Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Jun;179(12):3914–3921. doi: 10.1128/jb.179.12.3914-3921.1997

New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system.

D M Kehoe 1, A R Grossman 1
PMCID: PMC179199  PMID: 9190806

Abstract

Complementary chromatic adaptation appears to be controlled by a complex regulatory system with similarity to four-step phosphorelays. Such pathways utilize two histidine and two aspartate residues for signal transduction. Previous studies of the signaling system controlling complementary chromatic adaptation have uncovered two elements of this pathway, a putative sensor, RcaE, and a response regulator, RcaC. In this work, we describe a second response regulator controlling complementary chromatic adaptation, RcaF, and identify putative DNA binding and histidine phosphoacceptor domains within RcaC. RcaF is a small response regulator with similarity to SpoOF of Bacillus subtilis; the latter functions in the four-step phosphorelay system controlling sporulation. We have also determined that within this phosphorelay pathway, RcaE precedes RcaF, and RcaC is probably downstream of RcaE and RcaF. This signal transduction pathway is novel because it appears to use at least five, instead of four, phosphoacceptor domains in the phosphorelay circuit.

Full Text

The Full Text of this article is available as a PDF (322.9 KB).

Selected References

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

  1. Alex L. A., Borkovich K. A., Simon M. I. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3416–3421. doi: 10.1073/pnas.93.8.3416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Atkinson M. R., Ninfa A. J. Mutational analysis of the bacterial signal-transducing protein kinase/phosphatase nitrogen regulator II (NRII or NtrB). J Bacteriol. 1993 Nov;175(21):7016–7023. doi: 10.1128/jb.175.21.7016-7023.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett A., Bogorad L. Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol. 1973 Aug;58(2):419–435. doi: 10.1083/jcb.58.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bennett A., Bogorad L. Properties of subunits and aggregates of blue-green algal biliproteins. Biochemistry. 1971 Sep 14;10(19):3625–3634. doi: 10.1021/bi00795a022. [DOI] [PubMed] [Google Scholar]
  7. Boyd J. M., Lory S. Dual function of PilS during transcriptional activation of the Pseudomonas aeruginosa pilin subunit gene. J Bacteriol. 1996 Feb;178(3):831–839. doi: 10.1128/jb.178.3.831-839.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bruns B. U., Briggs W. R., Grossman A. R. Molecular characterization of phycobilisome regulatory mutants of Fremyella diplosiphon. J Bacteriol. 1989 Feb;171(2):901–908. doi: 10.1128/jb.171.2.901-908.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bryant D. A. The photoregulated expression of multiple phycocyanin species. A general mechanism for the control of phycocyanin synthesis in chromatically adapting cyanobacteria. Eur J Biochem. 1981 Oct;119(2):425–429. doi: 10.1111/j.1432-1033.1981.tb05625.x. [DOI] [PubMed] [Google Scholar]
  10. Burbulys D., Trach K. A., Hoch J. A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell. 1991 Feb 8;64(3):545–552. doi: 10.1016/0092-8674(91)90238-t. [DOI] [PubMed] [Google Scholar]
  11. Cavicchioli R., Schröder I., Constanti M., Gunsalus R. P. The NarX and NarQ sensor-transmitter proteins of Escherichia coli each require two conserved histidines for nitrate-dependent signal transduction to NarL. J Bacteriol. 1995 May;177(9):2416–2424. doi: 10.1128/jb.177.9.2416-2424.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Chiang G. G., Schaefer M. R., Grossman A. R. Complementation of a red-light-indifferent cyanobacterial mutant. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9415–9419. doi: 10.1073/pnas.89.20.9415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clegg D. O., Koshland D. E., Jr The role of a signaling protein in bacterial sensing: behavioral effects of increased gene expression. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5056–5060. doi: 10.1073/pnas.81.16.5056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Conley P. B., Lemaux P. G., Grossman A. R. Cyanobacterial light-harvesting complex subunits encoded in two red light-induced transcripts. Science. 1985 Nov 1;230(4725):550–553. doi: 10.1126/science.3931221. [DOI] [PubMed] [Google Scholar]
  16. Diakoff S., Scheibe J. Action Spectra for Chromatic Adaptation in Tolypothrix tenuis. Plant Physiol. 1973 Feb;51(2):382–385. doi: 10.1104/pp.51.2.382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Eraso J. M., Kaplan S. prrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol. 1994 Jan;176(1):32–43. doi: 10.1128/jb.176.1.32-43.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Federspiel N. A., Grossman A. R. Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bacteriol. 1990 Jul;172(7):4072–4081. doi: 10.1128/jb.172.7.4072-4081.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Feng J., Atkinson M. R., McCleary W., Stock J. B., Wanner B. L., Ninfa A. J. Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli. J Bacteriol. 1992 Oct;174(19):6061–6070. doi: 10.1128/jb.174.19.6061-6070.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fiedler U., Weiss V. A common switch in activation of the response regulators NtrC and PhoB: phosphorylation induces dimerization of the receiver modules. EMBO J. 1995 Aug 1;14(15):3696–3705. doi: 10.1002/j.1460-2075.1995.tb00039.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Golden S. S. Mutagenesis of cyanobacteria by classical and gene-transfer-based methods. Methods Enzymol. 1988;167:714–727. doi: 10.1016/0076-6879(88)67083-2. [DOI] [PubMed] [Google Scholar]
  22. Greck M., Platzer J., Sourjik V., Schmitt R. Analysis of a chemotaxis operon in Rhizobium meliloti. Mol Microbiol. 1995 Mar;15(6):989–1000. doi: 10.1111/j.1365-2958.1995.tb02274.x. [DOI] [PubMed] [Google Scholar]
  23. Haury J. F., Bogorad L. Action Spectra for Phycobiliprotein Synthesis in a Chromatically Adapting Cyanophyte, Fremyella diplosiphon. Plant Physiol. 1977 Dec;60(6):835–839. doi: 10.1104/pp.60.6.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hertig C., Li R. Y., Louarn A. M., Garnerone A. M., David M., Batut J., Kahn D., Boistard P. Rhizobium meliloti regulatory gene fixJ activates transcription of R. meliloti nifA and fixK genes in Escherichia coli. J Bacteriol. 1989 Mar;171(3):1736–1738. doi: 10.1128/jb.171.3.1736-1738.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hua J., Chang C., Sun Q., Meyerowitz E. M. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science. 1995 Sep 22;269(5231):1712–1714. doi: 10.1126/science.7569898. [DOI] [PubMed] [Google Scholar]
  26. Ishige K., Nagasawa S., Tokishita S., Mizuno T. A novel device of bacterial signal transducers. EMBO J. 1994 Nov 1;13(21):5195–5202. doi: 10.1002/j.1460-2075.1994.tb06850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jourlin C., Bengrine A., Chippaux M., Méjean V. An unorthodox sensor protein (TorS) mediates the induction of the tor structural genes in response to trimethylamine N-oxide in Escherichia coli. Mol Microbiol. 1996 Jun;20(6):1297–1306. doi: 10.1111/j.1365-2958.1996.tb02648.x. [DOI] [PubMed] [Google Scholar]
  28. Kadner R. J., Island M. D., Dahl J. L., Webber C. A. A transmembrane signalling complex controls transcription of the Uhp sugar phosphate transport system. Res Microbiol. 1994 Jun-Aug;145(5-6):381–387. doi: 10.1016/0923-2508(94)90085-x. [DOI] [PubMed] [Google Scholar]
  29. Kehoe D. M., Grossman A. R. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science. 1996 Sep 6;273(5280):1409–1412. doi: 10.1126/science.273.5280.1409. [DOI] [PubMed] [Google Scholar]
  30. Liu J. D., Parkinson J. S. Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8703–8707. doi: 10.1073/pnas.86.22.8703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lomax T. L., Conley P. B., Schilling J., Grossman A. R. Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA. J Bacteriol. 1987 Jun;169(6):2675–2684. doi: 10.1128/jb.169.6.2675-2684.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lukat G. S., McCleary W. R., Stock A. M., Stock J. B. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):718–722. doi: 10.1073/pnas.89.2.718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Malvar T., Gawron-Burke C., Baum J. A. Overexpression of Bacillus thuringiensis HknA, a histidine protein kinase homology, bypasses early Spo mutations that result in CryIIIA overproduction. J Bacteriol. 1994 Aug;176(15):4742–4749. doi: 10.1128/jb.176.15.4742-4749.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mazel D., Guglielmi G., Houmard J., Sidler W., Bryant D. A., Tandeau de Marsac N. Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res. 1986 Nov 11;14(21):8279–8290. doi: 10.1093/nar/14.21.8279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mettke I., Fiedler U., Weiss V. Mechanism of activation of a response regulator: interaction of NtrC-P dimers induces ATPase activity. J Bacteriol. 1995 Sep;177(17):5056–5061. doi: 10.1128/jb.177.17.5056-5061.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Oelmüller R., Conley P. B., Federspiel N., Briggs W. R., Grossman A. R. Changes in Accumulation and Synthesis of Transcripts Encoding Phycobilisome Components during Acclimation of Fremyella diplosiphon to Different Light Qualities. Plant Physiol. 1988 Dec;88(4):1077–1083. doi: 10.1104/pp.88.4.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Oelmüller R., Grossman A. R., Briggs W. R. Photoreversibility of the Effect of Red and Green Light Pulses on the Accumulation in Darkness of mRNAs Coding for Phycocyanin and Phycoerythrin in Fremyella diplosiphon. Plant Physiol. 1988 Dec;88(4):1084–1091. doi: 10.1104/pp.88.4.1084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ota I. M., Varshavsky A. A yeast protein similar to bacterial two-component regulators. Science. 1993 Oct 22;262(5133):566–569. doi: 10.1126/science.8211183. [DOI] [PubMed] [Google Scholar]
  40. Parkinson J. S., Kofoid E. C. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. doi: 10.1146/annurev.ge.26.120192.000443. [DOI] [PubMed] [Google Scholar]
  41. Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Perego M., Cole S. P., Burbulys D., Trach K., Hoch J. A. Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J Bacteriol. 1989 Nov;171(11):6187–6196. doi: 10.1128/jb.171.11.6187-6196.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Ravid S., Matsumura P., Eisenbach M. Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the chemotaxis protein CheY. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7157–7161. doi: 10.1073/pnas.83.19.7157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Rogowsky P. M., Close T. J., Chimera J. A., Shaw J. J., Kado C. I. Regulation of the vir genes of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol. 1987 Nov;169(11):5101–5112. doi: 10.1128/jb.169.11.5101-5112.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schaefer M. R., Chiang G. G., Cobley J. G., Grossman A. R. Plasmids from two morphologically distinct cyanobacterial strains share a novel replication origin. J Bacteriol. 1993 Sep;175(17):5701–5705. doi: 10.1128/jb.175.17.5701-5705.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Shattuck-Eidens D. M., Kadner R. J. Molecular cloning of the uhp region and evidence for a positive activator for expression of the hexose phosphate transport system of Escherichia coli. J Bacteriol. 1983 Sep;155(3):1062–1070. doi: 10.1128/jb.155.3.1062-1070.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tandeau de Marsac N. Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol. 1977 Apr;130(1):82–91. doi: 10.1128/jb.130.1.82-91.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Trach K. A., Chapman J. W., Piggot P. J., Hoch J. A. Deduced product of the stage 0 sporulation gene spo0F shares homology with the Spo0A, OmpR, and SfrA proteins. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7260–7264. doi: 10.1073/pnas.82.21.7260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wanner B. L. Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? J Bacteriol. 1992 Apr;174(7):2053–2058. doi: 10.1128/jb.174.7.2053-2058.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wilkinson J. Q., Lanahan M. B., Yen H. C., Giovannoni J. J., Klee H. J. An ethylene-inducible component of signal transduction encoded by never-ripe. Science. 1995 Dec 15;270(5243):1807–1809. doi: 10.1126/science.270.5243.1807. [DOI] [PubMed] [Google Scholar]
  52. Wolfe A. J., Conley M. P., Kramer T. J., Berg H. C. Reconstitution of signaling in bacterial chemotaxis. J Bacteriol. 1987 May;169(5):1878–1885. doi: 10.1128/jb.169.5.1878-1885.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yamaguchi S., Aizawa S., Kihara M., Isomura M., Jones C. J., Macnab R. M. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol. 1986 Dec;168(3):1172–1179. doi: 10.1128/jb.168.3.1172-1179.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES