Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Protein–chromophore interactions controlling photoisomerization in red/green cyanobacteriochromes

Journal Article · · Photochemical & Photobiological Sciences (Online)
Abstract

Photoreceptors in the phytochrome superfamily use 15,16-photoisomerization of a linear tetrapyrrole (bilin) chromophore to photoconvert between two states with distinct spectral and biochemical properties. Canonical phytochromes include master regulators of plant growth and development in which light signals trigger interconversion between a red-absorbing 15Z dark-adapted state and a metastable, far-red-absorbing 15E photoproduct state. Distantly related cyanobacteriochromes (CBCRs) carry out a diverse range of photoregulatory functions in cyanobacteria and exhibit considerable spectral diversity. One widespread CBCR subfamily typically exhibits a red-absorbing 15Z dark-adapted state similar to that of phytochrome that gives rise to a distinct green-absorbing 15E photoproduct. This red/green CBCR subfamily also includes red-inactive examples that fail to undergo photoconversion, providing an opportunity to study protein–chromophore interactions that either promote photoisomerization or block it. In this work, we identified a conserved lineage of red-inactive CBCRs. This enabled us to identify three substitutions sufficient to block photoisomerization in photoactive red/green CBCRs. The resulting red-inactive variants faithfully replicated the fluorescence and circular dichroism properties of naturally occurring examples. Converse substitutions restored photoconversion in naturally red-inactive CBCRs. This work thus identifies protein–chromophore interactions that control the fate of the excited-state population in red/green cyanobacteriochromes.

Research Organization:
Univ. of California, Davis, CA (United States)
Sponsoring Organization:
National Institutes of Health (NIH), National Institute of General Medical Sciences (NIGMS); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0002395
OSTI ID:
1862566
Alternate ID(s):
OSTI ID: 1903632
Journal Information:
Photochemical & Photobiological Sciences (Online), Journal Name: Photochemical & Photobiological Sciences (Online) Journal Issue: 4 Vol. 21; ISSN 1474-9092
Publisher:
Springer Science + Business MediaCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (133)

Combined Mutagenesis and Kinetics Characterization of the Bilin-Binding GAF Domain of the Protein Slr1393 from the Cyanobacterium Synechocystis PCC6803 journal April 2014
Effect of the PHY Domain on the Photoisomerization Step of the Forward P r →P fr Conversion of a Knotless Phytochrome journal November 2020
A Brief History of Phytochromes journal April 2010
Contribution of hydrogen bonds to protein stability: Hydrogen Bonds and Protein Stability journal March 2014
Knowledge-based protein secondary structure assignment journal December 1995
Estimating Maximum Likelihood Phylogenies with PhyML book January 2009
MAFFT: Iterative Refinement and Additional Methods book January 2013
Analysis of the phytochrome gene family in Ceratodon purpureus by gene targeting reveals the primary phytochrome responsible for photo- and polarotropism journal March 2009
Biophysics of rhodopsins and optogenetics journal February 2020
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
VMD: Visual molecular dynamics journal February 1996
The GAF domain: an evolutionary link between diverse phototransducing proteins journal December 1997
Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, or phycoerythrobilin chromophore in Escherichia coli journal January 2006
Blue-/Green-Light-Responsive Cyanobacteriochromes Are Cell Shade Sensors in Red-Light Replete Niches journal March 2020
A Novel Photoactive GAF Domain of Cyanobacteriochrome AnPixJ That Shows Reversible Green/Red Photoconversion journal July 2008
Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria journal May 2019
Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum journal August 2019
A Photo-Labile Thioether Linkage to Phycoviolobilin Provides the Foundation for the Blue/Green Photocycles in DXCF-Cyanobacteriochromes journal January 2013
Crystal Structure of Deinococcus Phytochrome in the Photoactivated State Reveals a Cascade of Structural Rearrangements during Photoconversion journal March 2016
Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too journal December 2007
Comparison of the Forward and Reverse Photocycle Dynamics of Two Highly Similar Canonical Red/Green Cyanobacteriochromes Reveals Unexpected Differences journal January 2021
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
The Red Edge: Bilin-Binding Photoreceptors as Optogenetic Tools and Fluorescence Reporters journal October 2021
Hydrogen Bond between a Tyrosine Residue and the C -Ring Propionate Has a Direct Influence on Conformation and Absorption of the Bilin Cofactor in Red/Green Cyanobacteriochromes journal February 2021
Protonation-Dependent Structural Heterogeneity in the Chromophore Binding Site of Cyanobacterial Phytochrome Cph1 journal December 2016
Defining the Bilin Lyase Domain:  Lessons from the Extended Phytochrome Superfamily journal November 2000
Multiple Roles of a Conserved GAF Domain Tyrosine Residue in Cyanobacterial and Plant Phytochromes journal November 2005
Reconstitution of Blue−Green Reversible Photoconversion of a Cyanobacterial Photoreceptor, PixJ1, in Phycocyanobilin-Producing Escherichia coli journal March 2006
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
On the Collective Nature of Phytochrome Photoactivation journal December 2011
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
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
Real-Time Tracking of Phytochrome’s Orientational Changes During Pr Photoisomerization journal January 2012
Second-Chance Forward Isomerization Dynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme journal December 2011
Reactive Ground-State Pathways Are Not Ubiquitous in Red/Green Cyanobacteriochromes journal April 2013
A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome journal November 2005
Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome journal October 2011
Signal amplification and transduction in phytochrome photosensors journal April 2014
Smallest near-infrared fluorescent protein evolved from cyanobacteriochrome as versatile tag for spectral multiplexing journal January 2019
Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors journal November 2018
A biliverdin-binding cyanobacteriochrome from the chlorophyll d–bearing cyanobacterium Acaryochloris marina journal January 2015
Ultrafast excited-state dynamics and fluorescence deactivation of near-infrared fluorescent proteins engineered from bacteriophytochromes journal August 2015
Identification of DXCF cyanobacteriochrome lineages with predictable photocycles journal January 2015
Structural heterogeneity in a parent ground-state structure of AnPixJg2 revealed by theory and spectroscopy journal January 2017
The first molecular characterisation of blue- and red-light photoreceptors from Methylobacterium radiotolerans journal January 2020
Histidine protonation controls structural heterogeneity in the cyanobacteriochrome AnPixJg2 journal January 2021
Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803 journal January 2004
Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria journal January 2008
Phytochrome three-dimensional structures and functions journal March 2010
Phytochrome photoconversion journal June 1997
Two independent, light-sensing two-component systems in a filamentous cyanobacterium: Light sensing two component systems in journal May 2002
Harnessing phytochrome's glowing potential journal November 2004
Single-molecule dynamics of phytochrome-bound fluorophores probed by fluorescence correlation spectroscopy journal July 2006
Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome journal August 2009
Proton-transfer and hydrogen-bond interactions determine fluorescence quantum yield and photochemical efficiency of bacteriophytochrome journal April 2010
Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome journal February 2011
Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803 journal June 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
Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis journal January 2013
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
Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation journal June 2015
Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4 journal April 2018
Rational conversion of chromophore selectivity of cyanobacteriochromes to accept mammalian intrinsic biliverdin journal April 2019
Structural elements regulating the photochromicity in a cyanobacteriochrome journal January 2020
Genetic engineering of phytochrome biosynthesis in bacteria journal September 2001
The interplay between chromophore and protein determines the extended excited state dynamics in a single-domain phytochrome journal June 2020
Evolution-inspired design of multicolored photoswitches from a single cyanobacteriochrome scaffold journal June 2020
A far-red cyanobacteriochrome lineage specific for verdins journal October 2020
Crystal structure of a far-red–sensing cyanobacteriochrome reveals an atypical bilin conformation and spectral tuning mechanism journal March 2021
Metabolic Flux of Extracellular Heme Uptake in Pseudomonas aeruginosa Is Driven by the Iron-regulated Heme Oxygenase (HemO) journal April 2012
The D-ring, Not the A-ring, Rotates in Synechococcus OS-B′ Phytochrome journal December 2013
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
Cyanobacteriochrome-based photoswitchable adenylyl cyclases (cPACs) for broad spectrum light regulation of cAMP levels in cells journal April 2018
Chance and Necessity in Eye Evolution journal January 2011
Phytochrome functions in Arabidopsis development journal October 2009
A Light-Independent Allele of Phytochrome B Faithfully Recapitulates Photomorphogenic Transcriptional Networks journal January 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
Novel Photosensory Two-Component System (PixA–NixB–NixC) Involved in the Regulation of Positive and Negative Phototaxis of Cyanobacterium Synechocystis sp. PCC 6803 journal November 2011
Natural diversity provides a broad spectrum of cyanobacteriochrome-based diguanylate cyclases journal May 2021
Accounting for Solvent Accessibility and Secondary Structure in Protein Phylogenetics Is Clearly Beneficial journal March 2010
Methylovulum psychrotolerans sp. nov., a cold-adapted methanotroph from low-temperature terrestrial environments, and emended description of the genus Methylovulum journal June 2016
The Arabidopsis HY2 Gene Encodes Phytochromobilin Synthase, a Ferredoxin-Dependent Biliverdin Reductase journal February 2001
Functional Genomic Analysis of the HY2 Family of Ferredoxin-Dependent Bilin Reductases from Oxygenic Photosynthetic Organisms journal April 2001
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome journal August 2018
Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803: c-di-GMP controls cyanobacterial phototaxis journal June 2012
Homologous expression of a bacterial phytochrome: The cyanobacterium Fremyella diplosiphon incorporates biliverdin as a genuine, functional chromophore journal March 2007
Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics: Characterization of two cyanobacteriochromes journal November 2011
Light-dependent gene activation in A spergillus nidulans is strictly dependent on phytochrome and involves the interplay of phytochrome and white collar-regulated histone H3 acetylation: Light regulation in A. nidulans journal June 2015
The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2 journal January 2017
Phytochrome evolution in 3D: deletion, duplication, and diversification journal November 2019
The shade-avoidance syndrome: multiple signals and ecological consequences: Neighbour detection and shade avoidance journal March 2017
There and Back Again: Loss and Reacquisition of Two-Cys Photocycles in Cyanobacteriochromes journal May 2017
Distinctive Properties of Dark Reversion Kinetics between Two Red/Green-Type Cyanobacteriochromes and their Application in the Photoregulation of cAMP Synthesis journal May 2017
Common Structural Elements in the Chromophore Binding Pocket of the Pfr State of Bathy Phytochromes journal May 2017
The Expanded Red/Green Cyanobacteriochrome Lineage: An Evolutionary Hot Spot journal May 2017
Role of Melanopsin in Circadian Responses to Light journal December 2002
Structural Basis of a Phototropin Light Switch journal September 2003
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light journal August 2014
A Cyanobacterial Phytochrome Two-Component Light Sensory System journal September 1997
Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein journal May 2016
Phytochrome B integrates light and temperature signals in Arabidopsis journal October 2016
Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme journal December 2014
Draft Genome Sequence of Methylovulum psychrotolerans Sph1 T , an Obligate Methanotroph from Low-Temperature Environments journal March 2018
Red- and Blue-Light Sensing in the Plant Pathogen Alternaria alternata Depends on Phytochrome and the White-Collar Protein LreA journal April 2019
Light Regulation of Plant Defense journal April 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
Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum” journal January 2013
The photophysics and photochemistry of the plant photosensor pigment phytochrome journal January 1984
RfpA, RfpB, and RfpC are the Master Control Elements of Far-Red Light Photoacclimation (FaRLiP) journal November 2015
Photoconversion and Fluorescence Properties of a Red/Green-Type Cyanobacteriochrome AM1_C0023g2 That Binds Not Only Phycocyanobilin But Also Biliverdin journal April 2016
Fluorescence Properties of a Novel Cyanobacteriochrome GAF Domain from Spirulina that Exhibits Moderate Dark Reversion journal August 2018
The Cruciality of Single Amino Acid Replacement for the Spectral Tuning of Biliverdin-Binding Cyanobacteriochromes journal August 2020
Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria journal December 2014
Effect of circularly polarized light on germination, hypocotyl elongation and biomass production of arabidopsis and lettuce: Involvement of phytochrome B journal January 2020