Skip to main content
SpringerLink
Log in
Book cover

Microbial Proteomics pp 249–260Cite as

Phosphoproteomics in Microbiology: Protocols for Studying Streptomyces coelicolor Differentiation

  • Protocol
  • First Online:

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1841))

Abstract

The extension and biological role of Ser/Thr/Tyr phosphorylation in prokaryotes have been only scarcely studied. In this chapter, we describe the state of the art of microbial phosphoproteomics, focusing on protocols used for studying the phosphoproteome of Streptomyces coelicolor, one of the bacteria encoding the largest number of eukaryote-like Ser/Thr/Tyr kinases.

This is a preview of subscription content, log in via an institution.

Protocol
USD   49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Springer Nature is developing a new tool to find and evaluate Protocols. Learn more

References

  1. Pawson T, Scott JD (2005) Protein phosphorylation in signaling—50 years and counting. Trends Biochem Sci 30(6):286–290

    Article  CAS  PubMed  Google Scholar 

  2. Hoch JA (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3(2):165–170

    Article  CAS  PubMed  Google Scholar 

  3. Galperin MY, Nikolskaya AN, Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203(1):11–21

    Article  CAS  PubMed  Google Scholar 

  4. Kleinnijenhuis AJ, Kjeldsen F, Kallipolitis B, Haselmann KF, Jensen ON (2007) Analysis of histidine phosphorylation using tandem MS and ion-electron reactions. Anal Chem 79(19):7450–7456

    Article  CAS  PubMed  Google Scholar 

  5. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, Mann M (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7(2):299–307

    Article  CAS  PubMed  Google Scholar 

  6. Soares NC, Spat P, Krug K, Macek B (2013) Global dynamics of the Escherichia coli proteome and phosphoproteome during growth in minimal medium. J Proteome Res 12(6):2611–2621

    Article  CAS  PubMed  Google Scholar 

  7. Sun X, Ge F, Xiao CL, Yin XF, Ge R, Zhang LH, He QY (2010) Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J Proteome Res 9(1):275–282

    Article  CAS  PubMed  Google Scholar 

  8. Lin MH, Hsu TL, Lin SY, Pan YJ, Jan JT, Wang JT, Khoo KH, Wu SH (2009) Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol Cell Proteomics 8(12):2613–2623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Soufi B, Gnad F, Jensen PR, Petranovic D, Mann M, Mijakovic I, Macek B (2008) The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics 8(17):3486–3493

    Article  CAS  PubMed  Google Scholar 

  10. Ravichandran A, Sugiyama N, Tomita M, Swarup S, Ishihama Y (2009) Ser/Thr/Tyr phosphoproteome analysis of pathogenic and non-pathogenic Pseudomonas species. Proteomics 9(10):2764–2775

    Article  CAS  PubMed  Google Scholar 

  11. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, Jensen PR, Mann M (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6(4):697–707

    Article  CAS  PubMed  Google Scholar 

  12. Aivaliotis M, Macek B, Gnad F, Reichelt P, Mann M, Oesterhelt D (2009) Ser/Thr/Tyr protein phosphorylation in the archaeon Halobacterium salinarum—a representative of the third domain of life. PLoS One 4(3):e4777

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bai X, Ji Z (2012) Phosphoproteomic investigation of a solvent producing bacterium Clostridium acetobutylicum. Appl Microbiol Biotechnol 95(1):201–211

    Article  CAS  PubMed  Google Scholar 

  14. Parker JL, Jones AM, Serazetdinova L, Saalbach G, Bibb MJ, Naldrett MJ (2010) Analysis of the phosphoproteome of the multicellular bacterium Streptomyces coelicolor A3(2) by protein/peptide fractionation, phosphopeptide enrichment and high-accuracy mass spectrometry. Proteomics 10(13):2486–2497

    Article  CAS  PubMed  Google Scholar 

  15. Manteca A, Ye J, Sanchez J, Jensen ON (2011) Phosphoproteome analysis of Streptomyces development reveals extensive protein phosphorylation accompanying bacterial differentiation. J Proteome Res 10(12):5481–5492

    Article  CAS  PubMed  Google Scholar 

  16. Prisic S, Dankwa S, Schwartz D, Chou MF, Locasale JW, Kang CM, Bemis G, Church GM, Steen H, Husson RN (2010) Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc Natl Acad Sci U S A 107(16):7521–7526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Soares NC, Spat P, Mendez JA, Nakedi K, Aranda J, Bou G (2014) Ser/Thr/Tyr phosphoproteome characterization of Acinetobacter baumannii: comparison between a reference strain and a highly invasive multidrug-resistant clinical isolate. J Proteome 102:113–124

    Article  CAS  Google Scholar 

  18. Misra SK, Milohanic E, Ake F, Mijakovic I, Deutscher J, Monnet V, Henry C (2011) Analysis of the serine/threonine/tyrosine phosphoproteome of the pathogenic bacterium Listeria monocytogenes reveals phosphorylated proteins related to virulence. Proteomics 11(21):4155–4165

    Article  CAS  PubMed  Google Scholar 

  19. Hu CW, Lin MH, Huang HC, Ku WC, Yi TH, Tsai CF, Chen YJ, Sugiyama N, Ishihama Y, Juan HF, Wu SH (2012) Phosphoproteomic analysis of Rhodopseudomonas palustris reveals the role of pyruvate phosphate dikinase phosphorylation in lipid production. J Proteome Res 11(11):5362–5375

    Article  CAS  Google Scholar 

  20. Takahata Y, Inoue M, Kim K, Iio Y, Miyamoto M, Masui R, Ishihama Y, Kuramitsu S (2012) Close proximity of phosphorylation sites to ligand in the phosphoproteome of the extreme thermophile Thermus thermophilus HB8. Proteomics 12(9):1414–1430

    Article  CAS  PubMed  Google Scholar 

  21. Ge R, Sun X, Xiao C, Yin X, Shan W, Chen Z, He QY (2011) Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over-representation of tyrosine phosphorylation and multiply phosphorylated proteins. Proteomics 11(8):1449–1461

    Article  CAS  PubMed  Google Scholar 

  22. Bäsell K, Otto A, Junker S, Zühlke D, Rappen GM, Schmidt S, Hentschker C, Macek B, Ohlsen K, Hecker M, Becher D (2014) The phosphoproteome and its physiological dynamics in Staphylococcus aureus. Int J Med Microbiol 304(2):121–132

    Article  PubMed  Google Scholar 

  23. Zhang X, Ye J, Jensen ON, Roepstorff P (2007) Highly efficient phosphopeptide enrichment by calcium phosphate precipitation combined with subsequent IMAC enrichment. Mol Cell Proteomics 6(11):2032–2042

    Article  CAS  PubMed  Google Scholar 

  24. Omura S (1992) The expanded horizon for microbial metabolites—a review. Gene 115(1–2):141–149

    Article  CAS  PubMed  Google Scholar 

  25. Tamaoki T, Nakano H (1990) Potent and specific inhibitors of protein kinase C of microbial origin. Biotechnology (N Y) 8(8):732–735

    CAS  Google Scholar 

  26. Umezawa K (1997) Induction of cellular differentiation and apoptosis by signal transduction inhibitors. Adv Enzym Regul 37:393–401

    Article  CAS  Google Scholar 

  27. Katz L, Baltz RH (2016) Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 43:155–176

    Article  CAS  PubMed  Google Scholar 

  28. Yague P, Lopez-Garcia MT, Rioseras B, Sanchez J, Manteca A (2013) Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives. FEMS Microbiol Lett 342(2):79–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Perez J, Castaneda-Garcia A, Jenke-Kodama H, Muller R, Munoz-Dorado J (2008) Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc Natl Acad Sci U S A 105(41):15950–15955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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 (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417(6885):141–147

    Article  PubMed  Google Scholar 

  31. Novella IS, Barbes C, Sanchez J (1992) Sporulation of Streptomyces antibioticus ETHZ 7451 in submerged culture. Can J Microbiol 38(8):769–773

    Article  CAS  PubMed  Google Scholar 

  32. Sharma K, D'Souza RC, Tyanova S, Schaab C, Wisniewski JR, Cox J, Mann M (2014) Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep 8(5):1583–1594

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank the European Research Council (ERC Starting Grant; Strp-differentiation 280304), the Spanish “Ministerio de Economía y Competitividad” (MINECO; BIO2015-65709-R), and the VILLUM Foundation (VILLUM Center for Bioanalytical Sciences at University of Southern Denmark) for financial support.

Author information

Authors and Affiliations

  1. Area de Microbiologia, Departamento de Biologia Funcional, Facultad de Medicina, IUOPA, Universidad de Oviedo, Oviedo, Spain

    Angel Manteca & Beatriz Rioseras

  2. Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark

    Adelina Rogowska-Wrzesinska & Ole N. Jensen

Authors
  1. Angel Manteca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beatriz Rioseras
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adelina Rogowska-Wrzesinska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ole N. Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angel Manteca .

Editor information

Editors and Affiliations

  1. Department of Microbial Proteomics, Institute for Microbiology, University Greifswald, Greifswald, Germany

    Dörte Becher

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Manteca, A., Rioseras, B., Rogowska-Wrzesinska, A., Jensen, O.N. (2018). Phosphoproteomics in Microbiology: Protocols for Studying Streptomyces coelicolor Differentiation. In: Becher, D. (eds) Microbial Proteomics. Methods in Molecular Biology, vol 1841. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8695-8_17

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-8695-8_17

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-8693-4

  • Online ISBN: 978-1-4939-8695-8

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation