Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore

Abstract

Phytochromes comprise a principal family of red/far-red light sensors in plants. Although phytochromes were thought originally to be confined to photosynthetic organisms, we have recently detected phytochrome-like proteins in two heterotrophic eubacteria, Deinococcus radiodurans and Pseudomonas aeruginosa. 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.

The Heme Oxygenase(s)-Phytochrome System of Pseudomonas aeruginosa

“…BV) was then associated with BphP, indicating that BV was removed from BphO and was attached to BphP. This attachment was identified to be covalent by zinc blotting (40) (data not shown) and is in agreement with other known bacterial phytochromes that form a covalent complex with BV (11,41). Experiments to identify real physical interaction between BphO and BphP using the GPC method after Hummel and Dreyer (42) with BphO⅐BV in the mobile phase did not reveal a stable complex of both proteins (data not shown).…”

“…The biological reason for the production of BV IX␤ and BV IX␦, however, remains unknown. In comparison, to date, there is only indirect evidence that bphO genes encode for functional HOs (11). In this report we present biochemical and biophysical evidence demonstrating that recombinant P. aeruginosa BphO is indeed a heme oxygenase that catalyzes the conversion of heme to BV IX␣.…”

“…Phytochromes are traditionally known as biliprotein photoreceptors in plants but have recently also been discovered in bacteria (10). Unlike plant and cyanobacterial phytochromes, which carry a phytochromobilin or phycocyanobilin chromophore, bacteriophytochromes (BphPs) from non-photosynthetic prokaryotes have been shown to utilize a BV chromophore (11). P. aeruginosa was among the first non-photosynthetic bacteria identified to harbor a gene encoding for a BphP.…”

The Structure of Phytochrome: A Picture Is Worth a Thousand Spectra

“…Phytochrome C-terminal domains mediate the transmission of photosensory signals perceived by the N-terminal region to signal transduction pathways within the cell. This region typically contains a histidine kinase-related domain that has been shown to confer ATP-dependent protein phosphotransferase activity in several cases (Yeh et al, 1997;Yeh and Lagarias, 1998;Bhoo et al, 2001;Hü bschmann et al, 2001;Lamparter et al, 2001;Karniol and Vierstra, 2003;Giraud et al, 2005;Tasler et al, 2005). While bacterial and cyanobacterial phytochromes typically employ classical two-component phosphotransfer relays, the mechanism of plant phytochrome signaling appears considerably more complex, involving lightmediated nuclear translocation and regulation of transcription factor function (Chen et al, 2004;Nagatani, 2004;Huq and Quail, 2005;Schä fer and Nagy, 2005).…”

“…Heme oxygenases convert heme to biliverdin IXa (BV), which is the direct precursor of the chromophores of bacteriophytochromes (Bhoo et al, 2001;Giraud et al, 2002Giraud et al, , 2005Lamparter et al, 2003Lamparter et al, , 2004Tasler et al, 2005) and probably also those of fungal phytochromes (Blumenstein et al, 2005;Froehlich et al, 2005). In cyanobacteria and algae, BV is converted to phycocyanobilin (PCB) via a four-electron reduction mediated by ferredoxin-dependent bilin reductases of the PcyA subfamily ).…”