1887

Abstract

Originally identified from eukaryotes, the Mg- or Mn-dependent protein phosphatases (PPMs) are a diverse group of enzymes whose members include eukaryotic PP2C and some prokaryotic serine/threonine phosphatases. In a previous study, unexpectedly large numbers of PPMs were identified in two genomes. In this work, a phylogenetic analysis was performed with all the PPMs available from a wide variety of microbial sources to determine the evolutionary origin of the PPM proteins. Consistent with earlier hypotheses, the results suggested that the microbial PPMs were relatively recent additions from eukaryotic sources. Results also indicated that the PPMs were divided into two major subfamilies at an early stage of their emergence in genomes. The first subfamily, which contains only six PPMs, possesses a catalytic domain whose sequence and architecture are similar to that of eukaryotic PPMs; the second subfamily contains 89 PPMs that lack the 5a and 5b catalytic domain motifs, similar to the PPMs SpoIIE and RsbU of . Significant gene duplication was observed for the PPMs in the second subfamily. In addition, more than half (54 %) of the PPMs from the second subfamily were found to have at least one additional sensory domain, most commonly the PAS or the GAF domain. Phylogenetic analysis showed that these domains tended to be clustered according to the putative physiological functions rather than taxonomic relationship, implying that they might have arisen as a result of domain recruitment in a late evolutionary stage. This study provides an insight into how spp. may have expanded their PPM-based signal transduction networks to enable them to respond to a greater range of environmental changes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27480-0
2004-12-01
2019-11-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/12/mic1504189.html?itemId=/content/journal/micro/10.1099/mic.0.27480-0&mimeType=html&fmt=ahah

References

  1. Aravind, L. & Ponting, C. P. ( 1997; ). The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22, 458–459.[CrossRef]
    [Google Scholar]
  2. 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]
  3. 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]
  4. Blumenberg, M. ( 1988; ). Concerted gene duplications in the two keratin gene families. J Mol Evol 27, 203–211.[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. Chater, K. F. ( 1993; ). Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47, 683–713.
    [Google Scholar]
  7. Cohen, P. T. W. ( 1994; ). Nomenclature and chromosomal localization of human protein serine/threonine phosphatase genes. Adv Protein Phosphatases 8, 371–376.
    [Google Scholar]
  8. Copley, R. R., Goodstadt, L. & Ponting, C. ( 2003; ). Eukaryotic domain evolution inferred from genome comparisons. Curr Opin Genet Dev 13, 623–628.[CrossRef]
    [Google Scholar]
  9. Coque, J. J., Martin, J. F., Calzada, J. G. & Liras, P. ( 1991; ). The cephamycin biosynthetic genes pcbAB, encoding a large multidomain peptide synthetase, and pcbC of Nocardia lactamdurans are clustered together in an organization different from the same genes in Acremonium chrysogenum and Penicillium chrysogenum. Mol Microbiol 5, 1125–1133.[CrossRef]
    [Google Scholar]
  10. 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]
  11. Egan, S., Wiener, P., Kallifidas, D. & Wellington, E. M. ( 2001; ). Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Antonie Van Leeuwenhoek 79, 127–133.[CrossRef]
    [Google Scholar]
  12. Gaidenko, T., Kim, T. J. & Price, C. W. ( 2002; ). The PrpC serine-threonine phosphatase and PrkC kinase have opposing physiological roles in stationary-phase Bacillus subtilis cells. J Bacteriol 184, 6109–6114.[CrossRef]
    [Google Scholar]
  13. Gruber, T. M. & Gross, C. A. ( 2003; ). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57, 441–466.[CrossRef]
    [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. Jain, R., Rivera, M. C. & Lake, J. A. ( 1999; ). Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96, 3801–3806.[CrossRef]
    [Google Scholar]
  19. Kennelly, P. J. ( 2001; ). Protein phosphatase – a phylogenetic perspective. Chem Rev 101, 2291–2312.[CrossRef]
    [Google Scholar]
  20. Kennelly, P. J. ( 2002; ). Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol Lett 206, 1–8.[CrossRef]
    [Google Scholar]
  21. Koonin, E. V. & Galperin, M. Y. ( 1997; ). Prokaryotic genomes: the emerging paradigm of genome-based microbiology. Curr Opin Genet Dev 7, 757–763.[CrossRef]
    [Google Scholar]
  22. Letunic, I., Goodstadt, L., Dickens, N. J. & 7 other authors ( 2002; ). Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res 30, 242–244.[CrossRef]
    [Google Scholar]
  23. 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]
  24. Ma, H. W. & Zeng, A. P. ( 2004; ). Phylogenetic comparison of metabolic capacities of organisms at genome level. Mol Phylogenet Evol 31, 204–213.[CrossRef]
    [Google Scholar]
  25. 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]
  26. Mittenhuber, G. ( 2002; ). A phylogenomic study of the general stress response sigma factor sigmaB of Bacillus subtilis and its regulatory proteins. J Mol Microbiol Biotechnol 4, 427–452.
    [Google Scholar]
  27. Nádvorník, R., Vomastek, T., Janecek, J., Techniková, Z. & Branny, P. ( 1999; ). Pkg2, a novel transmembrane protein Ser/Thr kinase of Streptomyces granaticolor. J Bacteriol 181, 15–23.
    [Google Scholar]
  28. Ponting, C. P., Aravind, L., Schultz, J., Bork, P. & Koonin, E. V. ( 1999; ). Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol 1289, 729–745.
    [Google Scholar]
  29. Rajagopal, L., Clancy, A. & Ruhens, C. E. ( 2003; ). A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J Biol Chem 278, 14429–14441.[CrossRef]
    [Google Scholar]
  30. Shi, L. ( 2004; ). Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions. Front Biosci 9, 1382–1397.[CrossRef]
    [Google Scholar]
  31. Shi, L. & Zhang, W. ( 2004; ). Comparative analysis of eukaryotic-type protein phosphatases in two streptomycete genomes. Microbiology 150, 2247–2256.[CrossRef]
    [Google Scholar]
  32. 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]
  33. Shi, L., Bischoff, K. M. & Kennelly, P. J. ( 1999; ). 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]
  34. Taylor, B. L. & Zhulin, I. B. ( 1999a; ). PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63, 479–506.
    [Google Scholar]
  35. Taylor, B. L., Zhulin, I. B. & Johnson, M. S. ( 1999b; ). Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53, 103–128.[CrossRef]
    [Google Scholar]
  36. 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]
  37. 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]
  38. 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]
  39. 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]
  40. 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 sigmaB transcription factor of Bacillus subtilis. Mol Microbiol 35, 180–188.[CrossRef]
    [Google Scholar]
  41. 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]
  42. Wellington, E. M., Cresswell, N. & Herron, P. R. ( 1992; ). Gene transfer between streptomycetes in soil. Gene 115, 193–198.[CrossRef]
    [Google Scholar]
  43. Woese, C. R., Kandler, O. & Wheelis, M. L. ( 1990; ). Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87, 4576–4579.[CrossRef]
    [Google Scholar]
  44. Yang, X., Kang, C. M., Brody, M. S. & Price, C. W. ( 1996; ). Opposing pairs 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]
  45. Zhang, C. C., Gonzalez, L. & Phalip, C. ( 1998; ). 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.0.27480-0
Loading
/content/journal/micro/10.1099/mic.0.27480-0
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