1887

Abstract

Two-component signal transduction systems, consisting of histidine kinase (HK) sensors and DNA-binding response regulators, allow bacteria and archaea to respond to diverse environmental stimuli. HKs possess a conserved domain (H-box region) which contains the site of phosphorylation and an ATP-binding kinase domain. In this study, a genomic approach was taken to analyse the HK family in bacteria and archaea. Based on phylogenetic analysis, differences in the sequence and organization of the H-box and kinase domains, and the predicted secondary structure of the H-box region, five major HK types were identified. Of the 336 HKs analysed, 92% could be assigned to one of the five major HK types. The Type I HKs were found predominantly in bacteria while Type II HKs were not prevalent in bacteria but constituted the major type (13 of 15 HKs) in the archaeon . Type III HKs were generally more prevalent in Gram-positive bacteria and were the major HK type (14 of 15 HKs) in the archaeon . Type IV HKs represented a minor type found in bacteria. The fifth HK type was composed of the chemosensor HKs, CheA. Several bacterial genomes contained all five HK types. In contrast, archaeal genomes either contained a specific HK type or lacked HKs altogether. These findings suggest that the different HK types originated in bacteria and that specific HK types were acquired in archaea by horizontal gene transfer.

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2001-05-01
2019-10-19
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References

  1. Alex, L. A., Borkovich, K. A. & Simon, M. I. ( 1996; ). Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc Natl Acad Sci USA 93, 3416-3421.[CrossRef]
    [Google Scholar]
  2. Appleby, J. L., Parkinson, J. S. & Bourret, R. B. ( 1996; ). Signal transduction via the multistep phosphorelay: not necessarily a road less traveled. Cell 86, 845-848.[CrossRef]
    [Google Scholar]
  3. Bilwes, A. M., Alex, L. A., Crane, B. R. & Simon, M. I. ( 1999; ). Structure of CheA, a signal-transducing histidine kinase. Cell 96, 131-141.[CrossRef]
    [Google Scholar]
  4. Blattner, F. R., Plunkett, G., Bloch, C. A. & 14 other authors ( 1997; ). The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1474.[CrossRef]
    [Google Scholar]
  5. Bult, C. J., White, O., Olsen, G. J. & 37 other authors ( 1996; ). Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058–1073.[CrossRef]
    [Google Scholar]
  6. Chang, C., Kwok, S. F., Bleecker, A. B. & Meyerowitz, E. M. ( 1993; ). Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262, 539-544.[CrossRef]
    [Google Scholar]
  7. Chang, W. T., Thomason, P. A., Gross, J. D. & Neweil, P. C. ( 1998; ). Evidence that the RdeA protein is a component of a multistep phosphorelay modulating rate of development in Dictyostelium. EMBO J 17, 2809-2816.[CrossRef]
    [Google Scholar]
  8. Davies, R., Devlin, K., Feltwell, T. & 39 other authors ( 1998; ). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537–544.[CrossRef]
    [Google Scholar]
  9. Deckert, G., Warren, P. V., Gaasterland, T. & 12 other authors ( 1998; ). The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392, 353–358.[CrossRef]
    [Google Scholar]
  10. Dutta, R., Qin, L. & Inouye, M. ( 1999; ). Histidine kinases: diversity of domain organization. Mol Microbiol 34, 633-640.[CrossRef]
    [Google Scholar]
  11. Egger, L. A., Park, H. & Inouye, M. ( 1997; ). Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells 2, 167-184.[CrossRef]
    [Google Scholar]
  12. Fabret, C., Feher, V. A. & Hoch, J. A. ( 1999; ). Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181, 1975-1983.
    [Google Scholar]
  13. Forst, S. A. & Roberts, D. L. ( 1994; ). Signal transduction by the EnvZ–OmpR phosphotransfer system in bacteria. Res Microbiol 145, 363-373.[CrossRef]
    [Google Scholar]
  14. Garzon, A. & Parkinson, J. S. ( 1996; ). Chemotactic signaling by the P1 phosphorylation domain liberated from the CheA histidine kinase of Escherichia coli. J Bacteriol 178, 6752-6758.
    [Google Scholar]
  15. Grebe, T. W. & Stock, J. B. ( 1999; ). The histidine protein kinase superfamily. Adv Microb Physiol 41, 139-227.
    [Google Scholar]
  16. Heidelberg, J. F., Eisen, J. A., Nelson, W. C. & 29 other authors ( 2000; ). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477–483.[CrossRef]
    [Google Scholar]
  17. Hoch, J. A. ( 1995; ). Control of cellular development in sporulation bacteria by the phosphorelay two-component signal transduction system. In Two-Component Signal Transduction , pp. 129-144. Edited by J. A. Hoch & T. J. Silhavy. Washington, DC: American Society for Microbiology Press.
  18. Hoch, J. A. & Silhavy, T. J. (eds) (1995). Two-Component Signal Transduction. Washington, DC: American Society for Microbiology Press.
  19. 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. DNA Res 3, 109–136.[CrossRef]
    [Google Scholar]
  20. Kawarabayasi, Y., Sawada, M., Horikawa, H. & 29 other authors ( 1998; ). Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res 5, 147–155.[CrossRef]
    [Google Scholar]
  21. Kawarabayasi, Y., Hino, Y., Horikawa, H. & 22 other authors ( 1999; ). Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res 6, 83–101.[CrossRef]
    [Google Scholar]
  22. Klenk, H.-P., Clayton, R. A., Tomb, J.-F. & 48 other authors ( 1998; ). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon, Archaeoglobus fulgidus. Nature 390, 364–370.
    [Google Scholar]
  23. Kofoid, E. C. & Parkinson, J. S. ( 1988; ). Transmitter and receiver modules in bacterial signaling proteins. Proc Natl Acad Sci USA 85, 4981-4985.[CrossRef]
    [Google Scholar]
  24. Kunst, F., Ogasawara, N., Moszer, I. & 148 other authors ( 1997; ). The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249–256.[CrossRef]
    [Google Scholar]
  25. Loomis, W. F., Kuspa, A. & Shaulsky, G. ( 1998; ). Two-component signal transduction systems in eukaryotic microorganisms. Curr Opin Microbiol 1, 643-648.[CrossRef]
    [Google Scholar]
  26. Mizuno, T. ( 1997; ). Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4, 161-168.[CrossRef]
    [Google Scholar]
  27. Mizuno, T., Kaneko, T. & Tabata, S. ( 1996; ). Compilation of all genes encoding bacterial two- component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res 3, 407-414.[CrossRef]
    [Google Scholar]
  28. Nelson, K. E., Clayton, R. A., Gill, S. R. & 23 other authors ( 1999; ). Evidence for the lateral gene transfer between archaea and bacteria from the sequence of Thermotoga maritima. Nature 399, 323–329.[CrossRef]
    [Google Scholar]
  29. Ng, V. W., Kennedy, P. S., Mahairasa, G. G. & 40 other authors ( 2000; ). Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97, 12176–12181.[CrossRef]
    [Google Scholar]
  30. Ota, I. M. & Varshavsky, A. ( 1993; ). A yeast protein similar to bacterial two-component regulators. Science 262, 566-569.[CrossRef]
    [Google Scholar]
  31. Park, H., Saha, S. K. & Inouye, M. ( 1998; ). Two-domain reconstitution of a functional protein histidine kinase. Proc Natl Acad Sci USA 95, 6728-6732.[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. Perraud, A.-L., Weiss, V. & Gross, R. ( 1999; ). Signalling pathways in two-component phosphorelay systems. Trends Microbiol 7, 115-120.[CrossRef]
    [Google Scholar]
  34. Robinson, V. L. & Stock, A. M. ( 1999; ). High energy exchange: proteins that make or break phosphoramidate bonds. Struct Fold Des 7, R47-R53.[CrossRef]
    [Google Scholar]
  35. Schuster, S. S., Noegel, A. A., Oehme, F., Gerisch, G. & Simon, M. I. ( 1996; ). The hybrid histidine kinase DokA is part of the osmotic response system in Dictyostelium. EMBO J 15, 3880-3889.
    [Google Scholar]
  36. Simson, A. J. G., Reinach, F. C., Arruda, P. & 113 other authors ( 2000; ). The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406, 151–157.[CrossRef]
    [Google Scholar]
  37. Smith, D. R., Doucette-Stamm, L. A., Deloughery, C. & 34 other authors 1997). Complete genome sequence of Methanobacterium thermoautotrophicum delta H: functional analysis and comparative genomics. J Bacteriol 179, 7135–7155.
  38. Stock, A., Chen, T., Welsh, D. & Stock, J. ( 1988; ). CheA protein, a central regulator of bacterial chemotaxis, belongs to a family of proteins that control gene expression in response to changing environmental conditions. Proc Natl Acad Sci USA 85, 1403-1407.[CrossRef]
    [Google Scholar]
  39. Stock, J. B., Srette, M. G., Levit, M. & Park, P. ( 1995; ). Two-component signal transduction systems: structure function relationships and mechanisms of catalysis. In Two-Component Signal Transduction , pp. 25-51. Edited by J. A. Hoch & T. J. Silhavy. Washington, DC: American Society for Microbiology Press.
  40. Stover, C. K., Pham, X. Q., Erwin, A. L. & 28 other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen . Nature 406, 959–964.[CrossRef]
    [Google Scholar]
  41. Suzuki, T., Imamura, A., Ueguchi, C. & Mizuno, T. ( 1998; ). Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol 39, 1258-1268.[CrossRef]
    [Google Scholar]
  42. Tanaka, T., Saha, S. K. & Inouye, M. ( 1998; ). NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature 396, 88-92.[CrossRef]
    [Google Scholar]
  43. Tomomori, C., Tanaka, T., Dutta, R. & 12 other authors ( 1999; ). Solution structure of the homodimeric core domain of Escherichia coli histidine kinase EnvZ. Nature Struct Biol 6, 729–734.[CrossRef]
    [Google Scholar]
  44. White, O., Eisen, J. A., Heidelberg, J. F. & 29 other authors ( 1999; ). Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286, 1571–1577.[CrossRef]
    [Google Scholar]
  45. Zhou, H. & Dalquihst, F. W. ( 1997; ). Phosphotransfer site of the chemotaxis-specific protein kinase CheA as revealed by NMR. Biochemistry 36, 699-710.[CrossRef]
    [Google Scholar]
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