Red/Green Cyanobacteriochromes: Sensors of Color and Power

Abstract

Phytochromes are red/far-red photoreceptors using cysteine-linked linear tetrapyrrole (bilin) chromophores to regulate biological responses to light. Light absorption triggers photoisomerization of the bilin between the 15Z and 15E photostates. The related cyanobacteriochromes (CBCRs) extend the photosensory range of the phytochrome superfamily to shorter wavelengths of visible light. Several subfamilies of CBCRs have been described. Representatives of one such subfamily, including AnPixJ and NpR6012g4, exhibit red/green photocycles in which the 15Z photostate is red-absorbing like that of phytochrome but the 15E photoproduct is instead green-absorbing. Using recombinant expression of individual CBCR domains in Escherichia coli, we fully survey the red/green subfamily from the cyanobacterium Nostoc punctiforme. In addition to 14 new photoswitching CBCRs, one apparently photochemically inactive protein exhibiting intense red fluorescence was observed. We describe a novel orange/green photocycle in one of these CBCRs, NpF2164g7. Dark reversion varied in this panel of CBCRs; some examples were stable as the 15E photoproduct for days, while others reverted to the 15Z dark state in minutes or even seconds. In the case of NpF2164g7, dark reversion was so rapid that reverse photoconversion of the green-absorbing photoproduct was not significant in restoring the dark state, resulting in a broadband response to light. Our results demonstrate that red/green CBCRs can thus act as sensors for the color or intensity of the ambient light environment.

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle

“…Both 15Z P g and 15E P r exhibited negative CD on the long-wavelength band (Fig. 1C), indicative of the α-facial bilin D-ring in both 15Z and 15E states (25,42) seen in many CBCRs (19,23,24). These features of RcaE are very similar to those previously described for CcaS (16,40), implicating a conserved green/red photocycle in known CCA photoreceptors.…”

“…Interestingly, the secondary chemical reaction requires only a few residues within the GAF domain (e.g., the protochromic triad or the second Cys), providing a powerful mechanism for evolution of CBCRs with distinct spectral properties. This work also provides a potential explanation for the spectral sensitivity of members of the red/green CBCR subfamily, proteins that typically exhibit a red/green photocycle, which is the opposite of that seen in green/red CBCRs (17,24). Such CBCRs also might change the bilin protonation state to induce changes in their absorption spectra.…”

“…* Cyanobacteriochromes (CBCRs) are widespread cyanobacterial photosensors with phytochrome-related GAF domains (1,2,13,14). Although CBCRs also convert between two photostates via bilin photoisomerization at C15, they exhibit much more spectral diversity, with peak absorptions ranging from 330 to 680 nm and hence spanning the entire visible spectrum and near UV (13,(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). CBCR subfamilies that sense light in the near-UV to blue region (330-470 nm) have been studied extensively.…”

Apo-bacteriophytochromes modulate bacterial photosynthesis in response to low light

“…Phytochromes and cyanobacteriochromes have been implicated in sensing not only light quality, but also light intensity (17,34). We were surprised to find that that the RpBphP2/P3 chromophore BV is not required to sense light intensity under anoxic conditions.…”

“…R. palustris also increases the synthesis of its LH4 complexes in response to a decrease in white light intensity when grown anaerobically, and both RpBphP2 and RpBphP3 are required for this response (7,8,16). In plants and cyanobacteria, phytochromes have been implicated in the sensing of light intensity, for which their ability to bind a chromophore and carry out photoconversion is essential (17,18).…”