Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism

Narikawa, Rei; Ishizuka, Takami; Muraki, Norifumi; Shiba, T.; Kurisu, Genji; Ikeuchi, Masahiko

doi:10.1073/pnas.1212098110

Cited by 160 publications

(399 citation statements)

References 44 publications

(98 reference statements)

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“…S1C). In both these motifs, the Asp side chain specifically and directly interacts with the 15E bilin (9,28). Moreover, typical pK a values for Glu residues are closer to the intrinsic bilin pK a [∼6 (45)] than are Lys pK a values.…”

Section: Discussionmentioning

confidence: 99%

“…CBCR subfamilies that sense light in the near-UV to blue region (330-470 nm) have been studied extensively. Such CBCRs combine bilin photoisomerization with subsequent formation or elimination of a second thioether linkage to the bilin C10 atom, shortening the conjugated π system to induce a remarkable spectral shift (19,21,23,(25)(26)(27)(28)(29). In such "two-Cys photocycles," the reactive thiol group is supplied by a second conserved Cys residue within the GAF domain.…”

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confidence: 99%

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

Hirose

Rockwell

Nishiyama

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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153

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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 bilincysteine 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.light sensing | phycobiliprotein | signal transduction | spectral tuning | two-component signaling P hytochrome photosensors initially were discovered in plants and later found in cyanobacteria, nonoxygenic photosynthetic bacteria, nonphotosynthetic bacteria, fungi, and algae (1, 2). These photoreceptors bind linear tetrapyrrole (bilin) chromophores within a conserved GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) domain via a covalent thioether linkage to a conserved Cys residue (Fig. S1A)(3-6). Upon illumination, phytochromes reversibly convert between a red-absorbing dark state and a far-red-absorbing photoproduct. This red/far-red photocycle is triggered by photoisomerization of the bilin 15,16-double bond between the 15Z and 15E configurations (7,8), with 15Z giving red absorption and 15E far-red absorption (4, 6, 9). In phytochromes, the conjugated π system of the bilin is protonated in both photostates, and this protonation is necessary to maintain the red and far-red absorption (10-12). Conserved GAF residues supply a hydrogen bond network to tune the chemical and spectral properties of the bilin (Fig. S1B).* 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 spe...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Hirose

Rockwell

Nishiyama

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

153

265

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“…However, PCB in ApcEΔ is exceptional in having, instead, the ZZZssa geometry (Figs. 3 and 4) that is characteristic for the photoactive bilin chromophores of the sensory photoreceptors, phytochromes, and cyanobacteriochromes (14)(15)(16)(17). The unusual ZZZssa geometry of PCB is stabilized in ApcEΔ by the pivotal carboxyl group of Asp161: the pyrrolic nitrogens of rings A, B, and C are in H-bonding positions [NH-O = 2.7 (ring A), NH-O = 2.9 (ring B), and NH-O = 2.8 Å (ring C)] (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…These shifts and their intense fluorescence are brought about by noncovalent interactions with the apoproteins (13). The malleability of this flexible open-chain tetrapyrrole chromophore by the apoprotein is also further emphasized by its presence in sensory photoreceptors (phytochromes and cyanobacteriochromes), which serve as photoswitches (14)(15)(16)(17). Here, PCB shows only low fluorescence.…”

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confidence: 99%

The terminal phycobilisome emitter, L _CM : A light-harvesting pigment with a phytochrome chromophore

Tang

Ding

Höppner

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Photosynthesis relies on energy transfer from light-harvesting complexes to reaction centers. Phycobilisomes, the light-harvesting antennas in cyanobacteria and red algae, attach to the membrane via the multidomain core-membrane linker, L CM . The chromophore domain of L CM forms a bottleneck for funneling the harvested energy either productively to reaction centers or, in case of light overload, to quenchers like orange carotenoid protein (OCP) that prevent photodamage. The crystal structure of the solubly modified chromophore domain from Nostoc sp. PCC7120 was resolved at 2.2 Å. Although its protein fold is similar to the protein folds of phycobiliproteins, the phycocyanobilin (PCB) chromophore adopts ZZZssa geometry, which is unknown among phycobiliproteins but characteristic for sensory photoreceptors (phytochromes and cyanobacteriochromes). However, chromophore photoisomerization is inhibited in L CM by tight packing. The ZZZssa geometry of the chromophore and π-π stacking with a neighboring Trp account for the functionally relevant extreme spectral red shift of L CM . Exciton coupling is excluded by the large distance between two PCBs in a homodimer and by preservation of the spectral features in monomers. The structure also indicates a distinct flexibility that could be involved in quenching. The conclusions from the crystal structure are supported by femtosecond transient absorption spectra in solution.cyanobacteria | phycobilisome | core-membrane linker | photosynthesis | crystal structure T he structural separation of light-harvesting and energy transduction processes allows photosynthetic organisms a flexible adaptation to the diverse light regimes present in terrestrial and aqueous habitats. In cyanobacteria and some phylogenetically related organisms that, together, provide a substantial proportion of global carbon fixation, light is harvested by hundreds of chromophores located in the peripheral antenna, namely, the phycobilisome (PBS). These excitations are then collected and transferred to the energy-transducing photosystems I (PSI) and PSII in the photosynthetic membrane via only two pigments, allophycocyanin B (AP-B) and the core-membrane linker (L CM ) (1-5). AP-B preferentially serves PSI (2); it is structurally similar to the bulk phycobiliproteins of the PBS (6). L CM (denoted as ApcE according to the gene by which it is encoded), preferentially serving PSII (5), is a more complex multidomain protein, with an N-terminal section that binds the phycocyanobilin (PCB) chromophore, and is homologous to phycobiliproteins but carries an additional loop that probably acts as a membrane anchor to PSII (4, 7-10). The Cterminal section consists of two to four repeats (depending on the PBS type) that are homologous to the N-terminal domain (Pfam PF00427) of structural PBS proteins, rod-linkers [Protein Data Bank (PDB) ID codes 3OSJ and 3OHW], and considered to organize the complex PBS core (9). They are probably also the loci for phosphorylation (11).Both AP-B and L CM contain the same PCB chromophores...

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“…CBCRs cover a broad range of the visible/near UV spectrum but are restricted to cyanobacteria. Whereas, the photosensory modules of several prokaryotic phytochromes from Groups I (8,9) and III (13,14) have been characterized structurally, little is known about Cph2 homologues in Group II.…”

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confidence: 99%

Structure of the Cyanobacterial Phytochrome 2 Photosensor Implies a Tryptophan Switch for Phytochrome Signaling

Anders

Daminelli-Widany

Mroginski

et al. 2013

Journal of Biological Chemistry

168

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Background: Phytochromes are red/far-red photoreceptors using a bilin chromophore. Results: Compared with Cph1, the Cph2 bilin-binding site differs around the propionates, but utilizes an otherwise conserved tongue for sealing the chromophore from solvent. Conclusion:The tongue signals via a tryptophan switch within the tongue-GAF domain interface. Significance: The first structure of a Cph2-type phytochrome indicates a common mechanism for photoswitching in all canonical phytochromes.

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Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism

Cited by 160 publications

References 44 publications

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

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

The terminal phycobilisome emitter, L _CM : A light-harvesting pigment with a phytochrome chromophore

Structure of the Cyanobacterial Phytochrome 2 Photosensor Implies a Tryptophan Switch for Phytochrome Signaling

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Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism

Cited by 160 publications

References 44 publications

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

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

The terminal phycobilisome emitter, L CM : A light-harvesting pigment with a phytochrome chromophore

Structure of the Cyanobacterial Phytochrome 2 Photosensor Implies a Tryptophan Switch for Phytochrome Signaling

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The terminal phycobilisome emitter, L _CM : A light-harvesting pigment with a phytochrome chromophore