Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

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

doi:10.1073/pnas.2300770120

Title: Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Abstract

Terrestrial ecosystems and human societies depend on oxygenic photosynthesis, which began to reshape our atmosphere approximately 2.5 billion years ago. The earliest known organisms carrying out oxygenic photosynthesis are the cyanobacteria, which use large complexes of phycobiliproteins as light-harvesting antennae. Phycobiliproteins rely on phycocyanobilin (PCB), a linear tetrapyrrole (bilin) chromophore, as the light-harvesting pigment that transfers absorbed light energy from phycobilisomes to the chlorophyll-based photosynthetic apparatus. Cyanobacteria synthesize PCB from heme in two steps: A heme oxygenase converts heme into biliverdin IXα (BV), and the ferredoxin-dependent bilin reductase (FDBR) PcyA then converts BV into PCB. In the current work, we examine the origins of this pathway. We demonstrate that PcyA evolved from pre-PcyA proteins found in nonphotosynthetic bacteria and that pre-PcyA enzymes are active FDBRs that do not yield PCB. Pre-PcyA genes are associated with two gene clusters. Both clusters encode bilin-binding globin proteins, phycobiliprotein paralogs that we designate as BBAGs (bilin biosynthesis-associated globins). Some cyanobacteria also contain one such gene cluster, including a BBAG, two V4R proteins, and an iron–sulfur protein. Phylogenetic analysis shows that this cluster is descended from those associated with pre-PcyA proteins and that light-harvesting phycobiliproteins are also descended from BBAGs found in other bacteria. Wemore »« less

Authors:

^[1]; Martin, Shelley S. ^[1];

^[1]

College of Biological Sciences, Department of Molecular and Cell Biology, University of California at Davis, Davis, CA 95616

Publication Date:: Tue Apr 18 00:00:00 EDT 2023

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

OSTI Identifier:: 1970392

Grant/Contract Number:: SC0002395

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 120 Journal Issue: 17; Journal ID: ISSN 0027-8424

Publisher:: Proceedings of the National Academy of Sciences

Country of Publication:: United States

Language:: English

Citation Formats


                    Rockwell, Nathan C., Martin, Shelley S., and Lagarias, J. Clark. Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins.  United States: N. p., 2023. 
Web.  doi:10.1073/pnas.2300770120.

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                    Rockwell, Nathan C., Martin, Shelley S., & Lagarias, J. Clark. Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins.  United States.  https://doi.org/10.1073/pnas.2300770120

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                    Rockwell, Nathan C., Martin, Shelley S., and Lagarias, J. Clark. Tue .  
"Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins".  United States.  https://doi.org/10.1073/pnas.2300770120.

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@article{osti_1970392,

  title        = {Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins},

  author       = {Rockwell, Nathan C. and Martin, Shelley S. and Lagarias, J. Clark},

  abstractNote = {Terrestrial ecosystems and human societies depend on oxygenic photosynthesis, which began to reshape our atmosphere approximately 2.5 billion years ago. The earliest known organisms carrying out oxygenic photosynthesis are the cyanobacteria, which use large complexes of phycobiliproteins as light-harvesting antennae. Phycobiliproteins rely on phycocyanobilin (PCB), a linear tetrapyrrole (bilin) chromophore, as the light-harvesting pigment that transfers absorbed light energy from phycobilisomes to the chlorophyll-based photosynthetic apparatus. Cyanobacteria synthesize PCB from heme in two steps: A heme oxygenase converts heme into biliverdin IXα (BV), and the ferredoxin-dependent bilin reductase (FDBR) PcyA then converts BV into PCB. In the current work, we examine the origins of this pathway. We demonstrate that PcyA evolved from pre-PcyA proteins found in nonphotosynthetic bacteria and that pre-PcyA enzymes are active FDBRs that do not yield PCB. Pre-PcyA genes are associated with two gene clusters. Both clusters encode bilin-binding globin proteins, phycobiliprotein paralogs that we designate as BBAGs (bilin biosynthesis-associated globins). Some cyanobacteria also contain one such gene cluster, including a BBAG, two V4R proteins, and an iron–sulfur protein. Phylogenetic analysis shows that this cluster is descended from those associated with pre-PcyA proteins and that light-harvesting phycobiliproteins are also descended from BBAGs found in other bacteria. We propose that PcyA and phycobiliproteins originated in heterotrophic, nonphotosynthetic bacteria and were subsequently acquired by cyanobacteria.},

  doi          = {10.1073/pnas.2300770120},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 17,

  volume       = 120,

  place        = {United States},

  year         = {Tue Apr 18 00:00:00 EDT 2023},

  month        = {Tue Apr 18 00:00:00 EDT 2023}

}

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The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2

Journal Article Rockwell, Nathan C. ; Martin, Shelley S. ; Li, Fay‐Wei ; ... - New Phytologist

Summary Land plant phytochromes perceive red and far‐red light to control growth and development, using the linear tetrapyrrole (bilin) chromophore phytochromobilin (PΦB). Phytochromes from streptophyte algae, sister species to land plants, instead use phycocyanobilin ( PCB ). PCB and PΦB are synthesized by different ferredoxin‐dependent bilin reductases ( FDBR s): PΦB is synthesized by HY 2, whereas PCB is synthesized by PcyA. The pathway for PCB biosynthesis in streptophyte algae is unknown. We used phylogenetic analysis and heterologous reconstitution of bilin biosynthesis to investigate bilin biosynthesis in streptophyte algae. Phylogenetic results suggest that PcyA is present in chlorophytes and prasinophytesmore »« less
Cited by 16
https://doi.org/10.1111/nph.14422
Insight Into the Radical Mechanism of Phycocyanobilin-Ferredoxin Oxidoreductase (Pcya) Revealed By X-Ray Crystallography And Biochemical Measurements

Journal Article Tu, S -L ; Rockwell, N ; Lagarias, J C ; ... - Biochem.46:1484-1494,2007

The X-ray crystal structure of the substrate-free form of phycocyanobilin (PCB)-ferredoxin oxidoreductase (PcyA; EC 1.3.7.5) from the cyanobacterium Nostoc sp. PCC7120 has been solved at 2.5 angstrom resolution. A comparative analysis of this structure with those recently reported for substrate-bound and substrate-free forms of PcyA from the cyanobacterium Synechocystis sp. PCC6803 (Hagiwara et al. (2006) Proc. Natl. Acad. Sci. U.S.A. 103, 27-32; Hagiwara et al. (2006) FEBS Lett. 580, 3823-3828) provides a compelling picture of substrate-induced changes in the PcyA enzyme and the chemical basis of PcyA's catalytic activity. On the basis of these structures and the biochemical analysis ofmore »« less
https://doi.org/10.1021/bi062038f
Roles of CpcF and CpcG1 in Peroxiredoxin-Mediated Oxidative Stress Responses and Cellular Fitness in the Cyanobacterium Synechocystis sp. PCC 6803

Journal Article Oh, Sookyung ; Montgomery, Beronda L. - Frontiers in Microbiology

As a component of the photosynthetic apparatus in cyanobacteria, the phycobilisome (PBS) plays an important role in harvesting and transferring light energy to the core photosynthetic reaction centers. The size, composition (phycobiliprotein and chromophore), and assembly of PBSs can be dynamic to cope with tuning photosynthesis and associated cellular fitness in variable light environments. Here, we explore the role of PBS-related stress responses by analyzing deletion mutants of cpcF or cpcG1 genes in Synechocystis sp. PCC 6803. The cpcF gene encodes a lyase that links the phycocyanobilin (PCB) chromophore to the alpha subunit of phycocyanin (PC), a central phycobiliprotein (PBP)more »« less
Cited by 6
https://doi.org/10.3389/fmicb.2019.01059
Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

Journal Article Wittkopp, Tyler M. ; Schmollinger, Stefan ; Saroussi, Shai ; ... - The Plant Cell

In land plants, linear tetrapyrrole (bilin)-based phytochrome photosensors optimize photosynthetic light capture by mediating massive reprogramming of gene expression. But, surprisingly, many green algal genomes lack phytochrome genes. Studies of the heme oxygenase mutant (hmox1) of the green alga Chlamydomonas reinhardtii suggest that bilin biosynthesis in plastids is essential for proper regulation of a nuclear gene network implicated in oxygen detoxification during dark-to-light transitions. hmox1 cannot grow photoautotrophically and photoacclimates poorly to increased illumination. We show that these phenotypes are due to reduced accumulation of photosystem I (PSI) reaction centers, the PSI electron acceptors 5'-monohydroxyphylloquinone and phylloquinone, and the lossmore »« less
Cited by 19
https://doi.org/10.1105/tpc.17.00149
Direct single-molecule measurements of phycocyanobilin photophysics in monomeric C-phycocyanin

Journal Article Squires, Allison H. ; Moerner, W. E. - Proceedings of the National Academy of Sciences of the United States of America

Phycobilisomes are highly organized pigment-protein antenna complexes found in the photosynthetic apparatus of cyanobacteria and rhodophyta that harvest solar energy and transport it to the reaction center. A detailed bottom-up model of pigment organization and energy transfer in phycobilisomes is essential to understanding photosynthesis in these organisms, and informing rational design of artificial light-harvesting systems. Particularly, heterogeneous photophysical behaviors of these proteins, which cannot be predicted de novo, may play an essential role in rapid light adaptation and photoprotection. Furthermore, the delicate architecture of these pigment-protein scaffolds sensitizes them to external perturbations, e.g: surface attachment, which can be avoided bymore »« less
Cited by 30
https://doi.org/10.1073/pnas.1705435114

Similar Records

Title: Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Abstract

Citation Formats

Oxygen-independent Coproporphyrinogen-III Oxidase HemN from Escherichia coli journal, July 2002

Slr0151 in Synechocystis sp. PCC 6803 is required for efficient repair of photosystem II under high-light condition: Role of Slr0151 in PSII repair of Synechocystis journal, September 2014

Responding to Color: The Regulation of Complementary Chromatic Adaptation journal, June 2006

Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism journal, January 2000

Radical new paradigm for heme degradation in Escherichia coli O157:H7 journal, October 2016

Evolution and molecular mechanism of four‐electron reducing ferredoxin‐dependent bilin reductases from oceanic phages journal, December 2017

Fluorescence Properties of C-Phycocyanin Isolated from a Thermophilic Cyanobacterium journal, August 1984

Renewing Felsenstein’s phylogenetic bootstrap in the era of big data journal, April 2018

Genetic engineering of phytochrome biosynthesis in bacteria journal, September 2001

New biosynthetic pathway for pink pigments from uncultured oceanic viruses: Viral pink pigments journal, April 2016

The Role of Slr0151, a Tetratricopeptide Repeat Protein from Synechocystis sp. PCC 6803, during Photosystem II Assembly and Repair journal, May 2016

Data access for the 1,000 Plants (1KP) project journal, October 2014

Prokaryotic Heme Biosynthesis: Multiple Pathways to a Common Essential Product journal, January 2017

Crystal structure of the first eukaryotic bilin reductase GtPEBB reveals a flipped binding mode of dihydrobiliverdin journal, September 2019

Heterogeneous Photodynamics of the P fr State in the Cyanobacterial Phytochrome Cph1 journal, July 2014

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal, September 1997

The Cyanobacteriochrome, TePixJ, Isomerizes Its Own Chromophore by Converting Phycocyanobilin to Phycoviolobilin journal, February 2011

Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme . 2. Reverse Dynamics journal, January 2012

High Sensitivity Proteomics Assisted Discovery of a Novel Operon Involved in the Assembly of Photosystem II, a Membrane Protein Complex journal, August 2008

Interplay of SpkG kinase and the Slr0151 protein in the phosphorylation of ferredoxin 5 in Synechocystis sp. strain PCC 6803 journal, February 2018

Protein–chromophore interactions controlling photoisomerization in red/green cyanobacteriochromes journal, April 2022

Insights into the Proton Transfer Mechanism of a Bilin Reductase PcyA Following Neutron Crystallography journal, April 2015

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome journal, March 2020

Photoglobin, a distinct family of non-heme binding globins, defines a potential photosensor in prokaryotic signal transduction systems journal, January 2022

Identification of Cyanobacteriochromes Detecting Far-Red Light journal, July 2016

Genomic and Phenotypic Characterization of Chloracidobacterium Isolates Provides Evidence for Multiple Species journal, June 2021

Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae journal, November 2021

Functional Differentiation of Two Analogous Coproporphyrinogen III Oxidases for Heme and Chlorophyll Biosynthesis Pathways in the Cyanobacterium Synechocystis sp. PCC 6803 journal, April 2010

Structure of a nonheme globin in environmental stress signaling journal, November 2005

Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria journal, May 2019

The phytofluors: a new class of fluorescent protein probes journal, November 1997

Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms journal, January 2008

Type I reversible photochemistry of phycoerythrocyanin involves Z/E-isomerization of α-84 phycoviolobilin chromophore journal, March 1995

Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803 journal, January 2004

Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals journal, October 2015

A Cyanobacterial Phytochrome Two-Component Light Sensory System journal, September 1997

Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes journal, December 2003

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle journal, March 2013

New Insight into the Mechanism of Anaerobic Heme Degradation journal, October 2019

Distinct phytochrome actions in nonvascular plants revealed by targeted inactivation of phytobilin biosynthesis journal, May 2012

A new view of the tree of life journal, April 2016

Structure of phycobilisome from the red alga Griffithsia pacifica journal, October 2017

Attachment of Noncognate Chromophores to CpcA of Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 by Heterologous Expression in Escherichia coli journal, June 2011

Crystal Structure of Red Chlorophyll Catabolite Reductase: Enlargement of the Ferredoxin-Dependent Bilin Reductase Family journal, June 2009

Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria journal, March 2008

Back from the dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus journal, January 2015

Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4 journal, April 2018

On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria journal, March 2017

Novel Predators Reshape Holozoan Phylogeny and Reveal the Presence of a Two-Component Signaling System in the Ancestor of Animals journal, July 2017

Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea journal, December 2019

Functional Genomic Analysis of the HY2 Family of Ferredoxin-Dependent Bilin Reductases from Oxygenic Photosynthetic Organisms journal, April 2001

The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2 journal, January 2017

Fungal phytochrome chromophore biosynthesis at mitochondria journal, July 2021

MAFFT: Iterative Refinement and Additional Methods book, January 2013

VMD: Visual molecular dynamics journal, February 1996

Crystal Structure of the Oxygen-dependant Coproporphyrinogen Oxidase (Hem13p) of Saccharomyces cerevisiae journal, September 2004

Red/Green Cyanobacteriochromes: Sensors of Color and Power journal, November 2012

Light Harvesting by Phycobilisomes journal, June 1985

A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer journal, March 2007

A novel thylakoid-less isolate fills a billion-year gap in the evolution of Cyanobacteria journal, July 2021

A Second Conserved GAF Domain Cysteine Is Required for the Blue/Green Photoreversibility of Cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus † journal, July 2008

Multiple Roles of a Conserved GAF Domain Tyrosine Residue in Cyanobacterial and Plant Phytochromes † journal, November 2005

Functional assignment of chromophores and energy transfer in C phycocyanin isolated from the thermophilic cyanobacterium Mastigocladus laminosus journal, February 1986

Effects of Modified Phycobilin Biosynthesis in the Cyanobacterium Synechococcus sp. Strain PCC 7002 journal, February 2011

Conserved Phenylalanine Residues Are Required for Blue-Shifting of Cyanobacteriochrome Photoproducts journal, May 2014

Mechanistic Insight into the Photosensory Versatility of DXCF Cyanobacteriochromes journal, April 2012

Phycoerythrobilin Synthase (PebS) of a Marine Virus journal, October 2008

Structural Insights into Vinyl Reduction Regiospecificity of Phycocyanobilin:Ferredoxin Oxidoreductase (PcyA) journal, January 2010

The Arabidopsis HY2 Gene Encodes Phytochromobilin Synthase, a Ferredoxin-Dependent Biliverdin Reductase journal, February 2001

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

Comparative Analysis of the Primary Transcriptome of Synechocystis sp. PCC 6803 journal, June 2014

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity journal, October 2017

Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, or phycoerythrobilin chromophore in Escherichia coli journal, January 2006

Highly accurate protein structure prediction with AlphaFold journal, July 2021

Gene family innovation, conservation and loss on the animal stem lineage journal, May 2018

Function and Regulation of Ferredoxins in the Cyanobacterium, Synechocystis PCC6803: Recent Advances journal, November 2014

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis journal, January 2023

Oxygen-independent Coproporphyrinogen-III Oxidase HemN from Escherichia coli
journal, July 2002

Slr0151 in Synechocystis sp. PCC 6803 is required for efficient repair of photosystem II under high-light condition: Role of Slr0151 in PSII repair of Synechocystis
journal, September 2014

Responding to Color: The Regulation of Complementary Chromatic Adaptation
journal, June 2006

Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism
journal, January 2000

Radical new paradigm for heme degradation in Escherichia coli O157:H7
journal, October 2016

Evolution and molecular mechanism of four‐electron reducing ferredoxin‐dependent bilin reductases from oceanic phages
journal, December 2017

Fluorescence Properties of C-Phycocyanin Isolated from a Thermophilic Cyanobacterium
journal, August 1984

Renewing Felsenstein’s phylogenetic bootstrap in the era of big data
journal, April 2018

Genetic engineering of phytochrome biosynthesis in bacteria
journal, September 2001

New biosynthetic pathway for pink pigments from uncultured oceanic viruses: Viral pink pigments
journal, April 2016

The Role of Slr0151, a Tetratricopeptide Repeat Protein from Synechocystis sp. PCC 6803, during Photosystem II Assembly and Repair
journal, May 2016

Data access for the 1,000 Plants (1KP) project
journal, October 2014

Prokaryotic Heme Biosynthesis: Multiple Pathways to a Common Essential Product
journal, January 2017

Crystal structure of the first eukaryotic bilin reductase GtPEBB reveals a flipped binding mode of dihydrobiliverdin
journal, September 2019

Heterogeneous Photodynamics of the P _fr State in the Cyanobacterial Phytochrome Cph1
journal, July 2014

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

The Cyanobacteriochrome, TePixJ, Isomerizes Its Own Chromophore by Converting Phycocyanobilin to Phycoviolobilin
journal, February 2011

Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme . 2. Reverse Dynamics
journal, January 2012

High Sensitivity Proteomics Assisted Discovery of a Novel Operon Involved in the Assembly of Photosystem II, a Membrane Protein Complex
journal, August 2008

Interplay of SpkG kinase and the Slr0151 protein in the phosphorylation of ferredoxin 5 in Synechocystis sp. strain PCC 6803
journal, February 2018

Protein–chromophore interactions controlling photoisomerization in red/green cyanobacteriochromes
journal, April 2022

Insights into the Proton Transfer Mechanism of a Bilin Reductase PcyA Following Neutron Crystallography
journal, April 2015

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome
journal, March 2020

Photoglobin, a distinct family of non-heme binding globins, defines a potential photosensor in prokaryotic signal transduction systems
journal, January 2022

Identification of Cyanobacteriochromes Detecting Far-Red Light
journal, July 2016

Genomic and Phenotypic Characterization of Chloracidobacterium Isolates Provides Evidence for Multiple Species
journal, June 2021

Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae
journal, November 2021

Functional Differentiation of Two Analogous Coproporphyrinogen III Oxidases for Heme and Chlorophyll Biosynthesis Pathways in the Cyanobacterium Synechocystis sp. PCC 6803
journal, April 2010

Structure of a nonheme globin in environmental stress signaling
journal, November 2005

Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria
journal, May 2019

The phytofluors: a new class of fluorescent protein probes
journal, November 1997

Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms
journal, January 2008

Type I reversible photochemistry of phycoerythrocyanin involves Z/E-isomerization of α-84 phycoviolobilin chromophore
journal, March 1995

Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803
journal, January 2004

Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
journal, October 2015

A Cyanobacterial Phytochrome Two-Component Light Sensory System
journal, September 1997

Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes
journal, December 2003

Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle
journal, March 2013

New Insight into the Mechanism of Anaerobic Heme Degradation
journal, October 2019

Distinct phytochrome actions in nonvascular plants revealed by targeted inactivation of phytobilin biosynthesis
journal, May 2012

A new view of the tree of life
journal, April 2016

Structure of phycobilisome from the red alga Griffithsia pacifica
journal, October 2017

Attachment of Noncognate Chromophores to CpcA of Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 by Heterologous Expression in Escherichia coli
journal, June 2011

Crystal Structure of Red Chlorophyll Catabolite Reductase: Enlargement of the Ferredoxin-Dependent Bilin Reductase Family
journal, June 2009

Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria
journal, March 2008

Back from the dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus
journal, January 2015

Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4
journal, April 2018

On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria
journal, March 2017

Novel Predators Reshape Holozoan Phylogeny and Reveal the Presence of a Two-Component Signaling System in the Ancestor of Animals
journal, July 2017

Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea
journal, December 2019

Functional Genomic Analysis of the HY2 Family of Ferredoxin-Dependent Bilin Reductases from Oxygenic Photosynthetic Organisms
journal, April 2001

The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2
journal, January 2017

Fungal phytochrome chromophore biosynthesis at mitochondria
journal, July 2021

MAFFT: Iterative Refinement and Additional Methods
book, January 2013

VMD: Visual molecular dynamics
journal, February 1996

Crystal Structure of the Oxygen-dependant Coproporphyrinogen Oxidase (Hem13p) of Saccharomyces cerevisiae
journal, September 2004

Red/Green Cyanobacteriochromes: Sensors of Color and Power
journal, November 2012

Light Harvesting by Phycobilisomes
journal, June 1985

A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer
journal, March 2007

A novel thylakoid-less isolate fills a billion-year gap in the evolution of Cyanobacteria
journal, July 2021

A Second Conserved GAF Domain Cysteine Is Required for the Blue/Green Photoreversibility of Cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus ^†
journal, July 2008

Multiple Roles of a Conserved GAF Domain Tyrosine Residue in Cyanobacterial and Plant Phytochromes ^†
journal, November 2005

Functional assignment of chromophores and energy transfer in C phycocyanin isolated from the thermophilic cyanobacterium Mastigocladus laminosus
journal, February 1986

Effects of Modified Phycobilin Biosynthesis in the Cyanobacterium Synechococcus sp. Strain PCC 7002
journal, February 2011

Conserved Phenylalanine Residues Are Required for Blue-Shifting of Cyanobacteriochrome Photoproducts
journal, May 2014

Mechanistic Insight into the Photosensory Versatility of DXCF Cyanobacteriochromes
journal, April 2012

Phycoerythrobilin Synthase (PebS) of a Marine Virus
journal, October 2008

Structural Insights into Vinyl Reduction Regiospecificity of Phycocyanobilin:Ferredoxin Oxidoreductase (PcyA)
journal, January 2010

The Arabidopsis HY2 Gene Encodes Phytochromobilin Synthase, a Ferredoxin-Dependent Biliverdin Reductase
journal, February 2001

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

Comparative Analysis of the Primary Transcriptome of Synechocystis sp. PCC 6803
journal, June 2014

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity
journal, October 2017

Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, or phycoerythrobilin chromophore in Escherichia coli
journal, January 2006

Highly accurate protein structure prediction with AlphaFold
journal, July 2021

Gene family innovation, conservation and loss on the animal stem lineage
journal, May 2018

Function and Regulation of Ferredoxins in the Cyanobacterium, Synechocystis PCC6803: Recent Advances
journal, November 2014

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis
journal, January 2023

The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing
journal, June 2014

Novel Gloeobacterales spp. from Diverse Environments across the Globe
journal, August 2021

Flexible mapping of homology onto structure with Homolmapper
journal, April 2007