1887

Abstract

Although most two-component signal transduction systems use a simple phosphotransfer pathway from one histidine kinase (HK) to one response regulator (RR), a multiple-step phosphorelay involving a phosphotransfer scheme of His–Asp–His–Asp was also discovered. Central to this multiple-step-type signal transduction pathway are a hybrid-type HK, containing both an HK domain and an RR receiver domain in a single protein, and a histidine-containing phosphotransfer (HPT) that can exist either as a domain in hybrid-type HKs or as a separate protein. Although multiple-step phosphorelay systems are predominant in eukaryotes, it has been previously suggested that they are less common in prokaryotes. In this study, it was found that putative hybrid-type HKs were present in 56 of 156 complete prokaryotic genomes, indicating that multiple-step phosphorelay systems are more common in prokaryotes than previously appreciated. Large expansions of hybrid-type HKs were observed in 26 prokaryotic species, including photosynthetic cyanobacteria such as sp. PCC 7120, and several pathogenic bacteria such as . Phylogenetic analysis indicated that there was no common ancestor for hybrid-type HKs, and their origin and expansion was achieved by lateral recruitment of a receiver domain into an HK molecule and then duplication as one unit. Lateral recruitment of additional sensory domains such as PAS was also evident. HPT domains or proteins were identified in 32 of the genomes with hybrid-type HKs; however, no significant gene expansion was observed for HPTs even in a genome with a large number of hybrid-type HKs. In addition, fewer HPTs than hybrid-type HKs were identified in all prokaryotic genomes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27987-0
2005-07-01
2019-11-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/7/mic1512159.html?itemId=/content/journal/micro/10.1099/mic.0.27987-0&mimeType=html&fmt=ahah

References

  1. Appleby, J. L., Parkinson, J. S. & Bourret, R. B. ( 1996; ). Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86, 845–848.[CrossRef]
    [Google Scholar]
  2. 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]
  3. Bijlsma, J. J. E. & Groisman, E. A. ( 2003; ). Making informed decisions: regulatory interactions between two-component systems. Trends Microbiol 11, 359–366.[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. Bourret, R. B., Hess, J. F., Borkovich, K. A., Pakula, A. A. & Simon, M. I. ( 1989; ). Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. J Biol Chem 264, 7085–7088.
    [Google Scholar]
  6. Burbulys, D., Trach, K. A. & Hoch, J. A. ( 1991; ). Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64, 545–552.[CrossRef]
    [Google Scholar]
  7. Catlett, N. L., Yoder, O. C. & Turgeon, B. G. ( 2003; ). Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2, 1151–1161.[CrossRef]
    [Google Scholar]
  8. Chang, C. & Stewart, R. C. ( 1998; ). The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiol 117, 723–731.[CrossRef]
    [Google Scholar]
  9. Chang, C. H., Zhu, J. & Winans, S. C. ( 1996; ). Pleiotropic phenotypes caused by genetic ablation of the receiver module of the Agrobacterium tumefaciens VirA protein. J Bacteriol 178, 4710–4716.
    [Google Scholar]
  10. Clarke, D. J., Joyce, S. A., Toutain, C. M., Jacq, A. & Holland, I. B. ( 2002; ). Genetic analysis of the RcsC sensor kinase from Escherichia coli K-12. J Bacteriol 184, 1204–1208.[CrossRef]
    [Google Scholar]
  11. Dutta, R., Qin, L. & Inouye, M. ( 1999; ). Histidine kinases: diversity of domain organization. Mol Microbiol 34, 633–640.[CrossRef]
    [Google Scholar]
  12. Forst, S., Delgado, J. & Inouye, M. ( 1989; ). Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. Proc Natl Acad Sci U S A 86, 6052–6056.[CrossRef]
    [Google Scholar]
  13. Galperin, M. Y., Nikolskaya, A. N. & Koonin, E. V. ( 2001; ). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203, 11–21.[CrossRef]
    [Google Scholar]
  14. Grefen, C. & Harter, K. ( 2004; ). Plant two-component systems: principles, functions, complexity and cross talk. Planta 219, 733–742.
    [Google Scholar]
  15. Grossman, A. D. ( 1995; ). Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet 29, 477–508.[CrossRef]
    [Google Scholar]
  16. Hagiwara, D., Yamashino, T. & Mizuno, T. ( 2004; ). Genome-wide comparison of the His-to-Asp phosphorelay signaling components of three symbiotic genera of Rhizobia. DNA Res 11, 57–65.[CrossRef]
    [Google Scholar]
  17. Heidelberg, J. F., Seshadri, R., Haveman, S. A. & 32 other authors ( 2004; ). The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22, 554–559.[CrossRef]
    [Google Scholar]
  18. Higgins, D. G. & Sharp, P. M. ( 1988; ). clustal: a package for performing multiple sequence alignment on a microcomputer. Gene 73, 237–244.[CrossRef]
    [Google Scholar]
  19. Hoch, J. A. ( 2000; ). Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3, 165–170.[CrossRef]
    [Google Scholar]
  20. Kaneko, T., Sato, S., Kotani, H. & 21 other authors ( 1996; ). 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 (supplement). DNA Res 3, 185–209.[CrossRef]
    [Google Scholar]
  21. Kaneko, T., Nakamura, Y., Wolk, C. P. & 19 other authors ( 2001; ). Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8, 205–213.[CrossRef]
    [Google Scholar]
  22. Kato, M., Mizuno, T., Shimizu, T. & Hakoshima, T. ( 1997; ). Insights into multistep phosphorelay from the crystal structure of the C-terminal HPt domain of ArcB. Cell 88, 717–723.[CrossRef]
    [Google Scholar]
  23. Kim, D. & Forst, S. ( 2001; ). Genomic analysis of the histidine kinase family in bacteria and archaea. Microbiol 147, 1197–1212.
    [Google Scholar]
  24. Koretke, K. K., Lupas, A. N., Warren, P. V., Rosenberg, M. & Brown, J. R. ( 2000; ). Evolution of two-component signal transduction. Mol Biol Evol 17, 1956–1970.[CrossRef]
    [Google Scholar]
  25. Leonardo, M. R. & Forst, S. ( 1996; ). Re-examination of the role of the periplasmic domain of EnvZ in sensing of osmolarity signals in Escherichia coli. Mol Microbiol 22, 405–413.[CrossRef]
    [Google Scholar]
  26. 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]
  27. 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]
  28. Methe, B. A., Nelson, K. E., Eisen, J. A. & 31 other authors ( 2003; ). Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967–1969.[CrossRef]
    [Google Scholar]
  29. Ogino, T., Matsubara, M., Kato, N., Nakamura, Y. & Mizuno, T. ( 1998; ). An Escherichia coli protein that exhibits phosphohistidine phosphatase activity towards the HPt domain of the ArcB sensor involved in the multistep His-Asp phosphorelay. Mol Microbiol 27, 573–585.[CrossRef]
    [Google Scholar]
  30. Oka, A., Sakai, H. & Iwakoshi, S. ( 2002; ). His-Asp phosphorelay signal transduction in higher plants: receptors and response regulators for cytokinin signaling in Arabidopsis thaliana. Genes Genet Syst 77, 383–391.[CrossRef]
    [Google Scholar]
  31. Pao, G. M. & Saier, M. H., Jr ( 1997; ). Nonplastid eukaryotic response regulators have a monophyletic origin and evolved from their bacterial precursors in parallel with their cognate sensor kinases. J Mol Evol 44, 605–613.[CrossRef]
    [Google Scholar]
  32. Parkinson, J. S. & Kofoid, E. C. ( 1992; ). Communication modules in bacterial signaling proteins. Annu Rev Genet 26, 71–112.[CrossRef]
    [Google Scholar]
  33. Pawson, T. & Scott, J. D. ( 1997; ). Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075–2080.[CrossRef]
    [Google Scholar]
  34. Posas, F., Wurgler-Murphy, S. M., Maeda, T., Witten, E. A., Thai, T. C. & Saito, H. ( 1996; ). Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86, 865–875.[CrossRef]
    [Google Scholar]
  35. Rabus, R., Ruepp, A., Frickey, T. & 15 other authors ( 2004; ). The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6, 887–902.[CrossRef]
    [Google Scholar]
  36. Robinson, V. L., Buckler, D. R. & Stock, A. M. ( 2000; ). A tale of two components: a novel kinase and a regulatory switch. Nat Struct Biol 7, 626–633.[CrossRef]
    [Google Scholar]
  37. Rodrigue, A., Quentin, Y., Lazdunski, A., Méjean, V. & Foglino, M. ( 2000; ). Cell signalling by oligosaccharides. Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8, 498–504.[CrossRef]
    [Google Scholar]
  38. Stephenson, K. & Hoch, J. A. ( 2002; ). Evolution of signalling in the sporulation phosphorelay. Mol Microbiol 46, 297–304.[CrossRef]
    [Google Scholar]
  39. Stock, J. B., Ninfa, A. J. & Stock, A. M. ( 1989; ). Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53, 450–490.
    [Google Scholar]
  40. Stoker, K., Reijnders, W. N., Oltmann, L. F. & Stouthamer, A. H. ( 1989; ). Initial cloning and sequencing of hydHG, an operon homologous to ntrBC and regulating the labile hydrogenase activity in Escherichia coli K-12. J Bacteriol 171, 4448–4456.
    [Google Scholar]
  41. Takeda, S., Fujisawa, Y., Matsubara, M., Aiba, H. & Mizuno, T. ( 2001; ). A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC→YojN→RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol 40, 440–450.[CrossRef]
    [Google Scholar]
  42. 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]
  43. Taylor, B. L., Zhulin, I. B. & Johnson, M. S. ( 1999; ). Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53, 103–128.[CrossRef]
    [Google Scholar]
  44. Uhl, M. A. & Miller, J. F. ( 1996; ). Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J 15, 1028–1036.
    [Google Scholar]
  45. West, A. H. & Stock, A. M. ( 2001; ). Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26, 369–376.[CrossRef]
    [Google Scholar]
  46. Xu, Q. & West, A. H. ( 1999; ). Conservation of structure and function among histidine-containing phosphotransfer (HPt) domains as revealed by the crystal structure of YPD1. J Mol Biol 292, 1039–1050.[CrossRef]
    [Google Scholar]
  47. Xu, J., Bjursell, M. K., Himrod, J., Deng, S., Carmichael, L. K., Chiang, H. C., Hooper, L. V. & Gordon, J. I. ( 2003; ). A genomic view of the human–Bacteroides thetaiotaomicron symbiosis. Science 299, 2074–2076.[CrossRef]
    [Google Scholar]
  48. Xu, J., Chiang, H. C., Bjursell, M. K. & Gordon, J. I. ( 2004; ). Message from a human gut symbiont: sensitivity is a prerequisite for sharing. Trends Microbiol 12, 21–28.[CrossRef]
    [Google Scholar]
  49. Zhang, W. & Shi, L. ( 2004; ). Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains. Microbiology 150, 4189–4197.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27987-0
Loading
/content/journal/micro/10.1099/mic.0.27987-0
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