Identification of Cyanobacteriochromes Detecting Far-Red Light

Rockwell, Nathan C.; Martin, Shelley S.; Lagarias, J. Clark

doi:10.1021/acs.biochem.6b00299

Title: Identification of Cyanobacteriochromes Detecting Far-Red Light

Journal Article · Sat Jul 02 00:00:00 EDT 2016 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.6b00299· OSTI ID:1260055

Rockwell, Nathan C. ^[1]; Martin, Shelley S. ^[1]; Lagarias, J. Clark ^[1]

Department of Molecular and Cellular Biology, University of California, Davis, California 95616, United States

The opacity of mammalian tissue to visible light and the strong attenuation of infrared light by water at ≥900 nm have contributed to growing interest in the development of far-red and near-infrared absorbing tools for visualizing and actuating responses within live cells. Here we report the discovery of cyanobacteriochromes (CBCRs) responsive to light in this far-red window. CBCRs are linear tetrapyrrole (bilin)-based light sensors distantly related to plant phytochrome sensors. Our studies reveal far-red (λ_max = 725–755 nm)/orange (λ_max = 590–600 nm) and far-red/red (λ_max = 615–685 nm) photoswitches that are small (<200 amino acids) and can be genetically reconstituted in living cells. Phylogenetic analysis and characterization of additional CBCRs demonstrated that far-red/orange CBCRs evolved after a complex transition from green/red CBCRs known for regulating complementary chromatic acclimation. Incorporation of different bilin chromophores demonstrated that tuning mechanisms responsible for red-shifted chromophore absorption act at the A-, B-, and/ or C-rings, whereas photoisomerization occurs at the D-ring. Two such proteins exhibited detectable fluorescence extending well into the near-infrared region. In conclusion, this work extends the spectral window of CBCRs to the edge of the infrared, raising the possibility of using CBCRs in synthetic biology applications in the far-red region of the spectrum.

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Research Organization:: Univ. of California, Davis, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0002395

OSTI ID:: 1260055

Alternate ID(s):: OSTI ID: 1267164

Journal Information:: Biochemistry, Journal Name: Biochemistry Vol. 55 Journal Issue: 28; ISSN 0006-2960

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 59 works

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A biliverdin-binding cyanobacteriochrome from the chlorophyll d–bearing cyanobacterium Acaryochloris marina Narikawa, Rei; Nakajima, Takahiro; Aono, Yuki Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep07950	journal	January 2015
Thiol-Based Photocycle of the Blue and Teal Light-Sensing Cyanobacteriochrome Tlr1999 Enomoto, Gen; Hirose, Yuu; Narikawa, Rei Biochemistry, Vol. 51, Issue 14 https://doi.org/10.1021/bi300020u	journal	March 2012
Phototropism: Bending towards Enlightenment Whippo, Craig W.; Hangarter, Roger P. The Plant Cell, Vol. 18, Issue 5 https://doi.org/10.1105/tpc.105.039669	journal	May 2006
Distinct classes of red/far-red photochemistry within the phytochrome superfamily Rockwell, N. C.; Shang, L.; Martin, S. S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0902370106	journal	April 2009
How to Switch Off a Histidine Kinase: Crystal Structure of Geobacillus stearothermophilus KinB with the inhibitor Sda Bick, Matthew J.; Lamour, Valerie; Rajashankar, Kanagalaghatta R. Journal of Molecular Biology, Vol. 386, Issue 1 https://doi.org/10.1016/j.jmb.2008.12.006	journal	February 2009
Bacterial phytochromes: More than meets the light Auldridge, Michele E.; Forest, Katrina T. Critical Reviews in Biochemistry and Molecular Biology, Vol. 46, Issue 1 https://doi.org/10.3109/10409238.2010.546389	journal	January 2011
Phototropins 1 and 2: versatile plant blue-light receptors Briggs, Winslow R.; Christie, John M. Trends in Plant Science, Vol. 7, Issue 5 https://doi.org/10.1016/S1360-1385(02)02245-8	journal	May 2002
Phytochrome functions in Arabidopsis development Franklin, K. A.; Quail, P. H. Journal of Experimental Botany, Vol. 61, Issue 1 https://doi.org/10.1093/jxb/erp304	journal	October 2009
A Brief History of Phytochromes Rockwell, Nathan C.; Lagarias, J. Clark ChemPhysChem, Vol. 11, Issue 6 https://doi.org/10.1002/cphc.200900894	journal	April 2010
Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too van der Horst, Michael A.; Key, Jason; Hellingwerf, Klaas J. Trends in Microbiology, Vol. 15, Issue 12 https://doi.org/10.1016/j.tim.2007.09.009	journal	December 2007
Defining the Bilin Lyase Domain: Lessons from the Extended Phytochrome Superfamily ^† Wu, Shu-Hsing; Lagarias, J. Clark Biochemistry, Vol. 39, Issue 44 https://doi.org/10.1021/bi001123z	journal	November 2000
Reconstitution of Blue−Green Reversible Photoconversion of a Cyanobacterial Photoreceptor, PixJ1, in Phycocyanobilin-Producing Escherichia coli ^† Yoshihara, Shizue; Shimada, Takashi; Matsuoka, Daisuke Biochemistry, Vol. 45, Issue 11 https://doi.org/10.1021/bi051983l	journal	March 2006
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein Marina, Alberto; Waldburger, Carey D.; Hendrickson, Wayne A. The EMBO Journal, Vol. 24, Issue 24 https://doi.org/10.1038/sj.emboj.7600886	journal	December 2005

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