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Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore

Nature volume 414, pages 776–779 (2001)Cite this article

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.

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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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Author notes

  1. Seth J. Davis

    Present address: Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK

  2. Seong-Hee Bhoo and Seth J. Davis: These authors contributed equally to this work

Authors and Affiliations

  1. Cellular and Molecular Biology Program and the Department of Horticulture, University of Wisconsin—Madison, 1575 Linden Drive, Madison, 53706, Wisconsin, USA

    Seong-Hee Bhoo, Seth J. Davis, Joseph Walker, Baruch Karniol & Richard D. Vierstra

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Correspondence to Richard D. Vierstra.

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Supplementary information

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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