Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes

Busche T, Winkler A, Wedderhoff I, Rückert C, Kalinowski J, Lucana DO de O (2016)
PLOS ONE 11(8): e0159873.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
Abstract / Bemerkung
The secreted protein HbpS, the membrane-embedded sensor kinase SenS and the cytoplasmic response regulator SenR from streptomycetes have been shown to form a novel type of signaling pathway. Based on structural biology as well as different biochemical and biophysical approaches, redox stress-based post-translational modifications in the three proteins were shown to modulate the activity of this signaling pathway. In this study, we show that the homologous system, named here HbpSc-SenSc-SenRc, from the model species Streptomyces coelicolor A3(2) provides this bacterium with an efficient defense mechanism under conditions of oxidative stress. Comparative analyses of the transcriptomes of the Streptomyces coelicolor A3(2) wild-type and the generated hbpSc-senSc-senRc mutant under native and oxidative-stressing conditions allowed to identify differentially expressed genes, whose products may enhance the anti-oxidative defense of the bacterium. Amongst others, the results show an up-regulated transcription of genes for biosynthesis of cysteine and vitamin B-12, transport of methionine and vitamin B-12, and DNA synthesis and repair. Simultaneously, transcription of genes for degradation of an anti-oxidant compound is down-regulated in a HbpSc-SenSc-SenRc-dependent manner. It appears that HbpSc-SenSc-SenRc controls the non-enzymatic response of Streptomyces coelicolor A3(2) to counteract the hazardous effects of oxidative stress. Binding of the response regulator SenRc to regulatory regions of some of the studied genes indicates that the regulation is direct. The results additionally suggest that HbpSc-SenSc-SenRc may act in concert with other regulatory modules such as a transcriptional regulator, a two-component system and the Streptomyces B-12 riboswitch. The transcriptomics data, together with our previous in vitro results, enable a profound characterization of the HbpS-SenS-SenR system from streptomycetes. Since homologues to HbpS-SenS-SenR are widespread in different actinobacteria with ecological and medical relevance, the data presented here will serve as a basis to elucidate the biological role of these homologues.
Erscheinungsjahr
Zeitschriftentitel
PLOS ONE
Band
11
Ausgabe
8
Art.-Nr.
e0159873
ISSN
PUB-ID

Zitieren

Busche T, Winkler A, Wedderhoff I, Rückert C, Kalinowski J, Lucana DO de O. Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLOS ONE. 2016;11(8): e0159873.
Busche, T., Winkler, A., Wedderhoff, I., Rückert, C., Kalinowski, J., & Lucana, D. O. de O. (2016). Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLOS ONE, 11(8), e0159873. doi:10.1371/journal.pone.0159873
Busche, T., Winkler, A., Wedderhoff, I., Rückert, C., Kalinowski, J., and Lucana, D. O. de O. (2016). Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLOS ONE 11:e0159873.
Busche, T., et al., 2016. Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLOS ONE, 11(8): e0159873.
T. Busche, et al., “Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes”, PLOS ONE, vol. 11, 2016, : e0159873.
Busche, T., Winkler, A., Wedderhoff, I., Rückert, C., Kalinowski, J., Lucana, D.O. de O.: Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes. PLOS ONE. 11, : e0159873 (2016).
Busche, Tobias, Winkler, Anika, Wedderhoff, Ina, Rückert, Christian, Kalinowski, Jörn, and Lucana, Dario Ortiz de Orue. “Deciphering the Transcriptional Response Mediated by the Redox-Sensing System HbpS-SenS-SenR from Streptomycetes”. PLOS ONE 11.8 (2016): e0159873.

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Physiological roles of sigma factor SigD in Corynebacterium glutamicum.
Taniguchi H, Busche T, Patschkowski T, Niehaus K, Pátek M, Kalinowski J, Wendisch VF., BMC Microbiol 17(1), 2017
PMID: 28701150

93 References

Daten bereitgestellt von Europe PubMed Central.

Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium.
Flardh K, Buttner MJ., Nat. Rev. Microbiol. 7(1), 2009
PMID: 19079351
Taxonomy, Physiology, and Natural Products of Actinobacteria.
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Meier-Kolthoff JP, Klenk HP, Clement C, Ouhdouch Y, van Wezel GP., Microbiol. Mol. Biol. Rev. 80(1), 2015
PMID: 26609051
The complex extracellular biology of Streptomyces.
Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H., FEMS Microbiol. Rev. 34(2), 2009
PMID: 20088961
The cellulolytic system of Streptomyces reticuli.
Schrempf H, Walter S., Int. J. Biol. Macromol. 17(6), 1995
PMID: 8789339
Genome plasticity and systems evolution in Streptomyces.
Zhou Z, Gu J, Li YQ, Wang Y., BMC Bioinformatics 13 Suppl 10(), 2012
PMID: 22759432
Recently published Streptomyces genome sequences.
Harrison J, Studholme DJ., Microb Biotechnol 7(5), 2014
PMID: 25100265
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
Two-component systems in Streptomyces: key regulators of antibiotic complex pathways.
Rodriguez H, Rico S, Diaz M, Santamaria RI., Microb. Cell Fact. 12(), 2013
PMID: 24354561
The mechanism of signal transduction by two-component systems.
Casino P, Rubio V, Marina A., Curr. Opin. Struct. Biol. 20(6), 2010
PMID: 20951027
Bacterial sensor kinases: diversity in the recognition of environmental signals.
Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME, Ramos JL., Annu. Rev. Microbiol. 64(), 2010
PMID: 20825354
PAS domains: internal sensors of oxygen, redox potential, and light.
Taylor BL, Zhulin IB., Microbiol. Mol. Biol. Rev. 63(2), 1999
PMID: 10357859
A ligand-induced switch in the periplasmic domain of sensor histidine kinase CitA.
Sevvana M, Vijayan V, Zweckstetter M, Reinelt S, Madden DR, Herbst-Irmer R, Sheldrick GM, Bott M, Griesinger C, Becker S., J. Mol. Biol. 377(2), 2008
PMID: 18258261
Novel redox-sensing modules: accessory protein- and nucleic acid-mediated signaling.
Siedenburg G, Groves MR, Ortiz de Orue Lucana D., Antioxid. Redox Signal. 16(7), 2012
PMID: 22114914
Iron binding at specific sites within the octameric HbpS protects streptomycetes from iron-mediated oxidative stress.
Wedderhoff I, Kursula I, Groves MR, Ortiz de Orue Lucana D., PLoS ONE 8(8), 2013
PMID: 24013686
The extracellular heme-binding protein HbpS from the soil bacterium Streptomyces reticuli is an aquo-cobalamin binder.
Ortiz de Orue Lucana D, Fedosov SN, Wedderhoff I, Che EN, Torda AE., J. Biol. Chem. 289(49), 2014
PMID: 25342754
Elucidation of haem-binding sites in the actinobacterial protein HbpS.
Torda AE, Groves MR, Wedderhoff I, Ortiz de Orue Lucana D., FEMS Microbiol. Lett. 342(2), 2013
PMID: 23373615
Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis.
Cho HY, Cho HJ, Kim YM, Oh JI, Kang BS., J. Biol. Chem. 284(19), 2009
PMID: 19276084
2.3 A X-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis.
Podust LM, Ioanoviciu A, Ortiz de Montellano PR., Biochemistry 47(47), 2008
PMID: 18980385
Iron-mediated oxidation induces conformational changes within the redox-sensing protein HbpS.
Ortiz de Orue Lucana D, Roscher M, Honigmann A, Schwarz J., J. Biol. Chem. 285(36), 2010
PMID: 20571030
Low-molecular-weight thiols in thiol-disulfide exchange.
Van Laer K, Hamilton CJ, Messens J., Antioxid. Redox Signal. 18(13), 2012
PMID: 23075082
Low-molecular-weight thiols in streptomycetes and their potential role as antioxidants.
Newton GL, Fahey RC, Cohen G, Aharonowitz Y., J. Bacteriol. 175(9), 1993
PMID: 8478335
Toxicity of iron and hydrogen peroxide: the Fenton reaction.
Winterbourn CC., Toxicol. Lett. 82-83(), 1995
PMID: 8597169

AUTHOR UNKNOWN, 1985
Antibiotic resistance gene cassettes derived from the omega interposon for use in E. coli and Streptomyces.
Blondelet-Rouault MH, Weiser J, Lebrihi A, Branny P, Pernodet JL., Gene 190(2), 1997
PMID: 9197550
A Vector System with Temperature-Sensitive Replication for Gene Disruption and Mutational Cloning in Streptomycetes
AUTHOR UNKNOWN, 1989
Crystallization and preliminary characterization of a novel haem-binding protein of Streptomyces reticuli.
Zou P, Groves MR, Viale-Bouroncle SD, Ortiz de Orue Lucana D., Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64(Pt 5), 2008
PMID: 18453708

AUTHOR UNKNOWN, 1989
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
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
ReadXplorer--visualization and analysis of mapped sequences.
Hilker R, Stadermann KB, Doppmeier D, Kalinowski J, Stoye J, Straube J, Winnebald J, Goesmann A., Bioinformatics 30(16), 2014
PMID: 24790157
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
The novel extracellular Streptomyces reticuli haem-binding protein HbpS influences the production of the catalase-peroxidase CpeB.
Ortiz de Orue Lucana D, Schaa T, Schrempf H., Microbiology (Reading, Engl.) 150(Pt 8), 2004
PMID: 15289554
Conversion of methionine to cysteine in Bacillus subtilis and its regulation.
Hullo MF, Auger S, Soutourina O, Barzu O, Yvon M, Danchin A, Martin-Verstraete I., J. Bacteriol. 189(1), 2006
PMID: 17056751
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
Genome-scale analysis reveals a role for NdgR in the thiol oxidative stress response in Streptomyces coelicolor.
Kim JN, Jeong Y, Yoo JS, Roe JH, Cho BK, Kim BG., BMC Genomics 16(), 2015
PMID: 25766138
Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes.
Sola-Landa A, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF., Mol. Microbiol. 56(5), 2005
PMID: 15882427
Transcriptional and preliminary functional analysis of the six genes located in divergence of phoR/phoP in Streptomyces lividans.
Darbon E, Martel C, Nowacka A, Pegot S, Moreau PL, Virolle MJ., Appl. Microbiol. Biotechnol. 95(6), 2012
PMID: 22466952
Streptomyces coelicolor SCO4226 is a nickel binding protein.
Lu M, Jiang YL, Wang S, Jin H, Zhang RG, Virolle MJ, Chen Y, Zhou CZ., PLoS ONE 9(10), 2014
PMID: 25285530
Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis.
Ames BN, Cathcart R, Schwiers E, Hochstein P., Proc. Natl. Acad. Sci. U.S.A. 78(11), 1981
PMID: 6947260
The Escherichia coli cysG gene encodes S-adenosylmethionine-dependent uroporphyrinogen III methylase.
Warren MJ, Roessner CA, Santander PJ, Scott AI., Biochem. J. 265(3), 1990
PMID: 2407234
A novel role for vitamin B(12): Cobalamins are intracellular antioxidants in vitro.
Birch CS, Brasch NE, McCaddon A, Williams JH., Free Radic. Biol. Med. 47(2), 2009
PMID: 19409980
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
NrdH Redoxin Enhances Resistance to Multiple Oxidative Stresses by Acting as a Peroxidase Cofactor in Corynebacterium glutamicum
AUTHOR UNKNOWN, 2014
RNA-Seq profiling reveals novel hepatic gene expression pattern in aflatoxin B1 treated rats.
Merrick BA, Phadke DP, Auerbach SS, Mav D, Stiegelmeyer SM, Shah RR, Tice RR., PLoS ONE 8(4), 2013
PMID: 23630614
Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG., Mol. Syst. Biol. 7(), 2011
PMID: 21988835
Transcriptomic studies of phosphate control of primary and secondary metabolism in Streptomyces coelicolor.
Martin JF, Santos-Beneit F, Rodriguez-Garcia A, Sola-Landa A, Smith MC, Ellingsen TE, Nieselt K, Burroughs NJ, Wellington EM., Appl. Microbiol. Biotechnol. 95(1), 2012
PMID: 22622839
WebLogo: a sequence logo generator.
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120
Interconversion of methionine and methionine sulfoxide.
Savige WE, Fontana A., Meth. Enzymol. 47(), 1977
PMID: 927198
Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation.
Levine RL, Moskovitz J, Stadtman ER., IUBMB Life 50(4-5), 2000
PMID: 11327324
Plant proteins under oxidative attack.
Jacques S, Ghesquiere B, Van Breusegem F, Gevaert K., Proteomics 13(6), 2013
PMID: 23172756
DksA-Dependent Transcriptional Regulation in Salmonella Experiencing Nitrosative Stress.
Crawford MA, Henard CA, Tapscott T, Porwollik S, McClelland M, Vazquez-Torres A., Front Microbiol 7(), 2016
PMID: 27065993
ROS-Mediated Signalling in Bacteria: Zinc-Containing Cys-X-X-Cys Redox Centres and Iron-Based Oxidative Stress.
Ortiz de Orue Lucana D, Wedderhoff I, Groves MR., J Signal Transduct 2012(), 2011
PMID: 21977318
Interplay between genetic regulation of phosphate homeostasis and bacterial virulence.
Chekabab SM, Harel J, Dozois CM., Virulence 5(8), 2014
PMID: 25483775
The Pho regulon: a huge regulatory network in bacteria.
Santos-Beneit F., Front Microbiol 6(), 2015
PMID: 25983732
Vitamin B(12) and redox homeostasis: cob(II)alamin reacts with superoxide at rates approaching superoxide dismutase (SOD).
Suarez-Moreira E, Yun J, Birch CS, Williams JH, McCaddon A, Brasch NE., J. Am. Chem. Soc. 131(42), 2009
PMID: 19799418
Vitamin B12: chemistry and biochemistry.
Krautler B., Biochem. Soc. Trans. 33(Pt 4), 2005
PMID: 16042603
Studies on vitamin B12 production with Streptomyces olivaceus.
HALL HH, BENEDICT RG, WIESEN CF, SMITH CE, JACKSON RW., Appl Microbiol 1(3), 1953
PMID: 13041183
Heterologous expression of the biosynthetic gene clusters of coumermycin A(1), clorobiocin and caprazamycins in genetically modified Streptomyces coelicolor strains.
Flinspach K, Westrich L, Kaysser L, Siebenberg S, Gomez-Escribano JP, Bibb M, Gust B, Heide L., Biopolymers 93(9), 2010
PMID: 20578003
Light-dependent gene regulation by a coenzyme B12-based photoreceptor.
Ortiz-Guerrero JM, Polanco MC, Murillo FJ, Padmanabhan S, Elias-Arnanz M., Proc. Natl. Acad. Sci. U.S.A. 108(18), 2011
PMID: 21502508
Vitamin B12 regulates photosystem gene expression via the CrtJ antirepressor AerR in Rhodobacter capsulatus.
Cheng Z, Li K, Hammad LA, Karty JA, Bauer CE., Mol. Microbiol. 91(4), 2014
PMID: 24329562
Members of the PpaA/AerR Antirepressor Family Bind Cobalamin.
Vermeulen AJ, Bauer CE., J. Bacteriol. 197(16), 2015
PMID: 26055116
Streptomyces spp. contain class Ia and class II ribonucleotide reductases: expression analysis of the genes in vegetative growth.
Borovok I, Kreisberg-Zakarin R, Yanko M, Schreiber R, Myslovati M, Aslund F, Holmgren A, Cohen G, Aharonowitz Y., Microbiology (Reading, Engl.) 148(Pt 2), 2002
PMID: 11832503
Oxidative DNA damage: mechanisms, mutation, and disease.
Cooke MS, Evans MD, Dizdaroglu M, Lunec J., FASEB J. 17(10), 2003
PMID: 12832285
Riboswitches. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA.
Mellin JR, Koutero M, Dar D, Nahori MA, Sorek R, Cossart P., Science 345(6199), 2014
PMID: 25146292
Riboswitches. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator.
DebRoy S, Gebbie M, Ramesh A, Goodson JR, Cruz MR, van Hoof A, Winkler WC, Garsin DA., Science 345(6199), 2014
PMID: 25146291
The mycelium-associated Streptomyces reticuli catalase-peroxidase, its gene and regulation by FurS.
Zou P, Borovok I, Ortiz de Orue Lucana D, Muller D, Schrempf H., Microbiology (Reading, Engl.) 145 ( Pt 3)(), 1999
PMID: 10217488

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 27541358
PubMed | Europe PMC

Suchen in

Google Scholar