The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties

Abstract

Bacteriophytochrome photoreceptors (BphPs) are a family of phytochrome-like sensor kinases that help a wide variety of bacteria respond to their light environment. In Agrobacterium tumefaciens, a unique pair of BphPs with potentially opposing roles in light sensing are present. Both AtBphPs contain an N-terminal chromophore-binding domain that covalently attaches a biliverdin chromophore. Whereas AtBphP1 assumes a Pr ground state, AtBphP2 is unusual in that it assumes a Pfr ground state that is produced nonphotochemically after biliverdin binding through a transient Pr-like intermediate. Photoconversion of AtBphP2 with far-red light then generates Pr but this Pr is also unstable and rapidly reverts nonphotochemically to Pfr. AtBphP1 contains a typical two-component histidine kinase domain at its C terminus whose activity is repressed after photoconversion to Pfr. AtBphP2 also functions as a histidine kinase but instead uses a distinct two-component kinase motif that is repressed after photoconversion to Pr. We identified sequences related to this domain in numerous predicted sensing proteins in A. tumefaciens and other bacteria, indicating that AtBphP2 might represent the founding member of a family of histidine phosphorelay proteins that is widely used in environmental signaling. By using these mutually opposing BphPs, A. tumefaciens presumably has the capacity to simultaneously sense red light-rich and far-red light-rich environments through deactivation of their associated kinase cascades.

Diatom Phytochromes Reveal the Existence of Far-Red-Light-Based Sensing in the Ocean

“…Given that Pt-DPH can undergo a R-FR photocycle, we further tested whether it could act as a light-regulated kinase in vitro, as already observed for several phytochrome photoreceptors (Yeh and Lagarias, 1998;Karniol and Vierstra, 2003;Giraud et al, 2005). Incubation of recombinant holo-Pt-DPH-FL in the presence of [Y-32 P]ATP revealed rapid protein autophosphorylation upon FR light illumination, whereas only a basal signal could be detected from R-light-irradiated Pt-DPH-FL ( Figure 4D).…”

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

“…Moreover, the residues surrounding the bilin D-ring are very highly conserved between plant phytochromes that utilize PFB as chromophore, cyanobacterial phytochromes that utilize PCB, and bacteriophytochromes that utilize BV ( Figure 4A). It therefore seems likely that the key chromophore motions and protein conformational changes associated with the photochemical reaction pathway will be conserved among all members of the phytochrome family, perhaps even those bacteriophytochromes that adopt the Pfr state at thermal equilibrium (Karniol and Vierstra, 2003;Tasler et al, 2005) or others that interconvert between Pr and a blue-shifted P nr (for pigment absorbing in the near red) state (Giraud et al, 2005).…”

“…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).…”

Structure of the Biliverdin Cofactor in the Pfr State of Bathy and Prototypical Phytochromes

“…While being attached to the protein through a different binding site, BV adopts nearly the same conformation in the binding pocket and undergoes an identical photochemistry with a C-15ϭC-16 double bond photoisomerization (12)(13)(14)(15). These BV-harboring bacteriochromes can further be grouped into prototypical and bathy phytochromes in which the thermodynamically stable states are Pr and Pfr, respectively (16,17).…”

“…This different stability of the parent states is most probably the reason why three-dimensional structures so far have been mainly obtained for the Pr state of protypical phytochromes and the Pfr state of bathy phytochromes (13)(14)(15)(16)(17)(18)(19)(20). Although the gross chromophore structures in the respective parent states are likely to be similar in prototypical and bathy phytochromes, it appears to be premature to consider the available three-dimensional structures of the Pr states of the prototypical phytochrome and the yet only available three-dimensional structure of the Pfr state of bathy phytochrome from Pseudomonas aeruginosa (PaBphP) as representative structures for the respective parent states in both classes of phytochromes (12).…”