1887

Abstract

Inspection of the genomes of A3(2) and reveals that each contains 55 putative eukaryotic-type protein phosphatases (PPs), the largest number ever identified from any single prokaryotic organism. Unlike most other prokaryotic genomes that have only one or two superfamilies of eukaryotic-type PPs, the streptomycete genomes possess the eukaryotic-type PPs that belong to four superfamilies: 2 phosphoprotein phosphatases and 2 low-molecular-mass protein tyrosine phosphatases in each species, 49 Mg- or Mn-dependent protein phosphatases (PPMs) and 2 conventional protein tyrosine phosphatases (CPTPs) in A3(2), and 48 PPMs and 3 CPTPs in . Sixty-four percent of the PPs found in A3(2) have orthologues in , indicating that they originated from a common ancestor and might be involved in the regulation of more conserved metabolic activities. The genes of eukaryotic-type PP unique to each surveyed streptomycete genome are mainly located in two arms of the linear chromosomes and their evolution might be involved in gene acquisition or duplication to adapt to the extremely variable soil environments where these organisms live. In addition, 56 % of the PPs from A3(2) and 65 % of the PPs from possess at least one additional domain having a putative biological function. These include the domains involved in the detection of redox potential, the binding of cyclic nucleotides, mRNA, DNA and ATP, and the catalysis of phosphorylation reactions. Because they contained multiple functional domains, most of them were assigned functions other than PPs in previous annotations. Although few studies have been conducted on the physiological functions of the PPs in streptomycetes, the existence of large numbers of putative PPs in these two streptomycete genomes strongly suggests that eukaryotic-type PPs play important regulatory roles in primary or secondary metabolic pathways. The identification and analysis of such a large number of putative eukaryotic-type PPs from A3(2) and constitute a basis for further exploration of the signal transduction pathways mediated by these phosphatases in industrially important strains of streptomycetes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27057-0
2004-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/7/mic1502247.html?itemId=/content/journal/micro/10.1099/mic.0.27057-0&mimeType=html&fmt=ahah

References

  1. Bentley S. D., Chater K. F., Cerdeno-Tarraga A. M.40 other authors 2002; Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147 [CrossRef]
    [Google Scholar]
  2. Beuf L., Brown N. P., Hegyi H., Schultz J. 1994; A protein involved in co-ordinated regulation of inorganic carbon and glucose metabolism in the facultative photoautotrophic cyanobacterium Synechocystis PCC 6803. Plant Mol Biol 25:855–864 [CrossRef]
    [Google Scholar]
  3. Bliska J. B., Guan K. L., Dixon J. E., Falkow S. 1991; Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc Natl Acad Sci U S A 88:1187–1191 [CrossRef]
    [Google Scholar]
  4. Boitel B., Ortiz-Lombardia M., Duran R., Pompeo F., Cole S. T., Cervenansky C., Alzari P. M. 2003; PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol Microbiol 49:1493–1508 [CrossRef]
    [Google Scholar]
  5. Bork P., Brown N. P., Hegyi H., Schultz J. 1996; The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci 5:1421–1425 [CrossRef]
    [Google Scholar]
  6. Bretz J. R., Mockm N. M., Charity J. C., Zeyad S., Baker C. J., Hutcheson S. W. 2003; A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defense response to infection. Mol Microbiol 49:389–400 [CrossRef]
    [Google Scholar]
  7. Chater K. F. 1993; Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47:683–713
    [Google Scholar]
  8. Cohen P. 1989; The structure and regulation of protein phosphatases. Annu Rev Biochem 58:453–508 [CrossRef]
    [Google Scholar]
  9. Cohen P. T. W. 1994; Nomenclature and chromosomal localization of human protein serine/threonine phosphatase genes. Adv Protein Phosphatases 8:371–376
    [Google Scholar]
  10. Cohen P. T. W., Cohen P. 1989; Discovery of a protein phosphatase activity encoded in the genome of bacteriophage lambda. Probable identity with open reading frame 221. Biochem J 260:931–934
    [Google Scholar]
  11. Cozzone A. J. 1988; Protein phosphorylation in prokaryotes. Annu Rev Microbiol 42:97–125 [CrossRef]
    [Google Scholar]
  12. Duncan L., Alper S., Arigoni F., Losick R., Stragier P. 1995; Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division. Science 270:641–644 [CrossRef]
    [Google Scholar]
  13. Espinosa A., Guo M., Tam V. C., Fu Z. Q., Alfano J. R. 2003; The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol Microbiol 49:377–387 [CrossRef]
    [Google Scholar]
  14. Galyov E. E., Hakansson S., Forsberg A., Wolf-Watz H. 1993; A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361:730–732 [CrossRef]
    [Google Scholar]
  15. Grangeasse C., Doublet P., Vincent C., Vaganay E., Riberty M., Duclos B., Cozzone A. J. 1998; Functional characterization of the low-molecular-mass phosphotyrosine-protein phosphatase of Acinetobacter johnsonii. J Mol Biol 278:339–347 [CrossRef]
    [Google Scholar]
  16. Ho Y. S., Burden L. M., Hurley J. H. 2000; Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor. EMBO J 19:5288–5299 [CrossRef]
    [Google Scholar]
  17. Hodgson D. A. 2000; Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238
    [Google Scholar]
  18. Hopwood D. A. 1999; Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico. Microbiology 145:2183–2202
    [Google Scholar]
  19. Horinouchi S. 2003; AfsR as an integrator of signals that are sensed by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). J Ind Microbiol Biotechnol 20:462–467
    [Google Scholar]
  20. Ikeda H., Ishikawa J., Hanamoto K. & 7 other authors; 2003; Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nature Biotechnol 21:526–531 [CrossRef]
    [Google Scholar]
  21. Irmler A., Forchhammer K. 2001; A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. Proc Natl Acad Sci U S A 98:12978–12983 [CrossRef]
    [Google Scholar]
  22. Iwanicki A., Herman-Antosiewicz A., Pierchod M., Seror S. J., Obuchowski M. 2002; PrpE, a PPP protein phosphatase from Bacillus subtilis with unusual substrate specificity. Biochem J 366:929–936
    [Google Scholar]
  23. Jackson M. D., Denu J. M. 2001; Molecular reactions of protein phosphatases – insights from structure and chemistry. Chem Rev 101:2313–2340 [CrossRef]
    [Google Scholar]
  24. Kaniga K., Uralil J., Bliska J. B., Galan J. E. 1996; A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol Microbiol 21:633–641 [CrossRef]
    [Google Scholar]
  25. Kennelly P. J. 2002; Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol Lett 206:1–8 [CrossRef]
    [Google Scholar]
  26. Koul A., Choidas A., Treder M., Tyagi A. K., Drlica K., Singh Y., Ullrich A. 2000; Cloning and characterization of secretory tyrosine phosphatases of Mycobacterium tuberculosis. J Bacteriol 182:5425–5432 [CrossRef]
    [Google Scholar]
  27. Leng J., Cameron A. J. M., Buckel S., Kennelly P. J. 1995; Isolation and cloning a protein-serine/threonine phosphatase from an archaeon. J Bacteriol 177:6510–6517
    [Google Scholar]
  28. Li Y., Strohl W. R. 1996; Cloning, purification, and properties of a phosphotyrosine protein phosphatase from Streptomyces coelicolor A3(2). J Bacteriol 178:136–142
    [Google Scholar]
  29. Mai B., Frey G., Swanson R. V., Mathur E. J., Stetter K. O. 1998; Molecular cloning and functional expression of a protein-serine/threonine phosphatase from the hyperthermophilic archaeon Pyrodictium abyssi TAG11. J Bacteriol 180:4030–4035
    [Google Scholar]
  30. Marchler-Bauer A., Anderson J. B., DeWeese-Scott C. & 24 other authors; 2003; CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387 [CrossRef]
    [Google Scholar]
  31. Missiakas D., Raina S. 1997; Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli: role of two new phosphoprotein phosphatases PrpA and PrpB. EMBO J 16:1670–1685 [CrossRef]
    [Google Scholar]
  32. Mukhopadhyay S., Kapatral V., Xu W., Chakrabarty A. M. 1999; Characterization of a Hank's type serine/threonine kinase and serine/threonine phosphoprotein phosphatase in Pseudomonas aeruginosa. J Bacteriol 181:6615–6622
    [Google Scholar]
  33. Nádvorník R., Vomastek T., Janecek J., Branny P., Techniková Z. 1999; Pkg2, a novel transmembrane protein Ser/Thr kinase of Streptomyces granaticolor. J Bacteriol 181:15–23
    [Google Scholar]
  34. Obuchowski M., Madec E., Delattre D., Boel G., Iwanicki A., Foulger D., Seror S. J. 2000; Characterization of PrpC from Bacillus subtilis, a member of the PPM phosphatase family. J Bacteriol 182:5634–5638 [CrossRef]
    [Google Scholar]
  35. Petrickova K., Petricek M. 2003; Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme. Microbiology 149:1609–1621 [CrossRef]
    [Google Scholar]
  36. Potts M., Sun H., Mockaitis K., Kennelly P. J., Reed D., Tonks N. K. 1993; A protein-tyrosine/serine phosphatase encoded by the genome of the cyanobacterium Nostoc commune UTEX 584. J Biol Chem 268:7632–7635
    [Google Scholar]
  37. Preneta R., Jarraud S., Vincent C., Doublet P., Duclos B., Etienne J., Cozzone A. J. 2002; Isolation and characterization of a protein-tyrosine kinase and a phosphotyrosine-protein phosphatase from Klebsiella pneumoniae. Comp Biochem Physiol B Biochem Mol Biol 131:103–112 [CrossRef]
    [Google Scholar]
  38. Rajagopal L., Clancy A., Ruhens C. E. 2003; A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylates an inorganic pyrophosphatase and affects growth, cell segregation, and virulence. J Biol Chem 278:14429–14441 [CrossRef]
    [Google Scholar]
  39. Redenbach M., Ikeda K., Yamasaki M., Kinashi H. 1998; Cloning and physical mapping of the EcoRI fragments of the giant linear plasmid SCP1. J Bacteriol 180:2796–2799
    [Google Scholar]
  40. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  41. Shi L. 2004; Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions. Front Biosci 9:1382–1397 [CrossRef]
    [Google Scholar]
  42. Shi L., Carmichael W. W. 1997; pp1-cyano2, a protein serine/threonine phosphatase 1 gene from the cyanobacterium Microcystis aeruginosa UTEX 2063. Arch Microbiol 168:528–531 [CrossRef]
    [Google Scholar]
  43. Shi L., Potts M., Kennelly P. J. 1998; The serine threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol Rev 22:229–253 [CrossRef]
    [Google Scholar]
  44. Shi L., Bischoff K. M., Kennelly P. J. 1999a; The icfG gene cluster of Synechocystis sp. strain PCC 6803 encodes an Rsb/Spo-like protein kinase, protein phosphatase, and two phosphoproteins. J Bacteriol 181:4761–4767
    [Google Scholar]
  45. Shi L., Carmichael W. W., Kennelly P. J. 1999b; Cyanobacterial PPP-family protein phosphatases possess multifunctional capabilities and are resistant to microcystin-LR. J Biol Chem 274:10039–10046 [CrossRef]
    [Google Scholar]
  46. Shi L., Kehres D. G., Maguire M. E. 2001; The PPP-family protein phosphatases PrpA and PrpB of Salmonella enterica serovar Typhimurium possess distinct biochemical properties. J Bacteriol 183:7053–7057 [CrossRef]
    [Google Scholar]
  47. Shu C. J., Zhulin I. B. 2002; ANTAR: an RNA-binding domain in transcription antitermination regulatory proteins. Trends Biochem Sci 27:3–5 [CrossRef]
    [Google Scholar]
  48. Solow B., Young J. C., Kennelly P. J. 1997; Gene cloning and expression and characterization of toxin-sensitive protein phosphatase from methanogenic archaeon Methanosarcina thermophila TM-1. J Bacteriol 179:5072–5075
    [Google Scholar]
  49. Soulat D., Vaganay E., Duclos B., Genestier A. L., Etienne J., Cozzone A. J. 2002; Staphylococcus aureus contains two low-molecular-mass phosphotyrosine protein phosphatases. J Bacteriol 184:5194–5199 [CrossRef]
    [Google Scholar]
  50. Stock A. M., Robinson V. L., Goudreau P. N. 2000; Two-component signal transduction. Annu Rev Biochem 69:183–215 [CrossRef]
    [Google Scholar]
  51. Taylor B. L., Zhulin I. B. 1999; PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506
    [Google Scholar]
  52. Treuner-Lange A., Ward M. J., Zusman D. R. 2001; Pph1 from Myxococcus xanthus is a protein phosphatase involved in vegetative growth and development. Mol Microbiol 40:126–140 [CrossRef]
    [Google Scholar]
  53. Ueda K., Miyake K., Horinouchi S., Beppu T. 1993; A gene cluster involved in aerial mycelium formation in Streptomyces griseus encodes proteins similar to the response regulators of two-component regulatory systems and membrane translocators. J Bacteriol 175:2006–2016
    [Google Scholar]
  54. Umeyama T., Tanabe Y., Aigle B. D., Horinouchi S. 1996; Expression of the Streptomyces coelicolor A3(2) ptpA gene encoding a phosphotyrosine protein phosphatase leads to overproduction of secondary metabolites in S. lividans. FEMS Microbiol Lett 144:177–184 [CrossRef]
    [Google Scholar]
  55. Umeyama T., Naruka A., Horinouchi S. 2000; Genetic and biochemical characterization of protein phosphatase with dual substrate specificity in Streptomyces coelicolor A3(2). . Gene 258:55–62 [CrossRef]
    [Google Scholar]
  56. Umeyama T., Lee P. C., Horinouchi S. 2002; Protein serine/threonine kinases in signal transduction for secondary metabolism and morphogenesis in Streptomyces. Appl Microbiol Biotechnol 59:419–425 [CrossRef]
    [Google Scholar]
  57. Vijay K., Brody M. S., Fredlund E., Price C. W. 2000; A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the σB transcription factor of Bacillus subtilis. Mol Microbiol 35:180–188 [CrossRef]
    [Google Scholar]
  58. Vincent C., Doublet P., Grangeasse C., Vaganay E., Cozzone A. J., Duclos B. 1999; Cells of Escherichia coli contain a protein-tyrosine kinase, Wzc, and a phosphotyrosine-protein phosphatase. Wzb. J Bacteriol 181:3472–3477
    [Google Scholar]
  59. Wang L., Sun Y.-P., Chen W.-L., Li J.-H., Zhang C. C. 2002; Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol Lett 217:155–165 [CrossRef]
    [Google Scholar]
  60. Wugeditsch T., Paiment A., Hocking J., Drummelsmith J., Forrester C., Whitfield C. 2001; Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J Biol Chem 276:2361–2371 [CrossRef]
    [Google Scholar]
  61. Yang X., Kang C. M., Brody M. S., Price C. W. 1996; Opposing pair of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev 10:2265–2275 [CrossRef]
    [Google Scholar]
  62. Zhang C. C., Friry A., Peng L. 1998a; Molecular and genetic analysis of two closely linked genes that encode, respectively, a protein phosphatase1/2A/2B homolog and protein kinase homolog in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 180:2616–2622
    [Google Scholar]
  63. Zhang C. C., Gonzalez L., Phalip C. 1998b; Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res 26:3619–3625 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27057-0
Loading
/content/journal/micro/10.1099/mic.0.27057-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error