analysis revealed that the RNase E/G ortholog cleaved at the −1 site of the 5′ end of 5S rRNA. However, 3′ maturation was essentially unaffected. These findings showed that C. glutamicum NCgl2281 endoribonuclease is involved in the 5′ maturation of 5S rRNA. This is the first report showing the physiological function of the RNase E/G ortholog in bacteria having one RNase E/G and one RNase J but no RNase Y.

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References

  • Amador E, Castro JM, Correia A, Martín JF (1999) Structure and organization of the rrnD operon of ‘Brevibacterium lactofermentum’: analysis of the 16S rRNA gene. Microbiology 145:915–924

    Article  PubMed  CAS  Google Scholar 

  • Apirion D, Lassar AB (1978) A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J Biol Chem 253:1738–1742

    PubMed  CAS  Google Scholar 

  • Arraiano CM, Yancey SD, Kushner SR (1988) Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J Bacteriol 170:4625–4633

    PubMed  CAS  Google Scholar 

  • Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, Moreira RN, Pobre V, Reis FP, Saramago M, Silva IJ, Viegas SC (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34:883–923

    PubMed  CAS  Google Scholar 

  • Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, Mathy N, Tobin C, Daou R, Szyk J, Condon C (2007) Maturation of the 5′ end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63:127–138

    Article  PubMed  CAS  Google Scholar 

  • Condon C, Brechemier-Baey D, Beltchev B, Grunberg-Manago M, Putzer H (2001) Identification of the gene encoding the 5S ribosomal RNA maturase in Bacillus subtilis: mature 5S rRNA is dispensable for ribosome function. RNA 7:242–253

    Article  PubMed  CAS  Google Scholar 

  • de la Sierra-Gallay IL, Zig L, Jamalli A, Putzer H (2008) Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15:206–212

    Article  Google Scholar 

  • Deutscher MP (2006) Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res 34:659–666

    Article  PubMed  CAS  Google Scholar 

  • Even S, Pellegrini O, Zig L, Labas V, Vinh J, Bréchemmier-Baey D, Putzer H (2005) Ribonuclease J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33:2141–2152

    Article  PubMed  CAS  Google Scholar 

  • Gao YG, Suzuki H, Itou H, Zhou Y, Tanaka Y, Wachi M, Watanabe N, Tanaka I, Yao M (2008) Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization. Nucleic Acids Res 36:7110–7123

    Article  PubMed  CAS  Google Scholar 

  • Gegenheimer P, Apirion D (1975) Escherichia coli ribosomal ribonucleic acids are not cut from an intact precursor molecule. J Biol Chem 250:2407–2409

    PubMed  CAS  Google Scholar 

  • Ghora BK, Apirion D (1978) Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15:1055–1066

    Article  PubMed  CAS  Google Scholar 

  • Hermann T (2003) Industrial production of amino acids by coryneform bacteria. J Biotechnol 104:155–172

    Article  PubMed  CAS  Google Scholar 

  • Herskovitz MA, Bechhofer DH (2000) Endoribonuclease RNase III is essential in Bacillus subtilis. Mol Microbiol 38:1027–1033

    Article  PubMed  CAS  Google Scholar 

  • Jiang X, Diwa A, Belasco JG (2000) Regions of RNase E important for 5′-end-dependent RNA cleavage and autoregulated synthesis. J Bacteriol 182:2468–2475

    Article  PubMed  CAS  Google Scholar 

  • Kaberdin VR, Miczak A, Jakobsen JS, Lin-Chao S, McDowall KJ, von Gabain A (1998) The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc Natl Acad Sci USA 95:11637–11642

    Article  PubMed  CAS  Google Scholar 

  • King TC, Sirdeshmukh R, Schlessinger D (1984) RNase III cleavage is obligate for maturation but not for function of Escherichia coli pre-23S rRNA. Proc Natl Acad Sci USA 81:185–188

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita S, Udaka S, Shimono M (1957) Studies on the amino acid fermentation. I. Production of l-glutamic acid by various microorganisms. J Gen Appl Microbiol 3:193–205

    Article  CAS  Google Scholar 

  • Kushner SR (2004) mRNA decay in prokaryotes and eukaryotes: different approaches to a similar problem. IUBMB Life 56:585–594

    Article  PubMed  CAS  Google Scholar 

  • Lee K, Cohen SN (2003) A Streptomyces coelicolor functional orthologue of Escherichia coli RNase E shows shuffling of catalytic and PNPase-binding domains. Mol Microbiol 48:349–360

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Deutscher MP (1995) The tRNA processing enzyme RNase T is essential for maturation of 5S RNA. Proc Natl Acad Sci USA 92:6883–6886

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Deutscher MP (2002) RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA 8:97–109

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Pandit S, Deutscher MP (1999a) RNase G (CafA protein) and RNase E are both required for the 5′ maturation of 16S ribosomal RNA. EMBO J 18:2878–2885

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Pandit S, Deutscher MP (1999b) Maturation of 23S ribosomal RNA requires the exoribonuclease RNase T. RNA 5:139–146

    Article  PubMed  CAS  Google Scholar 

  • Licht A, Preis S, Brantl S (2005) Implication of CcpN in the regulation of a novel untranslated RNA (SR1) in Bacillus subtilis. Mol Microbiol 58:189–206

    Article  PubMed  CAS  Google Scholar 

  • Liiv A, Remme J (1998) Base-pairing of 23S rRNA ends is essential for ribosomal large subunit assembly. J Mol Biol 276:537–545

    Article  PubMed  CAS  Google Scholar 

  • Lin-Chao S, Wong TT, McDowall KJ, Cohen SN (1994) Effects of nucleotide sequence on the specificity of rne-dependent and RNase E-mediated cleavages of RNA I encoded by the pBR322 plasmid. J Biol Chem 269:10797–10803

    PubMed  CAS  Google Scholar 

  • Lin-Chao S, Wei CL, Lin YT (1999) RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity. Proc Natl Acad Sci USA 96:12406–12411

    Article  PubMed  CAS  Google Scholar 

  • Mackie GA (1991) Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the product of the ams gene in vivo and in vitro. J Bacteriol 173:2488–2497

    PubMed  CAS  Google Scholar 

  • Mackie GA (1998) Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395:720–723

    Article  PubMed  CAS  Google Scholar 

  • Maeda T, Sakai T, Wachi M (2009) The Corynebacterium glutamicum NCgl2281 encoding an RNase E/G family endoribonuclease can complement the Escherichia coli rng:cat mutation but not the rne-1 mutation. Biosci Biotechnol Biochem 73:2281–2286

    Article  PubMed  CAS  Google Scholar 

  • Martín JF, Barreiro C, González-Lavado E, Barriuso M (2003) Ribosomal RNA and ribosomal proteins in corynebacteria. J Biotechnol 104:41–53

    Article  PubMed  Google Scholar 

  • Mathy N, Bénard L, Pellegrini O, Daou R, Wen T, Condon C (2007) 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129:681–692

    Article  PubMed  CAS  Google Scholar 

  • McDowall KJ, Cohen SN (1996) The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J Mol Biol 255:349–355

    Article  PubMed  CAS  Google Scholar 

  • McDowall KJ, Lin-Chao S, Cohen SN (1994) A + U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269:10790–10796

    PubMed  CAS  Google Scholar 

  • Misra TK, Apirion D (1979) RNase E, an RNA processing enzyme from Escherichia coli. J Biol Chem 254:11154–11159

    PubMed  CAS  Google Scholar 

  • Mohanty BK, Kushner SR (2007) Ribonuclease P processes polycistronic tRNA transcripts in Escherichia coli independent of ribonuclease E. Nucleic Acids Res 35:7614–7625

    Article  PubMed  CAS  Google Scholar 

  • Mohanty BK, Kushner SR (2008) Rho-independent transcription terminators inhibit RNase P processing of the secG leuU and metT tRNA polycistronic transcripts in Escherichia coli. Nucleic Acids Res 36:364–375

    Article  PubMed  CAS  Google Scholar 

  • Nikolaev N, Schlessinger D, Wellauer PK (1974) 30S pre-ribosomal RNA of Escherichia coli and products of cleavage by ribonuclease III: length and molecular weight. J Mol Biol 86:741–748

    Article  PubMed  CAS  Google Scholar 

  • Ono M, Kuwano M (1979) A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of messenger RNA. J Mol Biol 129:343–357

    Article  PubMed  CAS  Google Scholar 

  • Ow MC, Kushner SR (2002) Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes Dev 16:1102–1115

    Article  PubMed  CAS  Google Scholar 

  • Park YH, Hori H, Suzuki K, Osawa S, Kamagata K (1987) Phylogenetic analysis of the coryneform bacteria by 5S rRNA sequences. J Bacteriol 169:1801–1806

    PubMed  CAS  Google Scholar 

  • Redko Y, Bechhofer DH, Condon C (2008) Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis. Mol Microbiol 68:1096–1106

    Article  PubMed  CAS  Google Scholar 

  • Robertson HD, Webster RE, Zinder ND (1968) Purification and properties of ribonuclease III from Escherichia coli. J Biol Chem 243:82–91

    PubMed  CAS  Google Scholar 

  • Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A (1994) 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 145:69–73

    Article  PubMed  Google Scholar 

  • Shahbabian K, Jamalli A, Zig L, Putzer H (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28:3523–3533

    Article  PubMed  CAS  Google Scholar 

  • Sirdeshmukh R, Schlessinger D (1985) Ordered processing of Escherichia coli 23S rRNA in vitro. Nucleic Acids Res 13:5041–5054

    Article  PubMed  CAS  Google Scholar 

  • Sogin ML, Pace NR (1974) In vitro maturation of precursors of 5S ribosomal RNA from Bacillus subtilis. Nature 252:598–600

    Article  PubMed  CAS  Google Scholar 

  • Taraseviciene L, Björk GR, Uhlin BE (1995) Evidence for an RNA binding region in the Escherichia coli processing endoribonuclease RNase E. J Biol Chem 270:26391–26398

    Article  PubMed  CAS  Google Scholar 

  • Tauch A, Homann I, Mormann S, Rüberg S, Billault A, Bathe B, Brand S, Brockmann-Gretza O, Rückert C, Schischka N, Wrenger C, Hoheisel J, Möckel B, Huthmacher K, Pfefferle W, Pühler A, Kalinowski J (2002) Strategy to sequence the genome of Corynebacterium glutamicum ATCC 13032: use of a cosmid and a bacterial artificial chromosome library. J Biotechnol 95:25–38

    Article  PubMed  CAS  Google Scholar 

  • Tock MR, Walsh AP, Carroll G, McDowall KJ (2000) The CafA protein required for the 5′-maturation of 16S rRNA is a 5′-end-dependent ribonuclease that has context-dependent broad sequence specificity. J Biol Chem 275:8726–8732

    Article  PubMed  CAS  Google Scholar 

  • Vanzo NF, Li YS, Py B, Blum E, Higgins CF, Raynal LC, Krisch HM, Carpousis AJ (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12:2770–2781

    Article  PubMed  CAS  Google Scholar 

  • Wachi M, Umitsuki G, Nagai K (1997) Functional relationship between Escherichia coli RNase E and the CafA protein. Mol Gen Genet 253:515–519

    Article  PubMed  CAS  Google Scholar 

  • Wachi M, Umitsuki G, Shimizu M, Takada A, Nagai K (1999) Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5′ end of 16S rRNA. Biochem Biophys Res Commun 259:483–488

    Article  PubMed  CAS  Google Scholar 

  • Worrall JA, Luisi BF (2007) Information available at cut rates: structure and mechanism of ribonucleases. Curr Opin Struct Biol 17:128–137

    Article  PubMed  CAS  Google Scholar 

  • Zeller ME, Csanadi A, Miczak A, Rose T, Bizebard T, Kaberdin VR (2007) Quaternary structure and biochemical properties of mycobacterial RNase E/G. Biochem J 403:207–215

    Article  PubMed  CAS  Google Scholar 

  • Zemanová M, Kadeřábková P, Pátek M, Knoppová M, Šilar R, Nešvera J (2008) Chromosomally encoded small antisense RNA in Corynebacterium glutamicum. FEMS Microbiol Lett 279:195–201

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by a grant-in-aid for Scientific Research (B) (20380047 to M. W.) from the Japan Society for Promotion of Science, a grant from the Global COE Program of the Ministry of Education, Culture, Sports, Science and Technology of Japan, and a grant from the Ministry of Economy, Trade and Industry of Japan entrusted by the New Energy and Industrial Technology Development Organization.

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  1. Department of Bioengineering, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama, 226-8503, Japan

    Tomoya Maeda & Masaaki Wachi

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  1. Tomoya Maeda
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  2. Masaaki Wachi
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Correspondence to Masaaki Wachi.

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Communicated by Reinhard Kraemer.

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Maeda, T., Wachi, M. Corynebacterium glutamicum RNase E/G-type endoribonuclease encoded by NCgl2281 is involved in the 5′ maturation of 5S rRNA. Arch Microbiol 194, 65–73 (2012). https://doi.org/10.1007/s00203-011-0728-3

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  • DOI: https://doi.org/10.1007/s00203-011-0728-3

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