A Photochromic Histidine Kinase Rhodopsin (HKR1) That Is Bimodally Switched by Ultraviolet and Blue Light

• Published in: The Journal of biological chemistry Vol. 287; no. 47; pp. 40083 - 40090
• Main Authors: Luck, Meike, Mathes, Tilo, Bruun, Sara, Fudim, Roman, Hagedorn, Rolf, Tran Nguyen, Tra My, Kateriya, Suneel, Kennis, John T.M., Hildebrandt, Peter, Hegemann, Peter
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 16.11.2012; American Society for Biochemistry and Molecular Biology
• Subjects: Adaptation, Physiological - physiology; Adaptation, Physiological - radiation effects; Adenylyl Cyclases - chemistry; Adenylyl Cyclases - genetics; Adenylyl Cyclases - metabolism; Binding Sites; Chlamydomonas reinhardtii - enzymology; Chlamydomonas reinhardtii - genetics; Guanylate Cyclase - chemistry; Guanylate Cyclase - genetics; Guanylate Cyclase - metabolism; Histidine Kinase; Molecular Biophysics; Optogenetics; Photobiology; Photoreceptors; Plant Proteins - chemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Protein Kinases - chemistry; Protein Kinases - genetics; Protein Kinases - metabolism; Protein Structure, Tertiary; Raman Spectroscopy; Rhodopsin; Rhodopsin - chemistry; Rhodopsin - genetics; Rhodopsin - metabolism; Spectroscopy; Ultraviolet Rays; Raman Spectroscopy; Spectroscopy; Photoreceptors; Rhodopsin; Optogenetics; Photobiology
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1074/jbc.M112.401604

Rhodopsins are light-activated chromoproteins that mediate signaling processes via transducer proteins or promote active or passive ion transport as ion pumps or directly light-activated channels. Here, we provide spectroscopic characterization of a rhodopsin from the Chlamydomonas eyespot. It belongs to a recently discovered but so far uncharacterized family of histidine kinase rhodopsins (HKRs). These are modular proteins consisting of rhodopsin, a histidine kinase, a response regulator, and in some cases an effector domain such as an adenylyl or guanylyl cyclase, all encoded in a single protein as a two-component system. The recombinant rhodopsin fragment, Rh, of HKR1 is a UVA receptor (λmax = 380 nm) that is photoconverted by UV light into a stable blue light-absorbing meta state Rh-Bl (λmax = 490 nm). Rh-Bl is converted back to Rh-UV by blue light. Raman spectroscopy revealed that the Rh-UV chromophore is in an unusual 13-cis,15-anti configuration, which explains why the chromophore is deprotonated. The excited state lifetime of Rh-UV is exceptionally stable, probably caused by a relatively unpolar retinal binding pocket, converting into the photoproduct within about 100 ps, whereas the blue form reacts 100 times faster. We propose that the photochromic HKR1 plays a role in the adaptation of behavioral responses in the presence of UVA light. Background: Microbial rhodopsins in Chlamydomonas are employed for photoorientation and developmental processes. Results: HKR1 is a UVA-absorbing rhodopsin that is bimodally switched between a UV- and a blue light-absorbing isoform with different light colors. Conclusion: The chromophore of the dark-adapted UV state contains a deprotonated Schiff base stabilized by a 13-cis,15-anti conformation. Significance: This is the initial characterization of the first member of a novel rhodopsin family.