Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts

Schwientek P, Neshat A, Kalinowski J, Klein A, Rückert C, Schneiker-Bekel S, Wendler S, Stoye J, Pühler A (2014)
Journal of Biotechnology 190: 85-95.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
: Actinoplanes sp. SE50/110 is the producer of the alpha-glucosidase inhibitor acarbose, which is an economically relevant and potent drug in the treatment of type-2 diabetes mellitus. In this study, we present the detection of transcription start sites on this genome by sequencing enriched 5'-ends of primary transcripts. Altogether, 1,427 putative transcription start sites were initially identified. With help of the annotated genome sequence, 661 transcription start sites were found to belong to the leader region of protein-coding genes with the surprising result that roughly 20% of these genes rank among the class of leaderless transcripts. Next, conserved promoter motifs were identified for protein-coding genes with and without leader sequences. The mapped transcription start sites were finally used to improve the annotation of the Actinoplanes sp. SE50/110 genome sequence. Concerning protein-coding genes, 41 translation start sites were corrected and 9 novel protein-coding genes could be identified. In addition to this, 122 previously undetermined non-coding RNA (ncRNA) genes of Actinoplanes sp. SE50/110 were defined. Focusing on antisense transcription start sites located within coding genes or their leader sequences, it was discovered that 96 of those ncRNA genes belong to the class of antisense RNA (asRNA) genes. The remaining 26 ncRNA genes were found outside of known protein-coding genes. Four chosen examples of prominent ncRNA genes, namely the transfer messenger RNA gene ssrA, the ribonuclease P class A RNA gene rnpB, the cobalamin riboswitch RNA gene cobRS, and the selenocysteine-specific tRNA gene selC, are presented in more detail. This study demonstrates that sequencing of enriched 5'-ends of primary transcripts and the identification of transcription start sites are valuable tools for advanced genome annotation of Actinoplanes sp. SE50/110 and most probably also for other bacteria.
Erscheinungsjahr
Zeitschriftentitel
Journal of Biotechnology
Band
190
Seite(n)
85-95
ISSN
PUB-ID

Zitieren

Schwientek P, Neshat A, Kalinowski J, et al. Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts. Journal of Biotechnology. 2014;190:85-95.
Schwientek, P., Neshat, A., Kalinowski, J., Klein, A., Rückert, C., Schneiker-Bekel, S., Wendler, S., et al. (2014). Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts. Journal of Biotechnology, 190, 85-95. doi:10.1016/j.jbiotec.2014.03.013
Schwientek, P., Neshat, A., Kalinowski, J., Klein, A., Rückert, C., Schneiker-Bekel, S., Wendler, S., Stoye, J., and Pühler, A. (2014). Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts. Journal of Biotechnology 190, 85-95.
Schwientek, P., et al., 2014. Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts. Journal of Biotechnology, 190, p 85-95.
P. Schwientek, et al., “Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts”, Journal of Biotechnology, vol. 190, 2014, pp. 85-95.
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. Journal of Biotechnology. 190, 85-95 (2014).
Schwientek, Patrick, Neshat, Armin, Kalinowski, Jörn, Klein, Andreas, Rückert, Christian, Schneiker-Bekel, Susanne, Wendler, Sergej, Stoye, Jens, and Pühler, Alfred. “Improving the genome annotation of the acarbose producer Actinoplanes sp. SE50/110 by sequencing enriched 5'-ends of primary transcripts”. Journal of Biotechnology 190 (2014): 85-95.

7 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Genome improvement of the acarbose producer Actinoplanes sp. SE50/110 and annotation refinement based on RNA-seq analysis.
Wolf T, Schneiker-Bekel S, Neshat A, Ortseifen V, Wibberg D, Zemke T, Pühler A, Kalinowski J., J Biotechnol 251(), 2017
PMID: 28427920
Comparative proteome analysis of Actinoplanes sp. SE50/110 grown with maltose or glucose shows minor differences for acarbose biosynthesis proteins but major differences for saccharide transporters.
Wendler S, Otto A, Ortseifen V, Bonn F, Neshat A, Schneiker-Bekel S, Wolf T, Zemke T, Wehmeier UF, Hecker M, Kalinowski J, Becher D, Pühler A., J Proteomics 131(), 2016
PMID: 26597626
Complete genome sequence of Streptomyces lividans TK24.
Rückert C, Albersmeier A, Busche T, Jaenicke S, Winkler A, Friðjónsson ÓH, Hreggviðsson GÓ, Lambert C, Badcock D, Bernaerts K, Anne J, Economou A, Kalinowski J., J Biotechnol 199(), 2015
PMID: 25680930
Comprehensive proteome analysis of Actinoplanes sp. SE50/110 highlighting the location of proteins encoded by the acarbose and the pyochelin biosynthesis gene cluster.
Wendler S, Otto A, Ortseifen V, Bonn F, Neshat A, Schneiker-Bekel S, Walter F, Wolf T, Zemke T, Wehmeier UF, Hecker M, Kalinowski J, Becher D, Pühler A., J Proteomics 125(), 2015
PMID: 25896738

62 References

Daten bereitgestellt von Europe PubMed Central.

Exact and complete short-read alignment to microbial genomes using Graphics Processing Unit programming.
Blom J, Jakobi T, Doppmeier D, Jaenicke S, Kalinowski J, Stoye J, Goesmann A., Bioinformatics 27(10), 2011
PMID: 21450712
Coenzyme B12 controls transcription of the Streptomyces class Ia ribonucleotide reductase nrdABS operon via a riboswitch mechanism.
Borovok I, Gorovitz B, Schreiber R, Aharonowitz Y, Cohen G., J. Bacteriol. 188(7), 2006
PMID: 16547038
Alternative oxygen-dependent and oxygen-independent ribonucleotide reductases in Streptomyces: cross-regulation and physiological role in response to oxygen limitation.
Borovok I, Gorovitz B, Yanku M, Schreiber R, Gust B, Chater K, Aharonowitz Y, Cohen G., Mol. Microbiol. 54(4), 2004
PMID: 15522084
Bounded search for de novo identification of degenerate cis-regulatory elements.
Carlson JM, Chakravarty A, Khetani RS, Gross RH., BMC Bioinformatics 7(), 2006
PMID: 16700920
WebLogo: a sequence logo generator.
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120
Rfam: updates to the RNA families database.
Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, Bateman A., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18953034
RNase P: variations and uses.
Gopalan V, Vioque A, Altman S., J. Biol. Chem. 277(9), 2001
PMID: 11741968
Rfam: annotating non-coding RNAs in complete genomes
Griffiths-Jones, Nucleic Acids Res. 33(), 2004
Bacterial transcriptomics: what is beyond the RNA horiz-ome?
Guell M, Yus E, Lluch-Senar M, Serrano L., Nat. Rev. Microbiol. 9(9), 2011
PMID: 21836626
A selDABC cluster for selenocysteine incorporation in Eubacterium acidaminophilum.
Gursinsky T, Jager J, Andreesen JR, Sohling B., Arch. Microbiol. 174(3), 2000
PMID: 11041351
The enigma of ribonuclease P evolution.
Hartmann E, Hartmann RK., Trends Genet. 19(10), 2003
PMID: 14550630
The making of tRNAs and more - RNase P and tRNase Z.
Hartmann RK, Gossringer M, Spath B, Fischer S, Marchfelder A., Prog Mol Biol Transl Sci 85(), 2009
PMID: 19215776
NONCODE v2.0: decoding the non-coding.
He S, Liu C, Skogerbo G, Zhao H, Wang J, Liu T, Bai B, Zhao Y, Chen R., Nucleic Acids Res. 36(Database issue), 2007
PMID: 18000000

Hilker, 2014
Prodigal: prokaryotic gene recognition and translation initiation site identification.
Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ., BMC Bioinformatics 11(), 2010
PMID: 20211023

IDF, 2013
Ribonucleotide reductases.
Jordan A, Reichard P., Annu. Rev. Biochem. 67(), 1998
PMID: 9759483
An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?
Kaberdina, Mol. Cell 33(), 2010
Biology of trans-translation.
Keiler KC., Annu. Rev. Microbiol. 62(), 2008
PMID: 18557701
fRNAdb: a platform for mining/annotating functional RNA candidates from non-coding RNA sequences.
Kin T, Yamada K, Terai G, Okida H, Yoshinari Y, Ono Y, Kojima A, Kimura Y, Komori T, Asai K., Nucleic Acids Res. 35(Database issue), 2006
PMID: 17099231
Improved base calling for the Illumina Genome Analyzer using machine learning strategies.
Kircher M, Stenzel U, Kelso J., Genome Biol. 10(8), 2009
PMID: 19682367
Horizontal gene transfer in prokaryotes: quantification and classification.
Koonin EV, Makarova KS, Aravind L., Annu. Rev. Microbiol. 55(), 2001
PMID: 11544372
The prokaryotic selenoproteome.
Kryukov GV, Gladyshev VN., EMBO Rep. 5(5), 2004
PMID: 15105824
NONCODE: an integrated knowledge database of non-coding RNAs
Liu, Nucleic Acids Res. 33(), 2004
Selenoproteins.
Lu J, Holmgren A., J. Biol. Chem. 284(2), 2008
PMID: 18757362
High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons
McGrath, Nat. Biotechnol. 25(May (5)), 2007
tmRNA determinants required for facilitating nonstop mRNA decay.
Mehta P, Richards J, Karzai AW., RNA 12(12), 2006
PMID: 17077272
Comprehensive discovery and characterization of small RNAs in Corynebacterium glutamicum ATCC 13032.
Mentz A, Neshat A, Pfeifer-Sancar K, Puhler A, Ruckert C, Kalinowski J., BMC Genomics 14(), 2013
PMID: 24138339
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
The Functional RNA Database 3.0: databases to support mining and annotation of functional RNAs.
Mituyama T, Yamada K, Hattori E, Okida H, Ono Y, Terai G, Yoshizawa A, Komori T, Asai K., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18948287
Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control.
Moll I, Grill S, Gualerzi CO, Blasi U., Mol. Microbiol. 43(1), 2002
PMID: 11849551
Translation initiation with 70S ribosomes: an alternative pathway for leaderless mRNAs.
Moll I, Hirokawa G, Kiel MC, Kaji A, Blasi U., Nucleic Acids Res. 32(11), 2004
PMID: 15215335
Genetic control by a metabolite binding mRNA.
Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR., Chem. Biol. 9(9), 2002
PMID: 12323379
RNA sequencing: advances, challenges and opportunities.
Ozsolak F, Milos PM., Nat. Rev. Genet. 12(2), 2010
PMID: 21191423
Structure and complexity of a bacterial transcriptome.
Passalacqua KD, Varadarajan A, Ondov BD, Okou DT, Zwick ME, Bergman NH., J. Bacteriol. 191(10), 2009
PMID: 19304856
Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique.
Pfeifer-Sancar K, Mentz A, Ruckert C, Kalinowski J., BMC Genomics 14(), 2013
PMID: 24341750
The complete genome sequence of the acarbose producer Actinoplanes sp. SE50/110.
Schwientek P, Szczepanowski R, Ruckert C, Kalinowski J, Klein A, Selber K, Wehmeier UF, Stoye J, Puhler A., BMC Genomics 13(), 2012
PMID: 22443545
Sequencing of high G+C microbial genomes using the ultrafast pyrosequencing technology.
Schwientek P, Szczepanowski R, Ruckert C, Stoye J, Puhler A., J. Biotechnol. 155(1), 2011
PMID: 21536083
Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media.
Schwientek P, Wendler S, Neshat A, Eirich C, Ruckert C, Klein A, Wehmeier UF, Kalinowski J, Stoye J, Puhler A., J. Biotechnol. 167(2), 2012
PMID: 23142701
Riboswitch detection using profile hidden Markov models.
Singh P, Bandyopadhyay P, Bhattacharya S, Krishnamachari A, Sengupta S., BMC Bioinformatics 10(), 2009
PMID: 19814811
Escherichia coli σ⁷⁰ senses sequence and conformation of the promoter spacer region.
Singh SS, Typas A, Hengge R, Grainger DC., Nucleic Acids Res. 39(12), 2011
PMID: 21398630
Bacterial antisense RNAs: how many are there, and what are they doing?
Thomason MK, Storz G., Annu. Rev. Genet. 44(), 2010
PMID: 20707673
Thousands of corresponding human and mouse genomic regions unalignable in primary sequence contain common RNA structure.
Torarinsson E, Sawera M, Havgaard JH, Fredholm M, Gorodkin J., Genome Res. 16(7), 2006
PMID: 16751343
Ribonucleotide reductases: divergent evolution of an ancient enzyme.
Torrents E, Aloy P, Gibert I, Rodriguez-Trelles F., J. Mol. Evol. 55(2), 2002
PMID: 12107591
Chemistry and biochemistry of microbial α-Glucosidase inhibitors
Truscheit, Angew. Chem. Int. Ed. Engl. 20(9), 1981
Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli.
Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina AC, Engelberg-Kulka H, Moll I., Cell 147(1), 2011
PMID: 21944167
Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element.
Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS., RNA 9(9), 2003
PMID: 12923257
RNA-Seq: a revolutionary tool for transcriptomics.
Wang Z, Gerstein M, Snyder M., Nat. Rev. Genet. 10(1), 2009
PMID: 19015660
The cytosolic and extracellular proteomes of Actinoplanes sp. SE50/110 led to the identification of gene products involved in acarbose metabolism.
Wendler S, Hurtgen D, Kalinowski J, Klein A, Niehaus K, Schulte F, Schwientek P, Wehlmann H, Wehmeier UF, Puhler A., J. Biotechnol. 167(2), 2012
PMID: 22944206
Dual RNA-seq of pathogen and host.
Westermann AJ, Gorski SA, Vogel J., Nat. Rev. Microbiol. 10(9), 2012
PMID: 22890146
The tmRNA Website.
Williams KP, Bartel DP., Nucleic Acids Res. 26(1), 1998
PMID: 9399824
Comparative transcriptomics of pathogenic and non-pathogenic Listeria species.
Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, Becavin C, Archambaud C, Cossart P, Sorek R., Mol. Syst. Biol. 8(), 2012
PMID: 22617957
Comparative sequence analysis of tmRNA.
Zwieb C, Wower I, Wower J., Nucleic Acids Res. 27(10), 1999
PMID: 10219077

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 24642337
PubMed | Europe PMC

Suchen in

Google Scholar