A new group of photoreceptors has been experimentally revealed in cyanobacteria. They are phototaxis regulator SyPixJ1, TePixJ and AnPixJ, chromatic acclimation regulator SyCcaS, circadian input kinase homolog SyCikA and many other candidates, which have been found only in cyanobacteria to date. These new photoreceptors are now proposed to be “cyanobacteriochromes”. They are characterized by the presence of a chromophore-binding GAF domain that is homologous to the tetrapyrrole-binding GAF domain of the phytochrome. Here, we summarized unique features of those representatives: (1) only the GAF domain is sufficient for full photoconversion, (2) the GAF domain is homologous to but distinct from the phytochrome GAF, (3) the GAF domain binds a linear tetrapyrrole pigment such as phycoviolobilin or phycocyanobilin, (4) spectral properties are very diverse from near ultra-violet to red region. We also discussed the functionality of the other candidate GAFs, structure and evolution.

Cyanobacteriochromes are a newly recognized group of photoreceptors that are distinct relatives of phytochromes but are found only in cyanobacteria. A putative cyanobacteriochrome, CcaS, is known to chromatically regulate the expression of the phycobilisome linker gene ( cpcG2 ) in Synechocystis sp. PCC 6803. In this study, we isolated the chromophore-binding domain of CcaS from Synechocystis as well as from phycocyanobilin-producing Escherichia coli . Both preparations showed the same reversible photoconversion between a green-absorbing form (Pg, λ _max = 535 nm) and a red-absorbing form (Pr, λ _max = 672 nm). Mass spectrometry and denaturation analyses suggested that Pg and Pr bind phycocyanobilin in a double-bond configuration of C15- Z and C15- E , respectively. Autophosphorylation activity of the histidine kinase domain in nearly full-length CcaS was up-regulated by preirradiation with green light. Similarly, phosphotransfer to the cognate response regulator, CcaR, was higher in Pr than in Pg. From these results, we conclude that CcaS phosphorylates CcaR under green light and induces expression of cpcG2 , leading to accumulation of CpcG2-phycobilisome as a chromatic acclimation system. CcaS is the first recognized green light receptor in the expanded phytochrome superfamily, which includes phytochromes and cyanobacteriochromes.

Significance: Light-harvesting antenna are essential for photosynthetic systems, which comprise photosystems I and II (PSI and PSII, respectively). Phycobilisome (PBS) is a dominant and efficient antenna for PSII in cyanobacteria and some algae, whereas the attachment of PBS to PSI is a long-standing open question. We isolated a unique PBS–PSI supercomplex from a nitrogen-fixing cyanobacterium. Biochemical and spectral studies revealed that PBS is functionally connected to the PSI tetramer via a new universal connecting component. A pseudoatomic model explains the configuration of the PSI tetramer and how the PBS is connected to PSI. Such antenna may play an important role for light harvesting in PSI-driven cyclic electron transport to facilitate nitrogen fixation and other reactions.

Cyanobacteriochromes are cyanobacterial tetrapyrrole-binding photoreceptors that share a bilin-binding GAF domain with photoreceptors of the phytochrome family. Cyanobacteriochromes are divided into many subclasses with distinct spectral properties. Among them, putative phototaxis regulators PixJs of Anabaena sp. PCC 7120 and Thermosynechococcus elongatus BP-1 (denoted as AnPixJ and TePixJ, respectively) are representative of subclasses showing red-green-type and blue/green-type reversible photoconversion, respectively. Here, we determined crystal structures for the AnPixJ GAF domain in its red-absorbing 15 Z state (Pr) and the TePixJ GAF domain in its green-absorbing 15 E state (Pg). The overall structure of these proteins is similar to each other and also similar to known phytochromes. Critical differences found are as follows: ( i ) the chromophore of AnPixJ Pr is phycocyanobilin in a C5- Z ,syn/C10- Z ,syn/C15- Z ,anti configuration and that of TePixJ Pg is phycoviolobilin in a C10- Z ,syn/C15- E ,anti configuration, ( ii ) a side chain of the key aspartic acid is hydrogen bonded to the tetrapyrrole rings A, B and C in AnPixJ Pr and to the pyrrole ring D in TePixJ Pg, ( iii ) additional protein-chromophore interactions are provided by subclass-specific residues including tryptophan in AnPixJ and cysteine in TePixJ. Possible structural changes following the photoisomerization of the chromophore between C15- Z and C15- E are discussed based on the X-ray structures at 1.8 and 2.0-Å resolution, respectively, in two distinct configurations.

Cyanobacteriochromes (CBCRs) are cyanobacterial members of the phytochrome superfamily of photosensors. Like phytochromes, CBCRs convert between two photostates by photoisomerization of a covalently bound linear tetrapyrrole (bilin) chromophore. Although phytochromes are red/far-red sensors, CBCRs exhibit diverse photocycles spanning the visible spectrum and the near-UV (330–680 nm). Two CBCR subfamilies detect near-UV to blue light (330–450 nm) via a “two-Cys photocycle” that couples bilin 15Z/15E photoisomerization with formation or elimination of a second bilin–cysteine adduct. On the other hand, mechanisms for tuning the absorption between the green and red regions of the spectrum have not been elucidated as of yet. CcaS and RcaE are members of a CBCR subfamily that regulates complementary chromatic acclimation, in which cyanobacteria optimize light-harvesting antennae in response to green or red ambient light. CcaS has been shown to undergo a green/red photocycle: reversible photoconversion between a green-absorbing 15Z state ( ^15Z P _g ) and a red-absorbing 15E state ( ^15E P _r ). We demonstrate that RcaE from Fremyella diplosiphon undergoes the same photocycle and exhibits light-regulated kinase activity. In both RcaE and CcaS, the bilin chromophore is deprotonated as ^15Z P _g but protonated as ^15E P _r . This change of bilin protonation state is modulated by three key residues that are conserved in green/red CBCRs. We therefore designate the photocycle of green/red CBCRs a “protochromic photocycle,” in which the dramatic change from green to red absorption is not induced by initial bilin photoisomerization but by a subsequent change in bilin protonation state.