Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media

Schwientek P, Wendler S, Neshat A, Eirich C, Rückert C, Klein A, Wehmeier UF, Kalinowski J, Stoye J, Pühler A (2013)
Journal of Biotechnology 167(2): 166-177.

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Autor*in
Schwientek, PatrickUniBi; Wendler, SergejUniBi; Neshat, ArminUniBi; Eirich, Christina; Rückert, ChristianUniBi ; Klein, Andreas; Wehmeier, Udo F; Kalinowski, JörnUniBi; Stoye, JensUniBi ; Pühler, AlfredUniBi
Einrichtung
Centrum für Biotechnologie > Institut für Bioinformatik
Centrum für Biotechnologie > Institut für Genomforschung und Systembiologie
Technische Fakultät > AG Genominformatik
Centrum für Biotechnologie > Arbeitsgruppe A. Pühler
Centrum für Biotechnologie > Arbeitsgruppe J. Stoye
Centrum für Biotechnologie > Arbeitsgruppe J. Kalinowski
Centrum für Biotechnologie > Graduate Center > Graduate Cluster Industrial Biotechnology
Abstract / Bemerkung
Actinoplanes sp. SE50/110 is known as the producer of the alpha-glucosidase inhibitor acarbose, a potent drug in the treatment of type-2 diabetes mellitus. We conducted the first whole transcriptome analysis of Actinoplanes sp. SE50/110, using RNA-sequencing technology for comparative gene expression studies between cells grown in maltose minimal medium, maltose minimal medium with trace elements, and glucose complex medium. We first studied the behavior of Actinoplanes sp. SE50/110 cultivations in these three media and found that the different media had significant impact on growth rate and in particular on acarbose production. It was demonstrated that Actinoplanes sp. SE50/110 grew well in all three media, but acarbose biosynthesis was only observed in cultures grown in maltose minimal medium with and without trace elements. When comparing the expression profiles between the maltose minimal media with and without trace elements, only few significantly differentially expressed genes were found, which mainly code for uptake systems of metal ions provided in the trace element solution. In contrast, the comparison of expression profiles from maltose minimal medium and glucose complex medium revealed a large number of differentially expressed genes, of which the most conspicuous genes account for iron storage and uptake. Furthermore, the acarbose gene cluster was found to be highly expressed in maltose-containing media and almost silent in the glucose-containing medium. In addition, a putative antibiotic biosynthesis gene cluster was found to be similarly expressed as the acarbose cluster.
Erscheinungsjahr
2013
Zeitschriftentitel
Journal of Biotechnology
Band
167
Ausgabe
2
Seite(n)
166-177
ISSN
0168-1656
Page URI
https://pub.uni-bielefeld.de/record/2548236

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Schwientek P, Wendler S, Neshat A, et al. Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media. Journal of Biotechnology. 2013;167(2):166-177.
Schwientek, P., Wendler, S., Neshat, A., Eirich, C., Rückert, C., Klein, A., Wehmeier, U. F., et al. (2013). Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media. Journal of Biotechnology, 167(2), 166-177. doi:10.1016/j.jbiotec.2012.10.019
Schwientek, Patrick, Wendler, Sergej, Neshat, Armin, Eirich, Christina, Rückert, Christian, Klein, Andreas, Wehmeier, Udo F, Kalinowski, Jörn, Stoye, Jens, and Pühler, Alfred. 2013. “Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media”. Journal of Biotechnology 167 (2): 166-177.
Schwientek, P., Wendler, S., Neshat, A., Eirich, C., Rückert, C., Klein, A., Wehmeier, U. F., Kalinowski, J., Stoye, J., and Pühler, A. (2013). Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media. Journal of Biotechnology 167, 166-177.
Schwientek, P., et al., 2013. Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media. Journal of Biotechnology, 167(2), p 166-177.
P. Schwientek, et al., “Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media”, Journal of Biotechnology, vol. 167, 2013, pp. 166-177.
Schwientek, P., Wendler, S., Neshat, A., Eirich, C., Rückert, C., Klein, A., Wehmeier, U.F., Kalinowski, J., Stoye, J., Pühler, A.: Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media. Journal of Biotechnology. 167, 166-177 (2013).
Schwientek, Patrick, Wendler, Sergej, Neshat, Armin, Eirich, Christina, Rückert, Christian, Klein, Andreas, Wehmeier, Udo F, Kalinowski, Jörn, Stoye, Jens, and Pühler, Alfred. “Comparative RNA-sequencing of the acarbose producer Actinoplanes sp. SE50/110 cultivated in different growth media”. Journal of Biotechnology 167.2 (2013): 166-177.

10 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Comparative functional genomics of the acarbose producers reveals potential targets for metabolic engineering.
Xie H, Zhao Q, Zhang X, Kang Q, Bai L., Synth Syst Biotechnol 4(1), 2019
PMID: 30723817
Evaluation of vector systems and promoters for overexpression of the acarbose biosynthesis gene acbC in Actinoplanes sp. SE50/110.
Schaffert L, März C, Burkhardt L, Droste J, Brandt D, Busche T, Rosen W, Schneiker-Bekel S, Persicke M, Pühler A, Kalinowski J., Microb Cell Fact 18(1), 2019
PMID: 31253141
Optimization of critical medium components for enhancing antibacterial thiopeptide nocathiacin I production with significantly improved quality.
Yang MY, Zhang JW, Wu XR, Chen YJ., Chin J Nat Med 15(4), 2017
PMID: 28527515
Improving acarbose production and eliminating the by-product component C with an efficient genetic manipulation system of Actinoplanes sp. SE50/110.
Zhao Q, Xie H, Peng Y, Wang X, Bai L., Synth Syst Biotechnol 2(4), 2017
PMID: 29552655
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
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
Reconstruction and in silico analysis of an Actinoplanes sp. SE50/110 genome-scale metabolic model for acarbose production.
Wang Y, Xu N, Ye C, Liu L, Shi Z, Wu J., Front Microbiol 6(), 2015
PMID: 26161077
Identification of Oxygen-Responsive Transcripts in the Silage Inoculant Lactobacillus buchneri CD034 by RNA Sequencing.
Eikmeyer FG, Heinl S, Marx H, Pühler A, Grabherr R, Schlüter A., PLoS One 10(7), 2015
PMID: 26230316
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., J Biotechnol 190(), 2014
PMID: 24642337
Carbon source dependent biosynthesis of acarviose metabolites in Actinoplanes sp. SE50/110.
Wendler S, Ortseifen V, Persicke M, Klein A, Neshat A, Niehaus K, Schneiker-Bekel S, Walter F, Wehmeier UF, Kalinowski J, Pühler A., J Biotechnol 191(), 2014
PMID: 25169663

59 References

Daten bereitgestellt von Europe PubMed Central.

Differential expression analysis for sequence count data.
Anders S, Huber W., Genome Biol. 11(10), 2010
PMID: 20979621
An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11.
Bearden SW, Staggs TM, Perry RD., J. Bacteriol. 180(5), 1998
PMID: 9495751
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
A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2).
Brekasis D, Paget MS., EMBO J. 22(18), 2003
PMID: 12970197
Characterization of maltose and maltotriose transport in the acarbose-producing bacterium Actinoplanes sp.
Brunkhorst C, Schneider E., Res. Microbiol. 156(8), 2005
PMID: 15939574
EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7.
Cao J, Woodhall MR, Alvarez J, Cartron ML, Andrews SC., Mol. Microbiol. 65(4), 2007
PMID: 17627767
Ferritins, iron uptake and storage from the bacterioferritin viewpoint.
Carrondo MA., EMBO J. 22(9), 2003
PMID: 12727864
The Stigmatella aurantiaca homolog of Myxococcus xanthus high-mobility-group A-type transcription factor CarD: insights into the functional modules of CarD and their distribution in bacteria.
Cayuela ML, Elias-Arnanz M, Penalver-Mellado M, Padmanabhan S, Murillo FJ., J. Bacteriol. 185(12), 2003
PMID: 12775690
Revealing the missing expressed genes beyond the human reference genome by RNA-Seq.
Chen G, Li R, Shi L, Qi J, Hu P, Luo J, Liu M, Shi T., BMC Genomics 12(), 2011
PMID: 22133125
Stem cell transcriptome profiling via massive-scale mRNA sequencing.
Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, Robertson AJ, Perkins AC, Bruce SJ, Lee CC, Ranade SS, Peckham HE, Manning JM, McKernan KJ, Grimmond SM., Nat. Methods 5(7), 2008
PMID: 18516046
Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica.
Das A, Silaghi-Dumitrescu R, Ljungdahl LG, Kurtz DM Jr., J. Bacteriol. 187(6), 2005
PMID: 15743950
The iron/lead transporter superfamily of Fe/Pb2+ uptake systems.
Debut AJ, Dumay QC, Barabote RD, Saier MH Jr., J. Mol. Microbiol. Biotechnol. 11(1-2), 2006
PMID: 16825785
Transcriptional profiling of Actinobacillus pleuropneumoniae under iron-restricted conditions.
Deslandes V, Nash JH, Harel J, Coulton JW, Jacques M., BMC Genomics 8(), 2007
PMID: 17355629
The regulatory action of the myxobacterial CarD/CarG complex: a bacterial enhanceosome?
Elias-Arnanz M, Padmanabhan S, Murillo FJ., FEMS Microbiol. Rev. 34(5), 2010
PMID: 20561058
Opening the iron box: transcriptional metalloregulation by the Fur protein.
Escolar L, Perez-Martin J, de Lorenzo V., J. Bacteriol. 181(20), 1999
PMID: 10515908
Exploring the gonad transcriptome of two extreme male pigs with RNA-seq.
Esteve-Codina A, Kofler R, Palmieri N, Bussotti G, Notredame C, Perez-Enciso M., BMC Genomics 12(), 2011
PMID: 22067327
On the transcriptional regulation of methicillin resistance: MecI repressor in complex with its operator.
Garcia-Castellanos R, Mallorqui-Fernandez G, Marrero A, Potempa J, Coll M, Gomis-Ruth FX., J. Biol. Chem. 279(17), 2004
PMID: 14960592
A [2Fe-2S] protein encoded by an open reading frame upstream of the Escherichia coli bacterioferritin gene.
Garg RP, Vargo CJ, Cui X, Kurtz DM Jr., Biochemistry 35(20), 1996
PMID: 8639572
Global analysis of protein expression in yeast.
Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS., Nature 425(6959), 2003
PMID: 14562106
Micros for microbes: non-coding regulatory RNAs in bacteria.
Gottesman S., Trends Genet. 21(7), 2005
PMID: 15913835
An analysis of the binding of repressor protein ModE to modABCD (molybdate transport) operator/promoter DNA of Escherichia coli.
Grunden AM, Self WT, Villain M, Blalock JE, Shanmugam KT., J. Biol. Chem. 274(34), 1999
PMID: 10446207
Transcriptome complexity in a genome-reduced bacterium.
Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, Michalodimitrakis K, Yamada T, Arumugam M, Doerks T, Kuhner S, Rode M, Suyama M, Schmidt S, Gavin AC, Bork P, Serrano L., Science 326(5957), 2009
PMID: 19965477
Developmentally regulated cleavage of tRNAs in the bacterium Streptomyces coelicolor.
Haiser HJ, Karginov FV, Hannon GJ, Elliot MA., Nucleic Acids Res. 36(3), 2007
PMID: 18084030

IDF, 2011
Optimization of culture conditions and scale-up to plant scales for teicoplanin production by Actinoplanes teichomyceticus.
Jung HM, Kim SY, Prabhu P, Moon HJ, Kim IW, Lee JK., Appl. Microbiol. Biotechnol. 80(1), 2008
PMID: 18542948
Immunological investigation of the distribution of cytochromes related to the two terminal oxidases of Escherichia coli in other gram-negative bacteria.
Kranz RG, Gennis RB., J. Bacteriol. 161(2), 1985
PMID: 2981822
Characterization and improvement of RNA-Seq precision in quantitative transcript expression profiling.
Labaj PP, Leparc GG, Linggi BE, Markillie LM, Wiley HS, Kreil DP., Bioinformatics 27(13), 2011
PMID: 21685096
Biosynthetic studies on the alpha-glucosidase inhibitor acarbose in Actinoplanes sp.: source of the maltose unit.
Lee S, Sauerbrei B, Niggemann J, Egelkrout E., J. Antibiot. 50(11), 1997
PMID: 9592570
Crystal structures of the bacterial solute receptor AcbH displaying an exclusive substrate preference for β-D-galactopyranose.
Licht A, Bulut H, Scheffel F, Daumke O, Wehmeier UF, Saenger W, Schneider E, Vahedi-Faridi A., J. Mol. Biol. 406(1), 2010
PMID: 21168419
Highly integrated single-base resolution maps of the epigenome in Arabidopsis.
Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR., Cell 133(3), 2008
PMID: 18423832
The Enterococcus hirae paradigm of copper homeostasis: copper chaperone turnover, interactions, and transactions.
Lu ZH, Dameron CT, Solioz M., Biometals 16(1), 2003
PMID: 12572673
Copper chaperone cycling and degradation in the regulation of the cop operon of Enterococcus hirae.
Magnani D, Solioz M., Biometals 18(4), 2005
PMID: 16158233
CDD: a Conserved Domain Database for the functional annotation of proteins.
Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH., Nucleic Acids Res. 39(Database issue), 2010
PMID: 21109532
The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44.
Massa AN, Childs KL, Lin H, Bryan GJ, Giuliano G, Buell CR., PLoS ONE 6(10), 2011
PMID: 22046362
Regulatory roles for small RNAs in bacteria.
Masse E, Majdalani N, Gottesman S., Curr. Opin. Microbiol. 6(2), 2003
PMID: 12732300
Cytochromes of archaeal electron transfer chains
Mathias, Biochimica et Biophysica Acta (BBA): Bioenergetics 1229(), 1995
Genetic analysis of the modABCD (molybdate transport) operon of Escherichia coli.
Maupin-Furlow JA, Rosentel JK, Lee JH, Deppenmeier U, Gunsalus RP, Shanmugam KT., J. Bacteriol. 177(17), 1995
PMID: 7665460
Nucleotide sequences of streptomycete 16S ribosomal DNA: towards a specific identification system for streptomycetes using PCR.
Mehling A, Wehmeier UF, Piepersberg W., Microbiology (Reading, Engl.) 141 ( Pt 9)(), 1995
PMID: 7496525
Mapping and quantifying mammalian transcriptomes by RNA-Seq.
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B., Nat. Methods 5(7), 2008
PMID: 18516045
Complete genome sequence of Stackebrandtia nassauensis type strain (LLR-40K-21T)
Munk, Standards in Genomic Sciences 1(), 2009
The transcriptional landscape of the yeast genome defined by RNA sequencing.
Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M., Science 320(5881), 2008
PMID: 18451266
Role of the Fur regulon in iron transport in Bacillus subtilis.
Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD., J. Bacteriol. 188(10), 2006
PMID: 16672620
RNA sequencing: advances, challenges and opportunities.
Ozsolak F, Milos PM., Nat. Rev. Genet. 12(2), 2010
PMID: 21191423
Domain architecture of a high mobility group A-type bacterial transcriptional factor.
Padmanabhan S, Elias-Arnanz M, Carpio E, Aparicio P, Murillo FJ., J. Biol. Chem. 276(45), 2001
PMID: 11533063
Spectroscopic and voltammetric characterisation of the bacterioferritin-associated ferredoxin of Escherichia coli.
Quail MA, Jordan P, Grogan JM, Butt JN, Lutz M, Thomson AJ, Andrews SC, Guest JR., Biochem. Biophys. Res. Commun. 229(2), 1996
PMID: 8954950
EfeO-cupredoxins: major new members of the cupredoxin superfamily with roles in bacterial iron transport.
Rajasekaran MB, Nilapwar S, Andrews SC, Watson KA., Biometals 23(1), 2009
PMID: 19701722

AUTHOR UNKNOWN, 0
The gac-gene cluster for the production of acarbose from Streptomyces glaucescens GLA.O: identification, isolation and characterization.
Rockser Y, Wehmeier UF., J. Biotechnol. 140(1-2), 2008
PMID: 19059289
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
The primary transcriptome of the major human pathogen Helicobacter pylori.
Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermuller J, Reinhardt R, Stadler PF, Vogel J., Nature 464(7286), 2010
PMID: 20164839
Optimization of media composition and culture conditions for acarbose production by Actinoplanes utahensis ZJB-08196
Wang, World Journal of Microbiology and Biotechnology 27(), 2011
RNA-Seq: a revolutionary tool for transcriptomics.
Wang Z, Gerstein M, Snyder M., Nat. Rev. Genet. 10(1), 2009
PMID: 19015660
The Biosynthesis and Metabolism of Acarbose in Actinoplanes sp. SE 50/110: A Progress Report
Wehmeier, Biocatalysis and Biotransformation 21(), 2003
Biotechnology and molecular biology of the alpha-glucosidase inhibitor acarbose.
Wehmeier UF, Piepersberg W., Appl. Microbiol. Biotechnol. 63(6), 2003
PMID: 14669056
The cytosolic and extracellular proteomes of Actinoplanes sp. SE50/110 led to the identification of gene products involved in acarbose metabolism
Wendler, Journal of Biotechnology (), 1998
Cytochrome bd biosynthesis in Bacillus subtilis: characterization of the cydABCD operon.
Winstedt L, Yoshida K, Fujita Y, von Wachenfeldt C., J. Bacteriol. 180(24), 1998
PMID: 9852001
A single-base resolution map of an archaeal transcriptome.
Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R., Genome Res. 20(1), 2009
PMID: 19884261
RNA-Seq of the xylose-fermenting yeast Scheffersomyces stipitis cultivated in glucose or xylose.
Yuan T, Ren Y, Meng K, Feng Y, Yang P, Wang S, Shi P, Wang L, Xie D, Yao B., Appl. Microbiol. Biotechnol. 92(6), 2011
PMID: 22086068
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