Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 2001 Dec 15;360(Pt 3):639–644. doi: 10.1042/0264-6021:3600639

HstK, a cyanobacterial protein with both a serine/threonine kinase domain and a histidine kinase domain: implication for the mechanism of signal transduction.

V Phalip 1, J H Li 1, C C Zhang 1
PMCID: PMC1222267  PMID: 11736654

Abstract

Two distinct families of protein kinases are involved in signal transduction: Ser, Thr and Tyr kinases, which are predominantly found among eukaryotes, and His kinases, as part of bacterial two-component signalling systems. Genetic studies in Arabidopsis and Saccharomyces have demonstrated that bacterial-type two-component systems may act upstream of Ser/Thr kinases in the same signalling pathway, but how this coupling is accomplished remains unclear. In the present study, we report the characterization of a protein kinase, HstK, from the N(2)-fixing cyanobacterium Anabaena sp. PCC 7120, that possesses both a Ser/Thr kinase domain and a His kinase domain. Proteins with a structural architecture similar to that of HstK can be found in the eukaryote, Schizosaccharomyces pombe, and the bacterium, Rhodococcus sp. M5. HstK was present in cells grown with NH(4)(+) or N(2) as the nitrogen source, but was absent in cells grown with NO(3)(-). The hstK gene was inactivated and the mutant phenotype was characterized. The catalytic domain of the Ser/Thr kinase of HstK functionally replaced that of Hog1p, a well-characterized protein kinase required for the response to high osmolarity in the S. cerevisiae heterologous system. The unusual multidomain structure of HstK suggests that a two-component system could be directly coupled to Ser/Thr kinases in the same signal transduction pathway.

Full Text

The Full Text of this article is available as a PDF (207.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appleby J. L., Parkinson J. S., Bourret R. B. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell. 1996 Sep 20;86(6):845–848. doi: 10.1016/s0092-8674(00)80158-0. [DOI] [PubMed] [Google Scholar]
  2. Aravind L., Ponting C. P. The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci. 1997 Dec;22(12):458–459. doi: 10.1016/s0968-0004(97)01148-1. [DOI] [PubMed] [Google Scholar]
  3. Bonneaud N., Ozier-Kalogeropoulos O., Li G. Y., Labouesse M., Minvielle-Sebastia L., Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast. 1991 Aug-Sep;7(6):609–615. doi: 10.1002/yea.320070609. [DOI] [PubMed] [Google Scholar]
  4. Cairns B. R., Ramer S. W., Kornberg R. D. Order of action of components in the yeast pheromone response pathway revealed with a dominant allele of the STE11 kinase and the multiple phosphorylation of the STE7 kinase. Genes Dev. 1992 Jul;6(7):1305–1318. doi: 10.1101/gad.6.7.1305. [DOI] [PubMed] [Google Scholar]
  5. Chalfie M., Tu Y., Euskirchen G., Ward W. W., Prasher D. C. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–805. doi: 10.1126/science.8303295. [DOI] [PubMed] [Google Scholar]
  6. Chang C., Kwok S. F., Bleecker A. B., Meyerowitz E. M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. doi: 10.1126/science.8211181. [DOI] [PubMed] [Google Scholar]
  7. Clark K. L., Larsen P. B., Wang X., Chang C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5401–5406. doi: 10.1073/pnas.95.9.5401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. David M., Daveran M. L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell. 1988 Aug 26;54(5):671–683. doi: 10.1016/s0092-8674(88)80012-6. [DOI] [PubMed] [Google Scholar]
  9. Elhai J., Wolk C. P. Conjugal transfer of DNA to cyanobacteria. Methods Enzymol. 1988;167:747–754. doi: 10.1016/0076-6879(88)67086-8. [DOI] [PubMed] [Google Scholar]
  10. Gonzalez L., Phalip V., 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 Mar;268(6):1869–1875. [PubMed] [Google Scholar]
  11. Gustin M. C., Albertyn J., Alexander M., Davenport K. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1998 Dec;62(4):1264–1300. doi: 10.1128/mmbr.62.4.1264-1300.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanks S. K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 1995 May;9(8):576–596. [PubMed] [Google Scholar]
  13. Ho Y. S., Burden L. M., Hurley J. H. Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor. EMBO J. 2000 Oct 16;19(20):5288–5299. doi: 10.1093/emboj/19.20.5288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell. 1995 Jan 27;80(2):225–236. doi: 10.1016/0092-8674(95)90405-0. [DOI] [PubMed] [Google Scholar]
  15. Jiang J., Gu B. H., Albright L. M., Nixon B. T. Conservation between coding and regulatory elements of Rhizobium meliloti and Rhizobium leguminosarum dct genes. J Bacteriol. 1989 Oct;171(10):5244–5253. doi: 10.1128/jb.171.10.5244-5253.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996 Jun 30;3(3):109–136. doi: 10.1093/dnares/3.3.109. [DOI] [PubMed] [Google Scholar]
  17. Kieber J. J., Rothenberg M., Roman G., Feldmann K. A., Ecker J. R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 Feb 12;72(3):427–441. doi: 10.1016/0092-8674(93)90119-b. [DOI] [PubMed] [Google Scholar]
  18. Labbé D., Garnon J., Lau P. C. Characterization of the genes encoding a receptor-like histidine kinase and a cognate response regulator from a biphenyl/polychlorobiphenyl-degrading bacterium, Rhodococcus sp. strain M5. J Bacteriol. 1997 Apr;179(8):2772–2776. doi: 10.1128/jb.179.8.2772-2776.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maeda T., Wurgler-Murphy S. M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. doi: 10.1038/369242a0. [DOI] [PubMed] [Google Scholar]
  20. Mizuno T., Kaneko T., Tabata S. Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res. 1996 Dec 31;3(6):407–414. doi: 10.1093/dnares/3.6.407. [DOI] [PubMed] [Google Scholar]
  21. Muñoz-Dorado J., Inouye S., Inouye M. A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell. 1991 Nov 29;67(5):995–1006. doi: 10.1016/0092-8674(91)90372-6. [DOI] [PubMed] [Google Scholar]
  22. Phalip V., Kuhn I., Lemoine Y., Jeltsch J. M. Characterization of the biotin biosynthesis pathway in Saccharomyces cerevisiae and evidence for a cluster containing BIO5, a novel gene involved in vitamer uptake. Gene. 1999 May 17;232(1):43–51. doi: 10.1016/s0378-1119(99)00117-1. [DOI] [PubMed] [Google Scholar]
  23. Posas F., Wurgler-Murphy S. M., Maeda T., Witten E. A., Thai T. C., Saito H. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell. 1996 Sep 20;86(6):865–875. doi: 10.1016/s0092-8674(00)80162-2. [DOI] [PubMed] [Google Scholar]
  24. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  25. Schüller C., Brewster J. L., Alexander M. R., Gustin M. C., Ruis H. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 1994 Sep 15;13(18):4382–4389. doi: 10.1002/j.1460-2075.1994.tb06758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shi L., Potts M., Kennelly P. J. The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol Rev. 1998 Oct;22(4):229–253. doi: 10.1111/j.1574-6976.1998.tb00369.x. [DOI] [PubMed] [Google Scholar]
  27. Smith J. A., Francis S. H., Corbin J. D. Autophosphorylation: a salient feature of protein kinases. Mol Cell Biochem. 1993 Nov;127-128:51–70. doi: 10.1007/BF01076757. [DOI] [PubMed] [Google Scholar]
  28. Stock A. M., Robinson V. L., Goudreau P. N. Two-component signal transduction. Annu Rev Biochem. 2000;69:183–215. doi: 10.1146/annurev.biochem.69.1.183. [DOI] [PubMed] [Google Scholar]
  29. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  30. Thomason P. A., Traynor D., Cavet G., Chang W. T., Harwood A. J., Kay R. R. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J. 1998 May 15;17(10):2838–2845. doi: 10.1093/emboj/17.10.2838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wolk C. P. Heterocyst formation. Annu Rev Genet. 1996;30:59–78. doi: 10.1146/annurev.genet.30.1.59. [DOI] [PubMed] [Google Scholar]
  32. Wurgler-Murphy S. M., Saito H. Two-component signal transducers and MAPK cascades. Trends Biochem Sci. 1997 May;22(5):172–176. doi: 10.1016/s0968-0004(97)01036-0. [DOI] [PubMed] [Google Scholar]
  33. 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 U S A. 1993 Dec 15;90(24):11840–11844. doi: 10.1073/pnas.90.24.11840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zhang C. C. Bacterial signalling involving eukaryotic-type protein kinases. Mol Microbiol. 1996 Apr;20(1):9–15. doi: 10.1111/j.1365-2958.1996.tb02483.x. [DOI] [PubMed] [Google Scholar]
  35. Zhang C. C., Friry A., 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 May;180(10):2616–2622. doi: 10.1128/jb.180.10.2616-2622.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zhang C. C., Gonzalez L., Phalip V. Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res. 1998 Aug 15;26(16):3619–3625. doi: 10.1093/nar/26.16.3619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zhang C. C., Libs L. Cloning and characterisation of the pknD gene encoding an eukaryotic-type protein kinase in the cyanobacterium Anabaena sp. PCC7120. Mol Gen Genet. 1998 Apr;258(1-2):26–33. doi: 10.1007/s004380050703. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES