Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach

Musa YR, Baesell K, Schatschneider S, Vorhölter F-J, Becher D, Niehaus K (2013)
Journal of Biotechnology 167(2): 111-122.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ;
Abstract / Bemerkung
Xanthomonas campestris pv. campestris (Xcc) synthesizes huge amounts of the exopolysaccharide xanthan and is a plant pathogen affecting Brassicaceae, among them the model plant Arabidopsis thaliana. Xanthan is produced as a thickening agent at industrial scale by fermentation of Xcc. In an approach based on 2D gel electrophoresis, protein samples from different growth phases were characterized to initialize analysis of the Xanthomonas phosphoproteome. The 2D gels were stained with Pro-Q Diamond phosphoprotein stain to identify putatively phosphorylated proteins. Spots of putatively phosphorylated proteins were excised from the gel and analyzed by mass spectrometry. Three proteins were confirmed to be phosphorylated, the phosphoglucomutase/phosphomannomutase XanA that is important for xanthan and lipopolysaccharide biosynthesis, the phosphoenolpyruvate synthase PspA that is involved in gluconeogenesis, and an anti-sigma factor antagonist RsbR that was so far uncharacterized in xanthomonads. The growth phase in which the samples were collected had an influence on protein phosphorylation in Xcc, particular distinct in case of RsbR, which was phosphorylated during the transition from the late exponential growth phase to the stationary phase. (C) 2013 Elsevier B.V. All rights reserved.
Erscheinungsjahr
Zeitschriftentitel
Journal of Biotechnology
Band
167
Zeitschriftennummer
2
Seite
111-122
ISSN
PUB-ID

Zitieren

Musa YR, Baesell K, Schatschneider S, Vorhölter F-J, Becher D, Niehaus K. Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. Journal of Biotechnology. 2013;167(2):111-122.
Musa, Y. R., Baesell, K., Schatschneider, S., Vorhölter, F. - J., Becher, D., & Niehaus, K. (2013). Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. Journal of Biotechnology, 167(2), 111-122. doi:10.1016/j.jbiotec.2013.06.009
Musa, Y. R., Baesell, K., Schatschneider, S., Vorhölter, F. - J., Becher, D., and Niehaus, K. (2013). Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. Journal of Biotechnology 167, 111-122.
Musa, Y.R., et al., 2013. Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. Journal of Biotechnology, 167(2), p 111-122.
Y.R. Musa, et al., “Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach”, Journal of Biotechnology, vol. 167, 2013, pp. 111-122.
Musa, Y.R., Baesell, K., Schatschneider, S., Vorhölter, F.-J., Becher, D., Niehaus, K.: Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach. Journal of Biotechnology. 167, 111-122 (2013).
Musa, Yaarub Raji, Baesell, Katrin, Schatschneider, Sarah, Vorhölter, Frank-Jörg, Becher, Doerte, and Niehaus, Karsten. “Dynamic protein phosphorylation during the growth of Xanthomonas campestris pv. campestris B100 revealed by a gel-based proteomics approach”. Journal of Biotechnology 167.2 (2013): 111-122.

9 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Comparative proteomic analysis of Xanthomonas citri ssp. citri periplasmic proteins reveals changes in cellular envelope metabolism during in vitro pathogenicity induction.
Artier J, da Silva Zandonadi F, de Souza Carvalho FM, Pauletti BA, Leme AFP, Carnielli CM, Selistre-de-Araujo HS, Bertolini MC, Ferro JA, Belasque Júnior J, de Oliveira JCF, Novo-Mansur MTM., Mol Plant Pathol 19(1), 2018
PMID: 27798950
Comparative transcription profiling of two fermentation cultures of Xanthomonas campestris pv. campestris B100 sampled in the growth and in the stationary phase.
Alkhateeb RS, Vorhölter FJ, Steffens T, Rückert C, Ortseifen V, Hublik G, Niehaus K, Pühler A., Appl Microbiol Biotechnol 102(15), 2018
PMID: 29858955
Refined annotation of the complete genome of the phytopathogenic and xanthan producing Xanthomonas campestris pv. campestris strain B100 based on RNA sequence data.
Alkhateeb RS, Rückert C, Rupp O, Pucker B, Hublik G, Wibberg D, Niehaus K, Pühler A, Vorhölter FJ., J Biotechnol 253(), 2017
PMID: 28506932
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
Systems and synthetic biology perspective of the versatile plant-pathogenic and polysaccharide-producing bacterium Xanthomonas campestris.
Schatschneider S, Schneider J, Blom J, Létisse F, Niehaus K, Goesmann A, Vorhölter FJ., Microbiology 163(8), 2017
PMID: 28795660
Proteomic profiling of Bacillus licheniformis reveals a stress response mechanism in the synthesis of extracellular polymeric flocculants.
Yu W, Chen Z, Shen L, Wang Y, Li Q, Yan S, Zhong CJ, He N., Biotechnol Bioeng 113(4), 2016
PMID: 26388297
Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Xanthomonas campestris pv. campestris.
Frese M, Schatschneider S, Voss J, Vorhölter FJ, Niehaus K., Arch Biochem Biophys 546(), 2014
PMID: 24508689

93 References

Daten bereitgestellt von Europe PubMed Central.

Ser/Thr/Tyr protein phosphorylation in the archaeon Halobacterium salinarum--a representative of the third domain of life.
Aivaliotis M, Macek B, Gnad F, Reichelt P, Mann M, Oesterhelt D., PLoS ONE 4(3), 2009
PMID: 19274099
Qupe--a Rich Internet Application to take a step forward in the analysis of mass spectrometry-based quantitative proteomics experiments.
Albaum SP, Neuweger H, Franzel B, Lange S, Mertens D, Trotschel C, Wolters D, Kalinowski J, Nattkemper TW, Goesmann A., Bioinformatics 25(23), 2009
PMID: 19808875
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
High-resolution transcriptional analysis of the regulatory influence of cell-to-cell signalling reveals novel genes that contribute to Xanthomonas phytopathogenesis
An, Molecular Microbiology (), 2013
The STAS domain – a link between anion transporters and antisigma-factor antagonists
Aravind, Current Biology 10(), 2000
Bacterial polysaccharides suppress induced innate immunity by calcium chelation.
Aslam SN, Newman MA, Erbs G, Morrissey KL, Chinchilla D, Boller T, Jensen TT, De Castro C, Ierano T, Molinaro A, Jackson RW, Knight MR, Cooper RM., Curr. Biol. 18(14), 2008
PMID: 18639458
Xanthan gum biosynthesis and application: a biochemical/genetic perspective.
Becker A, Katzen F, Puhler A, Ielpi L., Appl. Microbiol. Biotechnol. 50(2), 1998
PMID: 9763683
EDGAR: a software framework for the comparative analysis of prokaryotic genomes.
Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19457249
Insights into the extracytoplasmic stress response of Xanthomonas campestris pv. campestris: role and regulation of {sigma}E-dependent activity.
Bordes P, Lavatine L, Phok K, Barriot R, Boulanger A, Castanie-Cornet MP, Dejean G, Lauber E, Becker A, Arlat M, Gutierrez C., J. Bacteriol. 193(1), 2010
PMID: 20971899
Regulation and secretion of Xanthomonas virulence factors.
Buttner D, Bonas U., FEMS Microbiol. Rev. 34(2), 2009
PMID: 19925633
Purification of a phosphoprotein from chromatin of rat liver.
Chan PK, Liew CC., Biochem. J. 183(1), 1979
PMID: 534478
Specific protein phosphorylation induced in Xanthomonas campestris pv. oryzae by bacteriophage Xp12.
Cheng CM, Tu J, Yang CC, Kuo TT., Arch. Microbiol. 161(4), 1994
PMID: 8002710
Qualitative and comparative proteomic analysis of Xanthomonas campestris pv. campestris 17.
Chung WJ, Shu HY, Lu CY, Wu CY, Tseng YH, Tsai SF, Lin CH., Proteomics 7(12), 2007
PMID: 17566974
Enzyme-specific profiles for genome annotation: PRIAM.
Claudel-Renard C, Chevalet C, Faraut T, Kahn D., Nucleic Acids Res. 31(22), 2003
PMID: 14602924
The mechanism of the phosphoenolpyruvate synthase reaction.
Cooper RA, Kornberg HL., Biochim. Biophys. Acta 141(1), 1967
PMID: 4293109
Comparison of the genomes of two Xanthomonas pathogens with differing host specificities.
da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, do Amaral AM, Bertolini MC, Camargo LE, Camarotte G, Cannavan F, Cardozo J, Chambergo F, Ciapina LP, Cicarelli RM, Coutinho LL, Cursino-Santos JR, El-Dorry H, Faria JB, Ferreira AJ, Ferreira RC, Ferro MI, Formighieri EF, Franco MC, Greggio CC, Gruber A, Katsuyama AM, Kishi LT, Leite RP, Lemos EG, Lemos MV, Locali EC, Machado MA, Madeira AM, Martinez-Rossi NM, Martins EC, Meidanis J, Menck CF, Miyaki CY, Moon DH, Moreira LM, Novo MT, Okura VK, Oliveira MC, Oliveira VR, Pereira HA, Rossi A, Sena JA, Silva C, de Souza RF, Spinola LA, Takita MA, Tamura RE, Teixeira EC, Tezza RI, Trindade dos Santos M, Truffi D, Tsai SM, White FF, Setubal JC, Kitajima JP., Nature 417(6887), 2002
PMID: 12024217
Fructose phosphotransferase system of Xanthomonas campestris pv. campestris: characterization of the fruB gene.
de Crecy-Lagard V, Binet M, Danchin A., Microbiology (Reading, Engl.) 141 ( Pt 9)(), 1995
PMID: 7496537
Ser/Thr/Tyr protein phosphorylation in bacteria - for long time neglected, now well established.
Deutscher J, Saier MH Jr., J. Mol. Microbiol. Biotechnol. 9(3-4), 2005
PMID: 16415586
Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity
Erbs, Chemistry and Biology 15(), 2008
Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis.
Eymann C, Becher D, Bernhardt J, Gronau K, Klutzny A, Hecker M., Proteomics 7(19), 2007
PMID: 17726680
In vivo phosphorylation patterns of key stressosome proteins define a second feedback loop that limits activation of Bacillus subtilis σB.
Eymann C, Schulz S, Gronau K, Becher D, Hecker M, Price CW., Mol. Microbiol. 80(3), 2011
PMID: 21362065
Changes to the proteome and targeted metabolites of xylem sap in Brassica oleracea in response to salt stress.
Fernandez-Garcia N, Hernandez M, Casado-Vela J, Bru R, Elortza F, Hedden P, Olmos E., Plant Cell Environ. 34(5), 2011
PMID: 21276013
The Pfam protein families database
Finn, Nucleic Acids Research 38(), 2010
Xanthan gum: production, recovery, and properties.
Garcia-Ochoa F, Santos VE, Casas JA, Gomez E., Biotechnol. Adv. 18(7), 2000
PMID: 14538095
Tyrosine sulfation in a Gram-negative bacterium.
Han SW, Lee SW, Bahar O, Schwessinger B, Robinson MR, Shaw JB, Madsen JA, Brodbelt JS, Ronald PC., Nat Commun 3(), 2012
PMID: 23093190
Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110
Hayashi, Molecular Systems Biology 2(), 2006
SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria.
Hecker M, Pane-Farre J, Volker U., Annu. Rev. Microbiol. 61(), 2007
PMID: 18035607
Swiveling-domain mechanism for enzymatic phosphotransfer between remote reaction sites.
Herzberg O, Chen CC, Kapadia G, McGuire M, Carroll LJ, Noh SJ, Dunaway-Mariano D., Proc. Natl. Acad. Sci. U.S.A. 93(7), 1996
PMID: 8610096
Bacterial protein acetylation: the dawning of a new age.
Hu LI, Lima BP, Wolfe AJ., Mol. Microbiol. 77(1), 2010
PMID: 20487279
Xanthan
Hublik, 2012
Pyruvic acid acetal residues are transferred from phosphoenolpyruvate to the pentasaccharide-P-P-lipid.
Ielpi L, Couso RO, Dankert MA., Biochem. Biophys. Res. Commun. 102(4), 1981
PMID: 7317056
Xanthan gum biosynthesis: acetylation occurs at the prenyl-phospho-sugar stage
Ielpi, Biochemistry International 6(), 1983
Structure of extracellular polysaccharide from Xanthomonas campestris.
Jansson PE, Kenne L, Lindberg B., Carbohydr. Res. 45(), 1975
PMID: 1212669
Promoter analysis of the Xanthomonas campestris pv. campestris gum operon directing biosynthesis of the xanthan polysaccharide.
Katzen F, Becker A, Zorreguieta A, Puhler A, Ielpi L., J. Bacteriol. 178(14), 1996
PMID: 8763965
A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity.
Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC., Science 326(5954), 2009
PMID: 19892983
Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation
Macek, Molecular and Cellular Proteomics 7(), 2008
Insights into the genome of the xanthan-producing phytopathogen Xanthomonas arboricola pv. pruni 109 by comparative genomic hybridization.
Mayer L, Vendruscolo CT, Silva WP, Vorholter FJ, Becker A, Puhler A., J. Biotechnol. 155(1), 2011
PMID: 21539867
Impact of phosphoproteomics on studies of bacterial physiology.
Mijakovic I, Macek B., FEMS Microbiol. Rev. 36(4), 2011
PMID: 22091997
Roles of active site residues in Pseudomonas aeruginosa phosphomannomutase/phosphoglucomutase.
Naught LE, Regni C, Beamer LJ, Tipton PA., Biochemistry 42(33), 2003
PMID: 12924943
Cloning and nucleotide sequence of the Escherichia coli K-12 ppsA gene, encoding PEP synthase
Niersbach, Molecular and General Genetics 231(), 1992
Protein glycosylation in bacteria: sweeter than ever.
Nothaft H, Szymanski CM., Nat. Rev. Microbiol. 8(11), 2010
PMID: 20948550
MyHits: improvements to an interactive resource for analyzing protein sequences.
Pagni M, Ioannidis V, Cerutti L, Zahn-Zabal M, Jongeneel CV, Hau J, Martin O, Kuznetsov D, Falquet L., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17545200
The RsbRST stress module in bacteria: a signalling system that may interact with different output modules.
Pane-Farre J, Lewis RJ, Stulke J., J. Mol. Microbiol. Biotechnol. 9(2), 2005
PMID: 16319496
Sigma factors and promoters in Corynebacterium glutamicum.
Patek M, Nesvera J., J. Biotechnol. 154(2-3), 2011
PMID: 21277915
Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris.
Qian W, Jia Y, Ren SX, He YQ, Feng JX, Lu LF, Sun Q, Ying G, Tang DJ, Tang H, Wu W, Hao P, Wang L, Jiang BL, Zeng S, Gu WY, Lu G, Rong L, Tian Y, Yao Z, Fu G, Chen B, Fang R, Qiang B, Chen Z, Zhao GP, Tang JL, He C., Genome Res. 15(6), 2005
PMID: 15899963
Molecules involved in the modulation of rapid cell death in Xanthomonas.
Raju KK, Gautam S, Sharma A., J. Bacteriol. 188(15), 2006
PMID: 16855230
Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris.
Ryan RP, McCarthy Y, Kiely PA, O'Connor R, Farah CS, Armitage JP, Dow JM., Mol. Microbiol. 86(3), 2012
PMID: 22924852
Pathogenomics of Xanthomonas: understanding bacterium-plant interactions.
Ryan RP, Vorholter FJ, Potnis N, Jones JB, Van Sluys MA, Bogdanove AJ, Dow JM., Nat. Rev. Microbiol. 9(5), 2011
PMID: 21478901
Establishment, in silico analysis, and experimental verification of a large-scale metabolic network of the xanthan producing Xanthomonas campestris pv. campestris strain B100
Schatschneider, Journal of Biotechnology (), 2013
Backbone flexibility, conformational change, and catalysis in a phosphohexomutase from Pseudomonas aeruginosa.
Schramm AM, Mehra-Chaudhary R, Furdui CM, Beamer LJ., Biochemistry 47(35), 2008
PMID: 18690721
In-gel digestion for mass spectrometric characterization of proteins and proteomes
Shevchenko, Nature Protocols 1(), 2007
PROSITE, a protein domain database for functional characterization and annotation
Sigrist, Nucleic Acids Research 38(), 2010
Location of a second O-acetyl group in xanthan gum by the reductive-cleavage method.
Stankowski JD, Mueller BE, Zeller SG., Carbohydr. Res. 241(), 1993
PMID: 8472258

AUTHOR UNKNOWN, 1993
Xanthomonas campestris pv. campestris possesses a single gluconeogenic pathway that is required for virulence.
Tang DJ, He YQ, Feng JX, He BR, Jiang BL, Lu GT, Chen B, Tang JL., J. Bacteriol. 187(17), 2005
PMID: 16109965
Genome sequence of Xanthomonas campestris JX, an industrially productive strain for Xanthan gum.
Tao F, Wang X, Ma C, Yang C, Tang H, Gai Z, Xu P., J. Bacteriol. 194(17), 2012
PMID: 22887662
Reorganizing the protein space at the Universal Protein Resource (UniProt).
UniProt Consortium, Apweiler R, Jesus Martin M, O'onovan C, Magrane M, Alam-Faruque Y, Antunes R, Barrera Casanova E, Bely B, Bingley M, Bower L, Bursteinas B, Mun Chan W, Chavali G, Da Silva A, Dimmer E, Eberhardt R, Fazzini F, Fedotov A, Garavelli J, Castro LG, Gardner M, Hieta R, Huntley R, Jacobsen J, Legge D, Liu W, Luo J, Orchard S, Patient S, Pichler K, Poggioli D, Pontikos N, Pundir S, Rosanoff S, Sawford T, Sehra H, Turner E, Wardell T, Watkins X, Corbett M, Donnelly M, van Rensburg P, Goujon M, McWilliam H, Lopez R, Xenarios I, Bougueleret L, Bridge A, Poux S, Redaschi N, Argoud-Puy G, Auchincloss A, Axelsen K, Baratin D, Blatter MC, Boeckmann B, Bolleman J, Bollondi L, Boutet E, Braconi Quintaje S, Breuza L, deCastro E, Cerutti L, Coudert E, Cuche B, Cusin I, Doche M, Dornevil D, Duvaud S, Estreicher A, Famiglietti L, Feuermann M, Gehant S, Ferro S, Gasteiger E, Gerritsen V, Gos A, Gruaz-Gumowski N, Hinz U, Hulo C, Hulo N, James J, Jimenez S, Jungo F, Kappler T, Keller G, Lara V, Lemercier P, Lieberherr D, Martin X, Masson P, Moinat M, Morgat A, Paesano S, Pedruzzi I, Pilbout S, Pozzato M, Pruess M, Rivoire C, Roechert B, Schneider M, Sigrist C, Sonesson K, Staehli S, Stanley E, Stutz A, Sundaram S, Tognolli M, Verbregue L, Veuthey AL, Wu CH, Arighi CN, Arminski L, Barker WC, Chen C, Chen Y, Dubey P, Huang H, Kukreja A, Laiho K, Mazumder R, McGarvey P, Natale DA, Natarajan TG, Roberts NV, Suzek BE, Vinayaka C, Wang Q, Wang Y, Yeh LS, Zhang J., Nucleic Acids Res. 40(Database issue), 2011
PMID: 22102590
Expression of the gum operon directing xanthan biosynthesis in Xanthomonas campestris and its regulation in planta.
Vojnov AA, Slater H, Daniels MJ, Dow JM., Mol. Plant Microbe Interact. 14(6), 2001
PMID: 11386372
Comparison of two Xanthomonas campestris pathovar campestris genomes revealed differences in their gene composition.
Vorholter FJ, Thias T, Meyer F, Bekel T, Kaiser O, Puhler A, Niehaus K., J. Biotechnol. 106(2-3), 2003
PMID: 14651861
The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis.
Vorholter FJ, Schneiker S, Goesmann A, Krause L, Bekel T, Kaiser O, Linke B, Patschkowski T, Ruckert C, Schmid J, Sidhu VK, Sieber V, Tauch A, Watt SA, Weisshaar B, Becker A, Niehaus K, Puhler A., J. Biotechnol. 134(1-2), 2008
PMID: 18304669
RNA-Seq facilitates a new perspective on signal transduction and gene regulation in important plant pathogens
Vorhölter, Molecular Microbiology (), 2013
A bacterial cell-cell communication signal with cross-kingdom structural analogues.
Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH., Mol. Microbiol. 51(3), 2004
PMID: 14731288
Comprehensive analysis of the extracellular proteins from Xanthomonas campestris pv. campestris B100.
Watt SA, Wilke A, Patschkowski T, Niehaus K., Proteomics 5(1), 2005
PMID: 15619296
Comparative glucose catabolism of Xanthomonas species.
Zagallo AC, Wang CH., J. Bacteriol. 93(3), 1967
PMID: 6025434
The diffusible factor synthase XanB2 is a bifunctional chorismatase that links the shikimate pathway to ubiquinone and xanthomonadins biosynthetic pathways.
Zhou L, Wang JY, Wu J, Wang J, Poplawsky A, Lin S, Zhu B, Chang C, Zhou T, Zhang LH, He YW., Mol. Microbiol. 87(1), 2012
PMID: 23113660

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 23792782
PubMed | Europe PMC

Suchen in

Google Scholar