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Title: There and Back Again: Loss and Reacquisition of Two‐Cys Photocycles in Cyanobacteriochromes

Journal Article · · Photochemistry and Photobiology
DOI: https://doi.org/10.1111/php.12708 · OSTI ID:1401740
 [1];  [1];  [1]
  1. Department of Molecular and Cellular Biology University of California Davis CA

Abstract Cyanobacteriochromes (CBCRs) are cyanobacterial photoreceptors distantly related to phytochromes. Both families use linear tetrapyrrole (bilin) chromophores that are covalently attached to a conserved Cys residue. CBCRs are more spectrally diverse than phytochromes, with known examples detecting light from the near ultraviolet to the edge of the infrared (370‐750 nm). Detection of ultraviolet to blue light by CBCRs is mediated by a second Cys residue, which forms a covalent linkage to the bilin C10 atom. Second linkage formation is best understood in a subfamily possessing a conserved Asp‐Xaa‐Cys‐Phe (DXCF) motif. Some DXCF CBCRs can isomerize their phycocyanobilin (PCB) chromophores into phycoviolobilin (PVB), a property not reported for other lineages. Both the DXCF Cys and PVB formation have been lost during evolution of other CBCR subfamilies. Using phylogenetic analysis and characterization of recombinantly expressed CBCRs, we show that the DXCF Cys residue has also been reacquired during CBCR evolution. Guided by this knowledge, we successfully reintroduced a second cysteine into a red/green CBCR, restoring blue‐light sensing and PVB formation with two additional substitutions. Our results validate the roles of these residues in CBCR spectral tuning and thus provide new insight into the molecular basis of their spectral diversity.

Sponsoring Organization:
USDOE
OSTI ID:
1401740
Journal Information:
Photochemistry and Photobiology, Journal Name: Photochemistry and Photobiology Journal Issue: 3 Vol. 93; ISSN 0031-8655
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (72)

Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features journal December 1983
A Brief History of Phytochromes journal April 2010
Estimating Maximum Likelihood Phylogenies with PhyML book January 2009
Type I and type II reversible photochemistry of phycoerythrocyanin α-subunit from Mastigocladus laminosus both involve Z, E isomerization of phycoviolobilin chromophore and are controlled by sulfhydryls in apoprotein journal March 1995
Type I reversible photochemistry of phycoerythrocyanin involves Z/E-isomerization of α-84 phycoviolobilin chromophore journal March 1995
Biosynthesis and Biological Functions of Bilins book January 2003
A Novel Photoactive GAF Domain of Cyanobacteriochrome AnPixJ That Shows Reversible Green/Red Photoconversion journal July 2008
A Photo-Labile Thioether Linkage to Phycoviolobilin Provides the Foundation for the Blue/Green Photocycles in DXCF-Cyanobacteriochromes journal January 2013
Phytochrome signaling mechanisms and the control of plant development journal November 2011
Characterization of Red/Green Cyanobacteriochrome NpR6012g4 by Solution Nuclear Magnetic Resonance Spectroscopy: A Hydrophobic Pocket for the C15- E,anti Chromophore in the Photoproduct journal June 2015
A Red/Green Cyanobacteriochrome Sustains Its Color Despite a Change in the Bilin Chromophore’s Protonation State journal September 2015
Identification of Cyanobacteriochromes Detecting Far-Red Light journal July 2016
Color Tuning in Red/Green Cyanobacteriochrome AnPixJ: Photoisomerization at C15 Causes an Excited-State Destabilization journal July 2015
Defining the Bilin Lyase Domain:  Lessons from the Extended Phytochrome Superfamily journal November 2000
Biliverdin Amides Reveal Roles for Propionate Side Chains in Bilin Reductase Recognition and in Holophytochrome Assembly and Photoconversion journal July 2010
The Cyanobacteriochrome, TePixJ, Isomerizes Its Own Chromophore by Converting Phycocyanobilin to Phycoviolobilin journal February 2011
Photoconversion Mechanism of a Green/Red Photosensory Cyanobacteriochrome AnPixJ: Time-Resolved Optical Spectroscopy and FTIR Analysis of the AnPixJ-GAF2 Domain journal July 2011
Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme . 1. Forward Dynamics journal January 2012
Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme . 2. Reverse Dynamics journal January 2012
Phycoviolobilin Formation and Spectral Tuning in the DXCF Cyanobacteriochrome Subfamily journal February 2012
Mechanistic Insight into the Photosensory Versatility of DXCF Cyanobacteriochromes journal April 2012
Red/Green Cyanobacteriochromes: Sensors of Color and Power journal November 2012
Photoconversion Mechanism of the Second GAF Domain of Cyanobacteriochrome AnPixJ and the Cofactor Structure of Its Green-Absorbing State journal July 2013
Primary and Secondary Photodynamics of the Violet/Orange Dual-Cysteine NpF2164g3 Cyanobacteriochrome Domain from Nostoc punctiforme journal February 2014
Conserved Phenylalanine Residues Are Required for Blue-Shifting of Cyanobacteriochrome Photoproducts journal May 2014
A New Type of Dual-Cys Cyanobacteriochrome GAF Domain Found in Cyanobacterium Acaryochloris marina , Which Has an Unusual Red/Blue Reversible Photoconversion Cycle journal July 2014
Conservation and Diversity in the Primary Forward Photodynamics of Red/Green Cyanobacteriochromes journal January 2015
Characterization of Red/Green Cyanobacteriochrome NpR6012g4 by Solution Nuclear Magnetic Resonance Spectroscopy: A Protonated Bilin Ring System in Both Photostates journal April 2015
A Second Conserved GAF Domain Cysteine Is Required for the Blue/Green Photoreversibility of Cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus journal July 2008
Second-Chance Forward Isomerization Dynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme journal December 2011
Chemical Inhomogeneity in the Ultrafast Dynamics of the DXCF Cyanobacteriochrome Tlr0924 journal July 2012
Reactive Ground-State Pathways Are Not Ubiquitous in Red/Green Cyanobacteriochromes journal April 2013
Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome journal October 2011
Photoconversion changes bilin chromophore conjugation and protein secondary structure in the violet/orange cyanobacteriochrome NpF2163g3 journal January 2014
NpR3784 is the prototype for a distinctive group of red/green cyanobacteriochromes using alternative Phe residues for photoproduct tuning journal January 2015
Identification of DXCF cyanobacteriochrome lineages with predictable photocycles journal January 2015
Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria journal January 2008
Engineered photoreceptors as novel optogenetic tools journal January 2010
Phytochrome three-dimensional structures and functions journal March 2010
Two independent, light-sensing two-component systems in a filamentous cyanobacterium: Light sensing two component systems in journal May 2002
Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein journal July 2008
Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter journal April 2010
Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome journal February 2011
Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula journal May 2011
Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes journal June 2011
Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism journal December 2012
Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle journal March 2013
Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803 journal June 2001
Eukaryotic algal phytochromes span the visible spectrum journal February 2014
Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation journal June 2015
Genetic engineering of phytochrome biosynthesis in bacteria journal September 2001
Dynamic Structural Changes Underpin Photoconversion of a Blue/Green Cyanobacteriochrome between Its Dark and Photoactivated States journal December 2013
Cyanobacteriochrome SesA Is a Diguanylate Cyclase That Induces Cell Aggregation in Thermosynechococcus journal July 2014
Phytochrome functions in Arabidopsis development journal October 2009
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Novel Putative Photoreceptor and Regulatory Genes Required for the Positive Phototactic Movement of the Unicellular Motile Cyanobacterium Synechocystis sp. PCC 6803 journal December 2000
Cyanobacterial Phytochrome-like PixJ1 Holoprotein Shows Novel Reversible Photoconversion Between Blue- and Green-absorbing Forms journal December 2004
Cyanobacteriochrome TePixJ of Thermosynechococcus elongatus Harbors Phycoviolobilin as a Chromophore journal July 2007
Accounting for Solvent Accessibility and Secondary Structure in Protein Phylogenetics Is Clearly Beneficial journal March 2010
Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites journal July 2011
Adaptive and acclimative responses of cyanobacteria to far-red light: Responses of cyanobacteria to far-red light journal August 2015
A rising tide of blue-absorbing biliprotein photoreceptors - characterization of seven such bilin-binding GAF domains in Nostoc sp. PCC7120 journal October 2012
Probing protein-chromophore interactions in Cph1 phytochrome by mutagenesis journal April 2006
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light journal August 2014
Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors journal September 1996
A Cyanobacterial Phytochrome Two-Component Light Sensory System journal September 1997
Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme journal December 2014
Phytochrome Cytoplasmic Signaling journal April 2013
Photoreceptor Signaling Networks in Plant Responses to Shade journal April 2013
Phytochrome Structure and Signaling Mechanisms journal June 2006
Responding to Color: The Regulation of Complementary Chromatic Adaptation journal June 2006
RfpA, RfpB, and RfpC are the Master Control Elements of Far-Red Light Photoacclimation (FaRLiP) journal November 2015