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Russian Journal of Plant Physiology

, Volume 60, Issue 5, pp 589–596 | Cite as

Eukaryotic protein kinases in cyanobacteria

  • A. A. ZorinaEmail author
Reviews

Abstract

This review presents the data on the role of eukaryotic-like serine/threonine protein kinases in the members of various groups of cyanobacteria. Information is provided for the two most studied model species (Anabaena and Synechocystis), differing in their morphology and ecophysiological features, and covers the entire period of study of this group of enzymes in cyanobacteria.

Keywords

Anabaena sp. PCC 7120 Synechocystis sp. PCC 6803 serine/threonine protein kinases 

Abbreviations

STPK

Ser/Thr protein kinase(s)

STPP

Ser/Thr protein phosphatase(s)

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References

  1. 1.
    Whitton, B.A. and Potts, M., Introduction to the cyanobacteria, The Ecology of Cyanobacteria: Their Diversity in Time and Space, Whitton, B.A. and Potts, M., Eds., Dordrecht: Kluwer, 2000, pp. 1–13.Google Scholar
  2. 2.
    Rastogia, R.P. and Sinha, R.P., Biotechnological and industrial significance of cyanobacterial secondary metabolites, Biotech. Adv., 2009, vol. 27, pp. 521–539.CrossRefGoogle Scholar
  3. 3.
    Bendera, J. and Phillips, P., Microbial mats for multiple applications in aquaculture and bioremediation, Biores. Technol., 2004, vol. 94, pp. 229–238.CrossRefGoogle Scholar
  4. 4.
    Dismukes, G.C., Carrieri, D., Bennette, N., Ananyev, G.M., and Posewitz, M.C., Aquatic phototrophs: efficient alternatives to land-based crops for biofuels, Curr. Opin. Biotechnol., 2008, vol. 19, pp. 235–240.PubMedCrossRefGoogle Scholar
  5. 5.
    Mijakovic, I. and Macek, B., Impact of phosphoproteomics on studies of bacterial physiology, FEMS Microbiol. Rev., 2012, vol. 36, pp. 877–892.PubMedCrossRefGoogle Scholar
  6. 6.
    Mitrophanov, A.Y. and Groisman, E.A., Signal integration in bacterial two-component regulatory systems, Gene Dev., 2008, vol. 22, pp. 2601–2611.PubMedCrossRefGoogle Scholar
  7. 7.
    Wang, L., Sun, Y.P., Chen, W.L., Li, J.H., and Zhang, C.C., Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120, FEMS Microbiol. Letts., 2002, vol. 217, pp. 155–165.CrossRefGoogle Scholar
  8. 8.
    Ashby, M.K. and Houmard, J., Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution, Microbiol. Mol. Biol. Rev., 2006, vol. 70, pp. 472–509.PubMedCrossRefGoogle Scholar
  9. 9.
    Klumpp, S. and Krieglstein, J., Phosphorylation and dephosphorylation of histidine residues in proteins, Eur. J. Biochem., 2002, vol. 269, pp. 1067–1071.PubMedCrossRefGoogle Scholar
  10. 10.
    Mascher, T., Helmann, J.D., and Unden, G., Stimulus perception in bacterial signal-transducing histidine kinases, Microbiol. Mol. Biol. Rev., 2006, vol. 70, pp. 910–938.PubMedCrossRefGoogle Scholar
  11. 11.
    Muñoz-Dorado, J., Inouye, S., and Inouye, M., A gene encoding a protein serine/threonine kinase is required for normal development of Myxococcus xanthus, a gram-negative bacterium, Cell, 1991, vol. 67, pp. 995–1006.PubMedCrossRefGoogle Scholar
  12. 12.
    Wurgler-Murphy, S.M. and Saito, H., Two-component signal transducers and MAPK cascades, Trends Biochem. Sci., 1997, vol. 22, pp. 172–176.PubMedCrossRefGoogle Scholar
  13. 13.
    Kennelly, P.J., Protein kinases and protein phosphatases in prokaryotes: a genomic perspective, FEMS Microbiol. Lett., 2002, vol. 206, pp. 1–8.PubMedCrossRefGoogle Scholar
  14. 14.
    Molle, V. and Kremer, L., Division and cell envelope regulation by Ser/Thr phosphorylation: mycobacterium shows the way, Mol. Microbiol., 2010, vol. 75, pp. 1064–1077.PubMedCrossRefGoogle Scholar
  15. 15.
    Petříčková, K. and Petříček, M., Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme, Microbiology, 2003, vol. 149, pp. 1609–1621.PubMedCrossRefGoogle Scholar
  16. 16.
    Nariya, H. and Inouye, S., Identification of a protein Ser/Thr kinase cascade that regulates essential transcriptional activators in Myxococcus xanthus, Mol. Microbiol., 2005, vol. 58, pp. 367–379.PubMedCrossRefGoogle Scholar
  17. 17.
    Blattner, F.R., Plunkett, G.,III, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., Gregor, J., Davis, N.W., Kirkpatrick, H.A., Goeden, M.A., Rose, D.J., Mau, B., and Shao, Y., The complete genome sequence of Escherichia coli K-12, Science, 1997, vol. 277, pp. 1453–1474.PubMedCrossRefGoogle Scholar
  18. 18.
    Enami, M. and Ishihama, A., Protein phosphorylation in Escherichia coli and purification of a protein kinase, J. Biol. Chem., 1984, vol. 259, pp. 526–533.PubMedGoogle Scholar
  19. 19.
    Macek, B., Gnad, F., Soufi, B., Kumar, C., Olsen, J.V., Mijakovic, I., and Mann, M., Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation, Mol. Cell Proteom., 2008, vol. 7, pp. 299–307.CrossRefGoogle Scholar
  20. 20.
    Zheng, J., He, C., Singh, V.K., Martin, N.L., and Jia, Z., Crystal structure of a novel prokaryotic Ser/Thr kinase and its implication in the Cpx stress response pathway, Mol. Microbiol., 2007, vol. 63, pp. 1360–1371.PubMedCrossRefGoogle Scholar
  21. 21.
    Scheeff, E.D. and Bourne, P.E., Structural evolution of the protein kinase-like superfamily, PLoS Comput. Biol., 2005, vol. 1: e49.Google Scholar
  22. 22.
    Pérez, J., Castañeda-García, A., Jenke-Kodama, H., Müller, R., and Muñoz-Dorado, J., Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 15950–15955PubMedCrossRefGoogle Scholar
  23. 23.
    Zhang, C.C., A gene encoding a protein related to eukaryotic protein kinases from the filamentous heterocystous cyanobacterium Anabaena PCC 7120, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 11840–11844.PubMedCrossRefGoogle Scholar
  24. 24.
    Zhang, X., Zhao, F., Guan, X., Yang, Y., Liang, C., and Qin, S., Genome-wide survey of putative serine/threonine protein kinases in cyanobacteria, BMC Genom., 2007, vol. 8, p. 395.CrossRefGoogle Scholar
  25. 25.
    Galperin, M.Y., A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts, BMC Microbiol., 2005, vol. 5, pp. 35–55.PubMedCrossRefGoogle Scholar
  26. 26.
    Ohmori, M., Ikeuchi, M., Sato, N., Wolk, P., Kaneko, T., Ogawa, T., Kanehisa, M., Goto, S., Kawashima, S., Okamoto, S., Yoshimura, H., Katoh, H., Fujisawa, T., Ehira, S., Kamei, A., Yoshihara, S., Narikawa, R., and Tabata, S., Characterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120, DNA Res., 2001, vol. 8, pp. 271–284.PubMedCrossRefGoogle Scholar
  27. 27.
    Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M., and Tabata, S., Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803: 2. Sequence determination of the entire genome and assignment of potential protein-coding regions, DNA Res., 1996, vol. 3, pp. 109–136.PubMedCrossRefGoogle Scholar
  28. 28.
    Kaneko, T., Nakamura, Y., Sasamoto, S., Watanabe, A., Kohara, M., Matsumoto, M., Shimpo, S., Yamada, M., and Tabata, S., Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803, DNA Res., 2003, vol. 10, pp. 221–228.PubMedCrossRefGoogle Scholar
  29. 29.
    Hanks, S.K. and Hunter, T., Protein kinases. 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification, J. FASEB, 1995, vol. 9, pp. 576–596.Google Scholar
  30. 30.
    Akamine, P., Madhusudan, Wu J., Xuong, N.-H., Ten, Eyck, L.F., and Taylor, S.S., Dynamic features of camp-dependent protein kinase revealed by apoenzyme crystal structure, J. Mol. Biol., 2003, vol. 327, pp. 159–171.PubMedCrossRefGoogle Scholar
  31. 31.
    Kannan, N., Taylor, S.S., Zhai, Y., Venter, C.J., and Manning, G., Structural and functional diversity of the microbial kinome, PLoS Biol., 2007, vol. 5: e17.PubMedCrossRefGoogle Scholar
  32. 32.
    Zhang, C.C., Gonzalez, L., and Phalip, V., Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome, Nucleic Acids Res., 1998, vol. 26, pp. 3619–3625.PubMedCrossRefGoogle Scholar
  33. 33.
    Taylor, S.S. and Kornev, A.P., Protein kinases: evolution of dynamic regulatory proteins, Trends Biochem. Sci., 2011, vol. 36, pp. 65–77.PubMedCrossRefGoogle Scholar
  34. 34.
    Krupa, A. and Srinivasan, N., Diversity in domain architectures of Ser/Thr kinases and their homologues in prokaryotes, BMC Genom., 2005, vol. 6, p. 129.CrossRefGoogle Scholar
  35. 35.
    Phalip, V., Li, J.H., and Zhang, C.C., Hstk, a cyanobacterial protein with both a serine/threonine kinase domain and a histidine kinase domain: implication for the mechanism of signal transduction, J. Biochem., 2001, vol. 360, pp. 639–644.CrossRefGoogle Scholar
  36. 36.
    Pereira, S.F.F., Goss, L., and Dworkin, J., Eukaryotelike serine/threonine kinases and phosphatases in bacteria, Microbiol. Mol. Biol. Rev., 2011, vol. 75, pp. 192–212.PubMedCrossRefGoogle Scholar
  37. 37.
    Molle, V., Kremer, L., Girard-Blanc, C., Besra, G.S., Cozzone, A.J., and Prost, J.-F., An FHA phosphoprotein recognition domain mediates protein Embr phosphorylation by Pknh, a Ser/Thr protein kinase from Mycobacterium tuberculosis, Biochemistry, 2003, vol. 42, pp. 15300–15309.PubMedCrossRefGoogle Scholar
  38. 38.
    Curry, J.M., Whalan, R., Hunt, D.M., Gohil, K., Strom, M., Rickman, L., Colston, M.J., Smerdon, S.J., and Buxton, R.S., An ABC transporter containing a forkhead-associated domain interacts with a serine- threonine protein kinase and is required for growth of Mycobacterium tuberculosis in mice, Infect. Immun., 2005, vol. 73, pp. 4471–4477.PubMedCrossRefGoogle Scholar
  39. 39.
    Canova, M.J., Veyron-Churlet, R., Zanella-Cleon, I., Cohen-Gonsaud, M., Cozzone, J.A., Becchi, M., Kremer, L., and Molle, V., The Mycobacterium tuberculosis serine/threonine kinase Pknl phosphorylates Rv2175c: mass spectrometric profiling of the activation loop phosphorylation sites and their role in the recruitment of Rv2175c, Proteomics, 2008, vol. 8, pp. 521–533.PubMedCrossRefGoogle Scholar
  40. 40.
    Absalon, C., Obuchowski, M., Madec, E., Delattre, D., Holland, I.B., and Séror, S.J., CpgA, EF-Tu and the stressosome protein Yezb are substrates of the Ser/Thr kinase/phosphatase couple, PrkC/PrpC, in Bacillus subtilis, Microbiology, 2009, vol. 155, pp. 932–943.PubMedCrossRefGoogle Scholar
  41. 41.
    Kennelly, P.J. and Potts, M., Fancy meeting you here! A fresh look at “prokaryotic” protein phosphorylation, J. Bacteriol., 1996, vol. 178, pp. 4759–4764.PubMedGoogle Scholar
  42. 42.
    Zhang, C.C. and Libs, L., Cloning and characterization of the pknD gene encoding an eukaryotic-type protein kinase in the cyanobacterium Anabaena sp. PCC 7120, Mol. Gen. Genet., 1998, vol. 258, pp. 26–33.PubMedCrossRefGoogle Scholar
  43. 43.
    Xu, W.L., Jeanjean, R., Liu, Y.D., and Zhang, C.C., pkn22 (alr2502) encoding a putative Ser/Thr kinase in the cyanobacteium Anabaena sp. PCC7120 is induced by both iron starvation and oxidative stress and regulates the expression of isiA, FEBS Lett., 2003, vol. 553, pp. 179–182.PubMedCrossRefGoogle Scholar
  44. 44.
    Gonzalez, L., Phalip, V., and Zhang, C.C., Characterization of PknC, a Ser/Thr kinase with broad substrate specificity from the cyanobacterium Anabaena sp. strain PCC 7120, Eur. J. Biochem., 2001, vol. 268, pp. 1869–1875.PubMedCrossRefGoogle Scholar
  45. 45.
    Cheng, Y., Li, J.-H., Shi, L., Wang, L., Latifi, A., and Zhang, C.C., A pair of iron-responsive genes encoding protein kinases with a Ser/Thr kinase domain and a His kinase domain are regulated by Ntca in the cyanobacterium Anabaena sp. strain PCC 7120, J. Bacteriol., 2006, vol. 188, pp. 4822–4829.PubMedCrossRefGoogle Scholar
  46. 46.
    Wei, T.F., Ramasubramanian, T.S., and Golden, J.W., Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development, J. Bacteriol., 1994, vol. 176, pp. 4473–4482.PubMedGoogle Scholar
  47. 47.
    Kumar, K., Mella-Herrera, R.A., and Golden, J.W., Cyanobacterial heterocysts, Cold Spring Harb. Perspect., Biol., 2010, vol. 2: a000315.CrossRefGoogle Scholar
  48. 48.
    Shi, L., Li, J.H., Cheng, Y., Wang, L., Chen, W.L., and Zhang, C.C., Two genes encoding protein kinases of the Hstk family are involved in synthesis of the minor heterocyst-specific glycolipid in the cyanobacterium Anabaena sp. strain PCC 7120, J. Bacteriol., 2007, vol. 189, pp. 5075–5081.PubMedCrossRefGoogle Scholar
  49. 49.
    Tom, S.K. and Callahan, S.M., The putative phosphatase All1758 is necessary for normal growth, cell size and synthesis of the minor heterocyst-specific glycolipid in the cyanobacterium Anabaena sp. strain PCC 7120, Microbiology, 2012, vol. 158, pp. 380–389.PubMedCrossRefGoogle Scholar
  50. 50.
    Jang, J., Wang, L., Jeanjean, R., and Zhang, C.C., PrpJ, a PP2C-type protein phosphatase located on the plasma membrane, is involved in heterocyst maturation in the cyanobacterium Anabaena sp. PCC 7120, Mol. Microbiol., 2007, vol. 64, pp. 347–358.PubMedCrossRefGoogle Scholar
  51. 51.
    Lechno-Yossef, S., Fan, Q., Ehira, S., Sato, N., and Wolk, C.P., Mutations in four regulatory genes have interrelated effects on heterocyst maturation in Anabaena sp. strain PCC 7120, J. Bacteriol., 2006, vol. 188, pp. 7387–7395.PubMedCrossRefGoogle Scholar
  52. 52.
    Ehira, S. and Ohmori, M., NrrA, a nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120, Mol. Microbiol., 2006, vol. 59, pp. 1692–1703.PubMedCrossRefGoogle Scholar
  53. 53.
    Saha, S.K. and Golden, J.W., Overexpression of pknE blocks heterocyst development in Anabaena sp. strain PCC 7120, J. Bacteriol., 2011, vol. 193, pp. 2619–2629.PubMedCrossRefGoogle Scholar
  54. 54.
    Zhang, C.C., Friry, A. and Peng, L., Molecular and genetic analysis of two closely linked genes that encode, respectively, a protein phosphatase 1/2A/2B homolog and a protein kinase homolog in the cyanobacterium Anabaena sp. strain PCC 7120, J. Bacteriol., 1998, vol. 180, pp. 2616–2622.PubMedGoogle Scholar
  55. 55.
    Ehira, S. and Ohmori, M., The pknH gene restrictively expressed in heterocysts is required for diazotrophic growth in the cyanobacterium Anabaena sp. strain PCC 7120, Microbiology, 2012, vol. 158, pp. 1437–1443.PubMedCrossRefGoogle Scholar
  56. 56.
    Espinosa, J., Brunner, T., Fiedler, N., Forchhammer, K., Muro-Pastor, A.M., and Maldener, I., DevT (Alr4674), resembling a Ser/Thr protein phosphatase, is essential for heterocyst function in the cyanobacterium Anabaena sp. PCC 7120, Microbiology, 2010, vol. 156, pp. 3544–3555.PubMedCrossRefGoogle Scholar
  57. 57.
    Kamei, A., Yuasa, T., Orikawa, K., Geng, X., and Ikeuchi, M., A eukaryotic-type protein kinase, SpkA, is required for normal motility of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803, J. Bacteriol., 2001, vol. 183, pp. 1505–1510.PubMedCrossRefGoogle Scholar
  58. 58.
    Kamei, A., Yoshihara, S., Yuasa, T., Geng, X., and Ikeuchi, M., Biochemical and functional characterization of a eukaryotic-type protein kinase, SpkB, in the cyanobacterium, Synechocystis sp. PCC 6803, Curr. Microbiol., 2003, vol. 46, pp. 296–301.PubMedCrossRefGoogle Scholar
  59. 59.
    Panichkin, V.B., Arakawa-Kobayashi, S., Kanaseki, T., Suzuki, I., Los, D.A., Shestakov, S.V., and Murata, N., Serine/threonine protein kinase SpkA in Synechocystis sp. strain PCC 6803 is a regulator of expression of three putative pilA operons, formation of thick Pili, and cell motility, J. Bacteriol., 2006, vol. 188, pp. 7696–7699.PubMedCrossRefGoogle Scholar
  60. 60.
    Galkin, A.N., Mikheeva, L.E., and Shestakov, S.V., The insertional inactivation of genes encoding eukaryotic-type serine/threonine protein kinases in the cyanobacterium Synechocystis sp. PCC 6803, Mikrobiology (Moscow), 2003, no. 72, pp. 52–57.Google Scholar
  61. 61.
    Laurent, S., Jang, J., Janicki, A., Zhang, C.C., and Bédu, S., Inactivaton of spkD, encoding a Ser/Thr kinase, affects the pool of the TCA cycle metabolites in Synechocyctis sp. strain PCC 6803, Microbiology, 2008, vol. 154, pp. 2161–2167.PubMedCrossRefGoogle Scholar
  62. 62.
    Zorina, A., Stepanchenko, N., Novikova, G.V., Sinetova, M., Panichkin, V.B., Moshkov, I.E., Zinchenko, V.V., Shestakov, S.V., Suzuki, I., Murata, N., and Los, D.A., Eukaryotic-like Ser/Thr protein kinases SpkC/F/K are involved in phosphorylation of GroES in the cyanobacterium Synechocystis, DNA Res., 2011, vol. 18, pp. 137–151.PubMedCrossRefGoogle Scholar
  63. 63.
    Mata-Cabana, A., García-Domínguez, M., Florencio, F.J., and Lindahl, M., Thiol-based redox modulation of a cyanobacterial eukaryotic-type serine/threonine kinase required for oxidative stress tolerance, Antiox. Redox Signal., 2012, vol. 17, pp. 521–533.CrossRefGoogle Scholar
  64. 64.
    Kamei, A., Yuasa, T., Geng, X., and Ikeuchi, M., Biochemical examination of the potential eukaryotic-type protein kinase genes in the complete genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803, DNA Res., 2002, vol. 9, pp. 71–78.PubMedCrossRefGoogle Scholar
  65. 65.
    Wegener, K.M., Welsh, E.A., Thornton, L.E., Keren, N., Jacobs, J.M., Hixson, K.K., Monroe, M.E., Camp, D.G., Smith, R.D., and Pakrasi, H.B., High sensitivity proteomics assisted discovery of a novel operon involved in the assembly of photosystem II, a membrane protein complex, J. Biol. Chem., 2008, vol. 283, pp. 27829–27837.PubMedCrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

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