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Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore

Abstract

Phytochromes comprise a principal family of red/far-red light sensors in plants1. Although phytochromes were thought originally to be confined to photosynthetic organisms2,3, we have recently detected phytochrome-like proteins in two heterotrophic eubacteria, Deinococcus radiodurans and Pseudomonas aeruginosa4. Here we show that these form part of a widespread family of bacteriophytochromes (BphPs) with homology to two-component sensor histidine kinases. Whereas plant phytochromes use phytochromobilin as the chromophore, BphPs assemble with biliverdin, an immediate breakdown product of haem, to generate photochromic kinases that are modulated by red and far-red light. In some cases, a unique haem oxygenase responsible for the synthesis of biliverdin is part of the BphP operon. Co-expression of this oxygenase with a BphP apoprotein and a haem source is sufficient to assemble holo-BphP in vivo. Both their presence in many diverse bacteria and their simplified assembly with biliverdin suggest that BphPs are the progenitors of phytochrome-type photoreceptors.

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Figure 1: Sequence comparison of the BphP family and detection of the BphP chromoprotein from D. radiodurans.
Figure 2: Detection of sequences encoding haem oxygenase (BphOs) in several BphP operons and assembly of BphPs with BV.
Figure 3: In vivo assembly of recombinant D. radiodurans BphP by co-expression of the apoprotein with D. radiodurans (Dr) BphO or Synechocystis (Syn) haem oxygenase 1.
Figure 4: Ps BphP assembled with BV acts as a R-activated histidine kinase in a two-component phospho-relay system.

References

  1. Smith, H. Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407, 585–591 (2000).

    Article  ADS  CAS  Google Scholar 

  2. Hughes, J. & Lamparter, T. Prokaryotes and phytochrome. The connection to chromophores and signaling. Plant Physiol. 121, 1059–1068 (1999).

    Article  CAS  Google Scholar 

  3. Vierstra, R. D. & Davis, S. J. Bacteriophytochromes: new tools for understanding phytochrome signal transduction. Semin. Cell. Dev. Biol. 11, 511–521 (2000).

    Article  CAS  Google Scholar 

  4. Davis, S. J., Vener, A. V. & Vierstra, R. D. Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286, 2517–2520 (1999).

    Article  CAS  Google Scholar 

  5. Jiang, Z. et al. Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285, 406–409 (1999).

    Article  CAS  Google Scholar 

  6. Herdman, M., Coursin, T., Rippka, R., Houmard, J. & Tandeau de Marsac, N. A new appraisal of the prokaryotic origin of eukaryotic phytochromes. J. Mol. Evol. 51, 205–213 (2000).

    Article  ADS  CAS  Google Scholar 

  7. Bhaya, D., Takahashi, A. & Grossman, A. R. Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proc. Natl Acad. Sci. USA 98, 7540–7545 (2001).

    Article  ADS  CAS  Google Scholar 

  8. Kehoe, D. M. & Grossman, A. R. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273, 1409–1412 (1996).

    Article  ADS  CAS  Google Scholar 

  9. Yeh, K. C., Wu, S. H., Murphy, J. T. & Lagarias, J. C. A cyanobacterial phytochrome two-component light sensory system. Science 277, 1505–1508 (1997).

    Article  CAS  Google Scholar 

  10. West, A. H. & Stock, A. M. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26, 369–376 (2001).

    Article  CAS  Google Scholar 

  11. Beale, S. I. Biosynthesis of phycobilins. Chem. Rev. 93, 785–802 (1993).

    Article  CAS  Google Scholar 

  12. Berkelman, T. R. & Lagarias, J. C. Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal. Biochem. 156, 194–201 (1986).

    Article  CAS  Google Scholar 

  13. Davis, S. J., Kurepa, J. & Vierstra, R. D. The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc. Natl Acad. Sci. USA 96, 6541–6546 (1999).

    Article  ADS  CAS  Google Scholar 

  14. Frankenberg, N., Mukougawa, K., Kohchi, T. & Lagarias, J. C. Functional genomic analysis of the hy2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13, 965–978 (2001).

    Article  CAS  Google Scholar 

  15. Zhu, W., Hunt, D. J., Richardson, A. R. & Stojiljkovic, I. Use of heme compounds as iron sources by pathogenic Neisseriae requires the product of the hemO gene. J Bacteriol 182, 439–447 (2000).

    Article  CAS  Google Scholar 

  16. Ochsner, U. A. & Vasil, M. L. Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. Proc. Natl Acad. Sci. USA 93, 4409–4414 (1996).

    Article  ADS  CAS  Google Scholar 

  17. Elich, T. D. & Lagarias, J. C. Formation of a photoreversible phycocyanobilin-apophytochrome adduct in vitro. J. Biol. Chem. 264, 12902–12908 (1989).

    Article  CAS  Google Scholar 

  18. Cornejo, J., Willows, R. D. & Beale, S. I. Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J. 15, 99–107 (1998).

    Article  CAS  Google Scholar 

  19. Yeh, K. C. & Lagarias, J. C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl Acad. Sci. USA 95, 13976–13981 (1998).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank P.-S. Song for providing PCB and PEB, and M. Wexler, J. Todd and A. Johnston for making the R. leguminosarium sequences available before publication. This work was supported by grants from the US Department of Energy and the National Science Foundation to R.D.V.

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Correspondence to Richard D. Vierstra.

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Figure 1

(GIF 48.85 KB)

Amino acid sequence alignments of the BphOs from D. radiodurans (GB: AF396710), P. aeruginosa (GB: A83131), P. syringae (GB: AF396712), P. fluorescens (GB AF396711) as compared to HemO from N. gonorrhoeae (GB: AF133695), and HOs from Synechocystis (GB: D90091), human (GB: P09601), and the higher plant Arabidopsis thaliana (GB: AF132475). The circle indicates the positionally conserved histidine essential for hemin iron binding during catalysis. The triangle shows the histidine required for protein stability in mammalian HOs. Reverse type and gray boxes denote identical and similar amino acids.

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Bhoo, SH., Davis, S., Walker, J. et al. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414, 776–779 (2001). https://doi.org/10.1038/414776a

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