Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions

Rebets Y, Tsolis KC, Gudmundsdottir EE, Koepff J, Wawiernia B, Busche T, Bleidt A, Horbal L, Myronovskyi M, Ahmed Y, Wiechert W, et al. (2018)
FRONTIERS IN MICROBIOLOGY 9: 3033.

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Abstract / Bemerkung
Alternative sigma factors control numerous aspects of bacterial life, including adaptation to physiological stresses, morphological development, persistence states and virulence. This is especially true for the physiologically complex actinobacteria. Here we report the development of a robust gene deletions system for Streptomyces lividans TK24 based on a BAC library combined with the lambda-Red recombination technique. The developed system was validated by systematically deleting the most highly expressed genes encoding alternative sigma factors and several other regulatory genes within the chromosome of S. lividans TK24. To demonstrate the possibility of large scale genomic manipulations, the major part of the undecylprodigiosin gene cluster was deleted as well. The resulting mutant strains were characterized in terms of morphology, growth parameters, secondary metabolites production and response to thiol-oxidation and cell-wall stresses. Deletion of SLIV_12645 gene encoding S. coelicolor SigR1 ortholog has the most prominent phenotypic effect, resulted in overproduction of actinorhodin and coelichelin P1 and increased sensitivity to diamide. The secreted proteome analysis of SLIV_12645 mutant revealed SigR1 influence on trafficking of proteins involved in cell wall biogenesis and refactoring. The reported here gene deletion system will further facilitate work on S. lividans strain improvement as a host for either secondary metabolites or protein production and will contribute to basic research in streptomycetes physiology, morphological development, secondary metabolism. On the other hand, the systematic deletion of sigma factors encoding genes demonstrates the complexity and conservation of regulatory processes conducted by sigma factors in streptomycetes.
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FRONTIERS IN MICROBIOLOGY
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3033
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Rebets Y, Tsolis KC, Gudmundsdottir EE, et al. Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions. FRONTIERS IN MICROBIOLOGY. 2018;9: 3033.
Rebets, Y., Tsolis, K. C., Gudmundsdottir, E. E., Koepff, J., Wawiernia, B., Busche, T., Bleidt, A., et al. (2018). Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions. FRONTIERS IN MICROBIOLOGY, 9, 3033. doi:10.3389/fmicb.2018.03033
Rebets, Y., Tsolis, K. C., Gudmundsdottir, E. E., Koepff, J., Wawiernia, B., Busche, T., Bleidt, A., Horbal, L., Myronovskyi, M., Ahmed, Y., et al. (2018). Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions. FRONTIERS IN MICROBIOLOGY 9:3033.
Rebets, Y., et al., 2018. Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions. FRONTIERS IN MICROBIOLOGY, 9: 3033.
Y. Rebets, et al., “Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions”, FRONTIERS IN MICROBIOLOGY, vol. 9, 2018, : 3033.
Rebets, Y., Tsolis, K.C., Gudmundsdottir, E.E., Koepff, J., Wawiernia, B., Busche, T., Bleidt, A., Horbal, L., Myronovskyi, M., Ahmed, Y., Wiechert, W., Rueckert, C., Hamed, M.B., Bilyk, B., Anne, J., Fridjonsson, O., Kalinowski, J., Oldiges, M., Economou, A., Luzhetskyy, A.: Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions. FRONTIERS IN MICROBIOLOGY. 9, : 3033 (2018).
Rebets, Yuriy, Tsolis, Konstantinos C., Gudmundsdottir, Elisabet Eik, Koepff, Joachim, Wawiernia, Beata, Busche, Tobias, Bleidt, Arne, Horbal, Liliya, Myronovskyi, Maksym, Ahmed, Yousra, Wiechert, Wolfgang, Rueckert, Christian, Hamed, Mohamed B., Bilyk, Bohdan, Anne, Jozef, Fridjonsson, Olafur, Kalinowski, Joern, Oldiges, Marco, Economou, Anastassios, and Luzhetskyy, Andriy. “Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions”. FRONTIERS IN MICROBIOLOGY 9 (2018): 3033.

87 References

Daten bereitgestellt von Europe PubMed Central.

Protein Secretion in Gram-Positive Bacteria: From Multiple Pathways to Biotechnology.
Anne J, Economou A, Bernaerts K., Curr. Top. Microbiol. Immunol. 404(), 2017
PMID: 27885530
Controlling the false discovery rate - a practical and powerful approach to multiple testing.
Benjamini Y., Hochberg Y.., 1995
SCP1, a 356,023 bp linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2).
Bentley SD, Brown S, Murphy LD, Harris DE, Quail MA, Parkhill J, Barrell BG, McCormick JR, Santamaria RI, Losick R, Yamasaki M, Kinashi H, Chen CW, Chandra G, Jakimowicz D, Kieser HM, Kieser T, Chater KF., Mol. Microbiol. 51(6), 2004
PMID: 15009889
Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2).
Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA., Nature 417(6885), 2002
PMID: 12000953

Bruijn F.., 2016
Multi-Omics and Targeted Approaches to Determine the Role of Cellular Proteases in Streptomyces Protein Secretion.
Busche T, Tsolis KC, Koepff J, Rebets Y, Ruckert C, Hamed MB, Bleidt A, Wiechert W, Lopatniuk M, Yousra A, Anne J, Karamanou S, Oldiges M, Kalinowski J, Luzhetskyy A, Economou A., Front Microbiol 9(), 2018
PMID: 29915569
The developmental fate of S. coelicolor hyphae depends upon a gene product homologous with the motility sigma factor of B. subtilis.
Chater KF, Bruton CJ, Plaskitt KA, Buttner MJ, Mendez C, Helmann JD., Cell 59(1), 1989
PMID: 2507166
DNA Phosphorothioate Modification Plays a Role in Peroxides Resistance in Streptomyces lividans.
Dai D, Du A, Xiong K, Pu T, Zhou X, Deng Z, Liang J, He X, Wang Z., Front Microbiol 7(), 2016
PMID: 27630631
Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth.
den Hengst CD, Tran NT, Bibb MJ, Chandra G, Leskiw BK, Buttner MJ., Mol. Microbiol. 78(2), 2010
PMID: 20979333
Amino acid uptake profiling of wild type and recombinant Streptomyces lividans TK24 batch fermentations.
D'Huys PJ, Lule I, Van Hove S, Vercammen D, Wouters C, Bernaerts K, Anne J, Van Impe JF., J. Biotechnol. 152(4), 2010
PMID: 20797416
A transposon insertion single-gene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2).
Fernandez-Martinez LT, Del Sol R, Evans MC, Fielding S, Herron PR, Chandra G, Dyson PJ., Antonie Van Leeuwenhoek 99(3), 2010
PMID: 20945092
Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145.
Gomez-Escribano J., Song L., Fox D., Yeo V., Bibb M., Challis G.., 2012
Secreted-protein response to sigmaU activity in Streptomyces coelicolor.
Gordon ND, Ottaviano GL, Connell SE, Tobkin GV, Son CH, Shterental S, Gehring AM., J. Bacteriol. 190(3), 2007
PMID: 18065550
Deletion of a regulatory gene within the cpk gene cluster reveals novel antibacterial activity in Streptomyces coelicolor A3(2).
Gottelt M, Kol S, Gomez-Escribano JP, Bibb M, Takano E., Microbiology (Reading, Engl.) 156(Pt 8), 2010
PMID: 20447997
Multiple sigma subunits and the partitioning of bacterial transcription space.
Gruber TM, Gross CA., Annu. Rev. Microbiol. 57(), 2003
PMID: 14527287
Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces.
Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ, Chater KF., Adv. Appl. Microbiol. 54(), 2004
PMID: 15251278
Identified members of the Streptomyces lividans AdpA regulon involved in differentiation and secondary metabolism.
Guyet A, Benaroudj N, Proux C, Gominet M, Coppee JY, Mazodier P., BMC Microbiol. 14(), 2014
PMID: 24694298
Genome-wide dynamics of a bacterial response to antibiotics that target the cell envelope.
Hesketh A, Hill C, Mokhtar J, Novotna G, Tran N, Bibb M, Hong HJ., BMC Genomics 12(), 2011
PMID: 21569315
ReadXplorer 2-detailed read mapping analysis and visualization from one single source.
Hilker R, Stadermann KB, Schwengers O, Anisiforov E, Jaenicke S, Weisshaar B, Zimmermann T, Goesmann A., Bioinformatics 32(24), 2016
PMID: 27540267
Plasmids, recombination and chromosome mapping in Streptomyces lividans 66.
Hopwood DA, Kieser T, Wright HM, Bibb MJ., J. Gen. Microbiol. 129(7), 1983
PMID: 6631413
One-step high-efficiency CRISPR/Cas9-mediated genome editing in Streptomyces.
Huang H, Zheng G, Jiang W, Hu H, Lu Y., Acta Biochim. Biophys. Sin. (Shanghai) 47(4), 2015
PMID: 25739462
Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation.
Juven B., Pierson M.., 1996
Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae).
Kaltenpoth M, Yildirim E, Gurbuz MF, Herzner G, Strohm E., Appl. Environ. Microbiol. 78(3), 2011
PMID: 22113914
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A., Bioinformatics 28(12), 2012
PMID: 22543367

Kieser T., Bibb M., Buttner M., Chater K., Hopwood D.., 2000
Conservation of thiol-oxidative stress responses regulated by SigR orthologues in actinomycetes.
Kim MS, Dufour YS, Yoo JS, Cho YB, Park JH, Nam GB, Kim HM, Lee KL, Donohue TJ, Roe JH., Mol. Microbiol. 85(2), 2012
PMID: 22651816
Fast and reliable strain characterization of Streptomyces lividans through micro-scale cultivation.
Koepff J, Keller M, Tsolis KC, Busche T, Ruckert C, Hamed MB, Anne J, Kalinowski J, Wiechert W, Economou A, Oldiges M., Biotechnol. Bioeng. 114(9), 2017
PMID: 28436005
Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions.
Koepff J, Sachs CC, Wiechert W, Kohlheyer D, Noh K, Oldiges M, Grunberger A., Front Microbiol 9(), 2018
PMID: 30524383
Diamide: an oxidant probe for thiols.
Kosower NS, Kosower EM., Meth. Enzymol. 251(), 1995
PMID: 7651192
Control of Morphological Differentiation of Streptomyces coelicolor A3(2) by Phosphorylation of MreC and PBP2.
Ladwig N, Franz-Wachtel M, Hezel F, Soufi B, Macek B, Wohlleben W, Muth G., PLoS ONE 10(4), 2015
PMID: 25927987
A master regulator sigmaB governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor.
Lee EJ, Karoonuthaisiri N, Kim HS, Park JH, Cha CJ, Kao CM, Roe JH., Mol. Microbiol. 57(5), 2005
PMID: 16101999
The SCO4117 ECF Sigma Factor Pleiotropically Controls Secondary Metabolism and Morphogenesis in Streptomyces coelicolor.
Lopez-Garcia MT, Yague P, Gonzalez-Quinonez N, Rioseras B, Manteca A., Front Microbiol 9(), 2018
PMID: 29515563
The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages.
Manganelli R, Voskuil MI, Schoolnik GK, Smith I., Mol. Microbiol. 41(2), 2001
PMID: 11489128
Involvement of SigT and RstA in the differentiation of Streptomyces coelicolor.
Mao XM, Zhou Z, Cheng LY, Hou XP, Guan WJ, Li YQ., FEBS Lett. 583(19), 2009
PMID: 19755120
Intergeneric conjugation between Escherichia coli and Streptomyces species.
Mazodier P, Petter R, Thompson C., J. Bacteriol. 171(6), 1989
PMID: 2656662
Iterative marker excision system.
Myronovskyi M, Rosenkranzer B, Luzhetskyy A., Appl. Microbiol. Biotechnol. 98(10), 2014
PMID: 24473925
Beta-glucuronidase as a sensitive and versatile reporter in actinomycetes.
Myronovskyi M, Welle E, Fedorenko V, Luzhetskyy A., Appl. Environ. Microbiol. 77(15), 2011
PMID: 21685164
The dynamic architecture of the metabolic switch in Streptomyces coelicolor.
Nieselt K, Battke F, Herbig A, Bruheim P, Wentzel A, Jakobsen OM, Sletta H, Alam MT, Merlo ME, Moore J, Omara WA, Morrissey ER, Juarez-Hermosillo MA, Rodriguez-Garcia A, Nentwich M, Thomas L, Iqbal M, Legaie R, Gaze WH, Challis GL, Jansen RC, Dijkhuizen L, Rand DA, Wild DL, Bonin M, Reuther J, Wohlleben W, Smith MC, Burroughs NJ, Martin JF, Hodgson DA, Takano E, Breitling R, Ellingsen TE, Wellington EM., BMC Genomics 11(), 2010
PMID: 20053288
Gene expression after transformation of Streptomyces lividans protoplasts with plasmid pIJ2 DNA.
Noack D, Fiedler G, Geuther R., Z. Allg. Mikrobiol. 24(3), 1984
PMID: 6328780
An alternative sigma factor governs the principal sigma factor in Streptomyces griseus.
Otani H, Higo A, Nanamiya H, Horinouchi S, Ohnishi Y., Mol. Microbiol. 87(6), 2013
PMID: 23347076

Paget M., Hong H.-J., Bibb M., Buttner M.., 2002
Tris-dependent oxidative DNA strand scission during electrophoresis.
Ray T, Mills A, Dyson P., Electrophoresis 16(6), 1995
PMID: 7498131
Actinomycetes biosynthetic potential: how to bridge in silico and in vivo?
Rebets Y, Brotz E, Tokovenko B, Luzhetskyy A., J. Ind. Microbiol. Biotechnol. 41(2), 2013
PMID: 24127068
Cloning and Expression of Metagenomic DNA in Streptomyces lividans and Subsequent Fermentation for Optimized Production.
Rebets Y, Kormanec J, Luzhetskyy A, Bernaerts K, Anne J., Methods Mol. Biol. 1539(), 2017
PMID: 27900687
A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome.
Redenbach M, Kieser HM, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood DA., Mol. Microbiol. 21(1), 1996
PMID: 8843436
Complete genome sequence of Streptomyces lividans TK24.
Ruckert C, Albersmeier A, Busche T, Jaenicke S, Winkler A, Friðjonsson OH, Hreggviðsson GO, Lambert C, Badcock D, Bernaerts K, Anne J, Economou A, Kalinowski J., J. Biotechnol. 199(), 2015
PMID: 25680930
Global quantification of mammalian gene expression control.
Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M., Nature 473(7347), 2011
PMID: 21593866
Bacterial protection of beetle-fungus mutualism.
Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR., Science 322(5898), 2008
PMID: 18832638
New approaches to achieve high level enzyme production in Streptomyces lividans.
Sevillano L, Vijgenboom E, van Wezel GP, Diaz M, Santamaria RI., Microb. Cell Fact. 15(), 2016
PMID: 26846788
Resuscitation-promoting factors are cell wall-lytic enzymes with important roles in the germination and growth of Streptomyces coelicolor.
Sexton DL, St-Onge RJ, Haiser HJ, Yousef MR, Brady L, Gao C, Leonard J, Elliot MA., J. Bacteriol. 197(5), 2014
PMID: 25512314
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443
Reducing the variability of antibiotic production in Streptomyces by cultivation in 24-square deepwell plates.
Siebenberg S, Bapat PM, Lantz AE, Gust B, Heide L., J. Biosci. Bioeng. 109(3), 2009
PMID: 20159569
Connecting Metabolic Pathways: Sigma Factors in Streptomyces spp.
Sun D, Liu C, Zhu J, Liu W., Front Microbiol 8(), 2017
PMID: 29312231
Occurrence, evolution, and functions of DNA phosphorothioate epigenetics in bacteria.
Tong T, Chen S, Wang L, Tang Y, Ryu JY, Jiang S, Wu X, Chen C, Luo J, Deng Z, Li Z, Lee SY, Chen S., Proc. Natl. Acad. Sci. U.S.A. 115(13), 2018
PMID: 29531068
CRISPR-Cas9 Based Engineering of Actinomycetal Genomes.
Tong Y, Charusanti P, Zhang L, Weber T, Lee SY., ACS Synth Biol 4(9), 2015
PMID: 25806970
Quantitative Proteomics of the E. coli Membranome.
Tsolis KC, Economou A., Meth. Enzymol. 586(), 2016
PMID: 28137561
Comprehensive subcellular topologies of polypeptides in Streptomyces.
Tsolis KC, Tsare EP, Orfanoudaki G, Busche T, Kanaki K, Ramakrishnan R, Rousseau F, Schymkowitz J, Ruckert C, Kalinowski J, Anne J, Karamanou S, Klapa MI, Economou A., Microb. Cell Fact. 17(1), 2018
PMID: 29544487
Regulation of myo-inositol catabolism by a GntR-type repressor SCO6974 in Streptomyces coelicolor.
Yu L, Li S, Gao W, Pan Y, Tan H, Liu G., Appl. Microbiol. Biotechnol. 99(7), 2015
PMID: 25575890
Streptomyces coelicolor A3(2) lacks a genomic island present in the chromosome of Streptomyces lividans 66.
Zhou X, He X, Li A, Lei F, Kieser T, Deng Z., Appl. Environ. Microbiol. 70(12), 2004
PMID: 15574907
Site-specific degradation of Streptomyces lividans DNA during electrophoresis in buffers contaminated with ferrous iron.
Zhou X, Deng Z, Firmin JL, Hopwood DA, Kieser T., Nucleic Acids Res. 16(10), 1988
PMID: 2837731

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