Transcriptome sequencing revealed the transcriptional organization at ribosome-mediated attenuation sites in Corynebacterium glutamicum and identified a novel attenuator involved in aromatic amino acid biosynthesis

Journal of Biotechnology

Volumn 190, Issue , 2014, Pages 55-63

  Neshat, Armin ^a   Mentz, Almut ^a   Rückert, Christian ^a   Kalinowski, Jörn ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Amino acid biosynthesis; Corynebacterium glutamicum; RNA sequencing; Small RNAs; Transcriptional attenuation

Indexed keywords

AROMATIC COMPOUNDS; BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES; NUCLEIC ACIDS; PEPTIDES; POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION;

AMINO ACID SEQUENCE MOTIFS; AROMATIC AMINO ACID; CORYNEBACTERIUM GLUTAMICUM; ECONOMIC IMPORTANCE; GRAM-POSITIVE BACTERIUM; HIGH-RESOLUTION TECHNIQUES; SMALL RNA; TRANSCRIPTIONAL ATTENUATION;

AMINO ACIDS;

3 DEOXY 7 PHOSPHOHEPTULONATE SYNTHASE; AROF PROTEIN; AROMATIC AMINO ACID; BACTERIAL PROTEIN; COMPLEMENTARY DNA; DIPEPTIDE; LEUA PROTEIN; PHENYLALANINE; TRANSCRIPTOME; TRANSFER RNA; TYROSINE; UNCLASSIFIED DRUG; RNA;

AMINO ACID SEQUENCE; AMINO ACID SYNTHESIS; ARTICLE; AUXOTROPHIC MUTANT; BACTERIAL GENE; CATALYSIS; CORYNEBACTERIUM GLUTAMICUM; DNA LIBRARY; GENE EXPRESSION; MICROBIAL ATTENUATION; NONHUMAN; OPEN READING FRAME; OPERON; PHYLOGENY; PROMOTER REGION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; RNA ANALYSIS; RNA SEQUENCE; TIME; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; SEQUENCE ANALYSIS;

CORYNEBACTERIUM GLUTAMICUM;

3-DEOXY-7-PHOSPHOHEPTULONATE SYNTHASE; AMINO ACIDS, AROMATIC; CORYNEBACTERIUM GLUTAMICUM; GENE EXPRESSION REGULATION, BACTERIAL; GENE LIBRARY; OPERON; RIBOSOMES; RNA; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84911195380     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.05.033     Document Type: Article

References (78)

1. Ajinomoto Co. First Quarter-FY2013 Market and Other Information 2013, Ajinomoto Co.
2. Altschul S., Gish W., Miller W. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Baumbach J., Brinkrolf K., Czaja L.F., Rahmann S., Tauch A. CoryneRegNet: an ontology-based data warehouse of corynebacterial transcription factors and regulatory networks. BMC Genomics 2006, 7:24.
4. Becker J., Wittmann C. Bio-based production of chemicals, materials and fuels-Corynebacterium glutamicum as versatile cell factory. Curr. Opin. Biotechnol. 2012, 23:631-640.
5. Brock J.E., Pourshahian S., Giliberti J., Limbach P.A., Janssen G.R. Ribosomes bind leaderless mRNA in Escherichia coli through recognition of their 5'-terminal AUG. RNA 2008, 14:2159-2169.
6. Burge S.W., Daub J., Eberhardt R., Tate J., Barquist L., Nawrocki E.P., Eddy S.R., Gardner P.P., Bateman A. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res. 2013, 41:D226-D232.
7. Cortes T., Schubert O.T., Rose G., Arnvig K.B., Comas I., Aebersold R., Young D.B. Genome-wide mapping of transcriptional start sites defines an extensive leaderless transcriptome in Mycobacterium tuberculosis. Cell Rep. 2013, 5:1121-1131.
8. Den Hengst C.D., Buttner M.J. Redox control in actinobacteria. Biochim. Biophys. Acta 2008, 1780:1201-1216.
9. Donà V., Rodrigue S., Dainese E., Palù G., Gaudreau L., Manganelli R., Provvedi R. Evidence of complex transcriptional, translational, and posttranslational regulation of the extracytoplasmic function sigma factor sigmaE in Mycobacterium tuberculosis. J. Bacteriol. 2008, 190:5963-5971.
10. Eggeling I., Cordes C., Eggeling L., Sahm H. Regulation of acetohydroxy acid synthase in Corynebacterium glutamicum during fermentation of α-ketobutyrate to l-isoleucine. Appl. Microbiol. Biotechnol. 1987, 25:346-351.
11. Elišáková V., Pátek M., Holátko J., Nesvera J., Leyval D., Goergen J.-L., Delaunay S. Feedback-resistant acetohydroxy acid synthase increases valine production in Corynebacterium glutamicum. Appl. Environ. Microbiol. 2005, 71:207-213.
12. Giegerich R., Voss B., Rehmsmeier M. Abstract shapes of RNA. Nucleic Acids Res. 2004, 32:4843-4851.
13. Gollnick P., Babitzke P., Antson A., Yanofsky C. Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. Annu. Rev. Genet. 2005, 39:47-68.
14. Gopinath V., Murali A., Dhar K.S., Nampoothiri K.M. Corynebacterium glutamicum as a potent biocatalyst for the bioconversion of pentose sugars to value-added products. Appl. Microbiol. Biotechnol. 2012, 93:95-106.
15. Green N., Grundy F., Henkin T. The T box mechanism: tRNA as a regulatory molecule. FEBS Lett. 2010, 584:318-324.
16. Grill S., Moll I., Hasenöhrl D., Gualerzi C.O., Bläsi U. Modulation of ribosomal recruitment to 5'-terminal start codons by translation initiation factors IF2 and IF3. FEBS Lett. 2001, 495:167-171.
17. Guo R.-T., Ko T.-P., Chen A.P.-C., Kuo C.-J., Wang A.H.-J., Liang P.-H. Crystal structures of undecaprenyl pyrophosphate synthase in complex with magnesium, isopentenyl pyrophosphate, and farnesyl thiopyrophosphate: roles of the metal ion and conserved residues in catalysis. J. Biol. Chem. 2005, 280:20762-20774.
18. Heery D.M., Dunican L.K. Cloning of the trp gene cluster from a tryptophan-hyperproducing strain of Corynebacterium glutamicum: identification of a mutation in the trp leader sequence. Appl. Environ. Microbiol. 1993, 59:791-799.
19. Henkin T.M., Yanofsky C. Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. BioEssays 2002, 24:700-707.
20. Hermann T. Industrial production of amino acids by coryneform bacteria. J. Biotechnol. 2003, 104:155-172.
21. Herrmann K.M. The common aromatic biosynthetic pathway. Amino Acids: Biosynthsis and Genetic Regulation 1983, 301-322. Addison-Wesley, Reading, MA. K.M. Herrmann, R.L. Somerville (Eds.).
22. Hilker R., Stadermann K.B., Doppmeier D., Kalinowski J., Stoye J., Straube J., Winnebald J., Goesmann A. Genome analysis ReadXplorer - Visualization and Analysis of Mapped Sequences. Bioinformatics 2014, 1-8.
23. Hiraga S., Yanofsky C. Inhibition of the progress of transcription on the tryptophan operon of Escherichia coli. J. Mol. Biol. 1973, 79:339-349.
24. Ignatov D., Malakho S., Majorov K., Skvortsov T., Apt A., Azhikina T. RNA-Seq analysis of Mycobacterium avium non-coding transcriptome. PLoS One 2013, 8:e74209.
25. Ikeda M., Nakagawa S. The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl. Microbiol. Biotechnol. 2003, 62:99-109.
26. Jung S., Chun J., Yim S., Lee S., Cheon C., Song E., Lee M. Transcriptional regulation of histidine biosynthesis genes in Corynebacterium glutamicum. Canadian J. of Microbio. 2010, 187:178-187.
27. Kaberdina A.C., Szaflarski W., Nierhaus K.H., Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?. Mol. Cell. 2010, 33:227-236.
28. Kalinowski J., Bathe B., Bartels D., Bischoff N., Bott M., Burkovski A., Dusch N., Eggeling L., Eikmanns B.J., Gaigalat L., Goesmann A., Hartmann M., Huthmacher K., Krämer R., Linke B., McHardy A.C., Meyer F., Möckel B., Pfefferle W., Pühler A., Rey D.A., Rückert C., Rupp O., Sahm H., Wendisch V.F., Wiegräbe I., Tauch A. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of l-aspartate-derived amino acids and vitamins. J. Biotechnol. 2003, 104:5-25.
29. Katsumata R., Ikeda M. Hyperproduction of tryptophan in Corynebacterium glutamicum by pathway engineering. Nat. Biotechnol. 1993, 11:921-925.
30. Keilhauer C., Eggeling L., Sahm H. Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon. J. Bacteriol. 1993, 175:5595-5603.
31. Kingsford C.L., Ayanbule K., Salzberg S.L. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol. 2007, 8:R22.
32. Kolter R., Yanofsky C. Attenuation in amino acid biosynthetic operons. Annu. Rev. Genet. 1982, 16:113-134.
33. Lalaouna D., Simoneau-Roy M., Lafontaine D., Massé E. Regulatory RNAs and target mRNA decay in prokaryotes. Biochim. Biophys. Acta 2013, 1829:742-747.
34. Lin Y., David Romero A., Guan S., Mamanova L., McDowall K.J. A combination of improved differential and global RNA-seq reveals pervasive transcription initiation and events in all stages of the life-cycle of functional RNAs in Propionibacterium acnes, a major contributor to wide-spread human disease. BMC Genomics 2013, 14:620.
35. Liu Y.-J., Li P.-P., Zhao K.-X., Wang B.-J., Jiang C.-Y., Drake H.L., Liu S.-J. Corynebacterium glutamicum contains 3-deoxy-d-arabino-heptulosonate 7-phosphate synthases that display novel biochemical features. Appl. Environ. Microbiol. 2008, 74:5497-5503.
36. ® of Systematic Bacteriology Volume Five The Actinobacteria, Part A 2012, 1-28. Springer, New York, Dordrecht, Heidelberg, London. M. Goodfellow, P. Kämpfer, H.-J. Busse, M.E. Trujillo, K. Suzuki, W. Ludwig, W.B. Whitman (Eds.).
37. Matsui K., Sano K., Ohtsubo E. Sequence analysis of the Brevibacterium lactofermentum trp operon. Mol. Gen. Genet. MGG 1987, 209:299-305.
38. Mentz A., Neshat A., Pfeifer-Sancar K., Pühler A. Comprehensive discovery and characterization of small RNAs in Corynebacterium glutamicum ATCC 13032. BMC Genomics 2013, 14:714.
39. Moll I., Grill S., Gualerzi C.O., Bläsi U. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol. Microbiol. 2002, 43:239-246.
40. Moll I., Hirokawa G., Kiel M.C., Kaji A., Bläsi U. Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs. Nucleic Acids Res. 2004, 32:3354-3363.
41. Morbach S., Junger C., Sahm H., Eggeling L. Attenuation control of ilvBNC in Corynebacterium glutamicum: evidence of leader peptide formation without the presence of a ribosome binding site. J. Biosci. Bioeng. 2000, 90:501-507.
42. Mormann S., Lömker A., Rückert C., Gaigalat L., Tauch A., Pühler A., Kalinowski J. Random mutagenesis in Corynebacterium glutamicum ATCC 13032 using an IS6100-based transposon vector identified the last unknown gene in the histidine biosynthesis pathway. BMC Genomics 2006, 7:205.
43. Naville M., Gautheret D. Transcription attenuation in bacteria: theme and variations. Brief. Funct. Genomics Proteomics 2009, 8:482-492.
44. Naville M., Gautheret D. Premature terminator analysis sheds light on a hidden world of bacterial transcriptional attenuation. Genome Biol. 2010, 11:R97.
45. Neal R.J., Chater K.F. Bidirectional promoter and terminator regions bracket mmr, a resistance gene embedded in the Streptomyces coelicolor A3(2) gene cluster encoding methylenomycin production. Gene 1991, 100:75-83.
46. O'Gara J., Dunican L. Direct evidence for a constitutive internal promoter in the tryptophan operon of Corynebacterium glutamicum. Biochem. Biophys. Res. Commun. 1994, 203:820-827.
47. Pátek M. Regulation of gene expression. Handbook of Corynebacterium glutamicum 2005, 81-98. CRC Press, Boca Raton, FL, USA. L. Eggeling, M. Bott (Eds.).
48. Pátek M. Branched-chain amino acids. Amino Acid Biosynthesis-Pathways, Regulation and Metabolic Engineering 2007, 130-155. Springer-Verlag, Berlin, Heidelberg. V.F. Wendisch (Ed.).
49. Pátek M., Krumbach K., Eggeling L., Sahm H. Leucine synthesis in Corynebacterium glutamicum: enzyme activities, structure of leuA, and effect of leuA inactivation on lysine synthesis. Appl. Environ. Microbiol. 1994, 60:133-140.
50. Pauling J., Röttger R., Tauch A., Azevedo V., Baumbach J. CoryneRegNet 6.0-updated database content, new analysis methods and novel features focusing on community demands. Nucleic Acids Res. 2012, 40:D610-D614.
51. Perkins T.T., Kingsley R.A., Fookes M.C., Gardner P.P., James K.D., Yu L., Assefa S.A., He M., Croucher N.J., Pickard D.J., Maskell D.J., Parkhill J., Choudhary J., Thomson N.R., Dougan G. A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet. 2009, 5:e1000569.
52. Pfeifer-Sancar K., Mentz A., Rückert C., Kalinowski J. Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique. BMC Genomics 2013, 14:888.
53. Sano K., Matsui K. Structure and function of the trp operon control regions of Brevibacterium lactofermentum, a glutamic-acid-producing bacterium. Gene 1987, 53:191-200.
54. Schwientek P., Neshat A., Kalinowski J., Klein A., Rückert C., Schneiker-Bekel S., Wendler S., Stoye J., Pühler A. Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts. J. Biotechnol. 2014, S0168-S1656:116-123.
55. Seliverstov A.V., Putzer H., Gelfand M.S., Lyubetsky V.A. Comparative analysis of RNA regulatory elements of amino acid metabolism genes in Actinobacteria. BMC Microbiol. 2005, 5:1-14.
56. Sharma C., Hoffmann S., Darfeuille F., Reignier J., Findeiss S., Sittka A., Chabas S., Reiche K., Hackermüller J., Reinhardt R., Stadler P.F., Vogel J. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464:250-255.
57. Sorek R., Cossart P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat. Rev. Genet. 2010, 11:9-16.
58. Sprenger G. Aromatic amino acids. Amino Acid Biosynthesis-Pathways, Regulation and Metabolic Engineering 2007, 93-127. Springer-Verlag, Berlin Heidelberg. V.F. Wendisch (Ed.).
59. Steffek M., Newton G.L., Av-Gay Y., Fahey R.C. Characterization of Mycobacterium tuberculosis mycothiol S-conjugate amidase. Biochemistry 2003, 42:12067-12076.
60. Steffen P., Voss B., Rehmsmeier M., Reeder J., Giegerich R. RNAshapes: an integrated RNA analysis package based on abstract shapes. Bioinformatics 2006, 22:500-503.
61. Storz G., Vogel J., Wassarman K. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell. 2011, 43:880-891.
62. Tichopad A., Dzidic A., Pfaffl M. Improving quantitative real-time RT-PCR reproducibility by boosting primer-linked amplification efficiency. Biotechnol. Lett. 2002, 2053-2056.
63. Udagawa T., Shimizu Y., Ueda T. Evidence for the translation initiation of leaderless mRNAs by the intact 70 S ribosome without its dissociation into subunits in eubacteria. J. Biol. Chem. 2004, 279:8539-8546.
64. Umbarger H. Amino acid biosynthesis and its regulation. Annu. Rev. Biochem. 1978, 47:533-606.
65. Umbarger H. Biosynthesis of the branched-chain amino acids. Escherichia Coli and Salmonella: Cellular and Molecular Biology 1996, 442-457. ASM Press, Washington, D.C. F.C. Neidhardt, R. Curtiss, J.L. Ingraham, E.C.C. Lin, K.B. Low, B. Magasanik, W.S. Reznikoff, M. Riley, M. Schaechter, H.E. Umbarger (Eds.).
66. Unniraman S., Prakash R., Nagaraja V. Conserved economics of transcription termination in eubacteria. Nucleic Acids Res. 2002, 30:675-684.
67. Uyar B., Chu J.S.C., Vergara I.A., Chua S.Y., Jones M.R., Wong T., Baillie D.L., Chen N. RNA-seq analysis of the C. briggsae transcriptome. Genome Res. 2012, 22:1567-1580.
68. Vesper O., Amitai S., Belitsky M., Byrgazov K., Kaberdina A.C., Engelberg-Kulka H., Moll I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011, 147:147-157.
69. Vitreschak A.G., Lyubetskaya E.V., Shirshin M.A., Gelfand M.S., Lyubetsky V.A. Attenuation regulation of amino acid biosynthetic operons in proteobacteria: comparative genomics analysis. FEMS Microbiol. Lett. 2004, 234:357-370.
70. Vitreschak A.G., Mironov A.A., Lyubetsky V.A., Gelfand M.S. Comparative genomic analysis of T-box regulatory systems in bacteria. RNA 2008, 14:717-735.
71. Walsh C.T., Benson T.E., Kim D.H., Lees W.J. The versatility of phosphoenolpyruvate and its vinyl ether products in biosynthesis. Chem. Biol. 1996, 3:83-91.
72. Wek R.C., Hauser C.A., Hatfield G.W. The nucleotide sequence of the ilvBN operon of Escherichia coli: sequence homologies of the acetohydroxy acid synthase isozymes. Nucleic Acids Res. 1985, 13:3995-4010.
73. Westermann A.J., Gorski S.A., Vogel J. Dual RNA-seq of pathogen and host. Nat. Rev. Microbiol. 2012, 10:618-630.
74. Wilms I., Overlöper A., Nowrousian M., Sharma C.M., Narberhaus F. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol. 2012, 9:446-457.
75. Wu J., Sheflyan G.Y., Woodard R.W. Bacillus subtilis 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase revisited: resolution of two long-standing enigmas. Biochem. J. 2005, 390:583-590.
76. Xie G., Keyhani O.N., Bonner A.C., Jensen A.R. Ancient origin of the tryptophan operon and the dynamics of evolutionary change. Microbiol. Mol. Biol. Rev. 2003, 67:303-342.
77. Yanofsky C. Attenuation in the control of expression of bacterial operons. Nature 1981, 289:751-758.
78. Zheng X., Hu G.-Q., She Z.-S., Zhu H. Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes. BMC Genomics 2011, 12:361.