Characterization of the genuine type 2 chromatic acclimation in the two Geminocystis cyanobacteria

Hirose, Yuu; Misawa, Nobuo; Yonekawa, Chinatsu; Nagao, Nobuyoshi; Watanabe, Masayo; Ikeuchi, Masahiko; Eki, Toshihiko

doi:10.1093/dnares/dsx011

Cited by 18 publications

(13 citation statements)

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“…Characterization of Novel Types of CA Regulating PEC and CpcL ccaS and ccaR are typically clustered with the PBS genes they regulate (Hirose et al, 2017). Following an extensive survey of the $1300 strains of cyanobacteria genomes in GenBank (Benson et al, 2018), we identified five variations in the composition of PBS genes in the ccaS gene cluster (Figure 1A and Supplemental Figure 1).…”

Section: Resultsmentioning

confidence: 99%

“…In brief, PCC 6406 cells were grown in liquid BG11 medium containing 10% (v/v) ASN-III medium bubbled with air containing 1% (v/v) CO 2 at 26 C. Cells were illuminated with 20 mE m À2 s À1 green light (peak at 524 nm) or 15 mE m À2 s À1 red light (peak at 658 nm). Spectroscopy and RNA-seq were performed as described previously with minor modifications (Hirose et al, 2017). For PBS isolation, cells were lysed with 0.65 M potassium phosphate (pH 7.0) containing 2% (v/v) Triton X-100 and 0.5% (w/v) DM.…”

Section: Methodsmentioning

confidence: 99%

“…In addition, transcriptional regulation of a rod-membrane linker (cpcL) for the rod-shaped PBS was characterized in Synechocystis sp. PCC 6803 and Nostoc punctiforme ATCC 29133 (Katayama and Ikeuchi, 2006;Hirose et al, 2008Hirose et al, , 2010; cpcL regulation was proposed to be CA0, but this has never been proved biochemically (Hirose et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria

et al. 2019

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Cyanobacteria have evolved various photoacclimation processes to perform oxygenic photosynthesis under different light environments. Chromatic acclimation (CA) is a widely recognized and ecologically important type of photoacclimation, whereby cyanobacteria alter the absorbing light colors of a supermolecular antenna complex called the phycobilisome. To date, several CA variants that regulate the green-absorbing phycoerythrin (PE) and/or the red-absorbing phycocyanin (PC) within the hemi-discoidal form of phycobilisome have been characterized. In this study, we identified a unique CA regulatory gene cluster encoding yellow-green-absorbing phycoerythrocyanin (PEC) and a rod-membrane linker protein (CpcL) for the rod-shaped form of phycobilisome. Using the cyanobacterium Leptolyngbya sp. PCC 6406, we revealed novel CA variants regulating PEC (CA7) and the rod-shaped phycobilisome (CA0), which maximize yellowgreen light-harvesting capacity and balance the excitation of photosystems, respectively. Analysis of the distribution of CA gene clusters in 445 cyanobacteria genomes revealed eight CA variants responding to green and red light, which are classified based on the presence of PEC, PE, cpcL, and CA photosensor genes. Phylogenetic analysis further suggested that the emergence of CA7 was a single event and preceded that of heterocystous strains, whereas the acquisition of CA0 occurred multiple times. Taken together, these results offer novel insights into the diversity and evolution of the complex cyanobacterial photoacclimation mechanisms.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria

et al. 2019

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“…Phycoerythrin (PE) is a bioactive pigment mainly found in Rhodophyta, but it can also be recovered from Cyanobacteria [1]. This water-soluble pigment is a bioactive molecule with interesting properties such as anti-inflammatory, immunosuppressive, antitumor, antioxidant, antidiabetic, and antihypertensive effects [2,3,4,5].…”

Section: Introductionmentioning

confidence: 99%

Light Intensity and Nitrogen Concentration Impact on the Biomass and Phycoerythrin Production by Porphyridium purpureum

et al. 2019

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Several factors have the potential to influence microalgae growth. In the present study, nitrogen concentration and light intensity were evaluated in order to obtain high biomass production and high phycoerythrin accumulation from Porphyridium purpureum. The range of nitrogen concentrations evaluated in the culture medium was 0.075–0.450 g L−1 and light intensities ranged between 30 and 100 μmol m−2 s−1. Surprisingly, low nitrogen concentration and high light intensity resulted in high biomass yield and phycoerythrin accumulation. Thus, the best biomass productivity (0.386 g L−1 d−1) and biomass yield (5.403 g L−1) were achieved with NaNO3 at 0.075 g L−1 and 100 μmol m−2 s−1. In addition, phycoerythrin production was improved to obtain a concentration of 14.66 mg L−1 (2.71 mg g−1 of phycoerythrin over dry weight). The results of the present study indicate that it is possible to significantly improve biomass and pigment production in Porphyridium purpureum by limiting nitrogen concentration and light intensity.

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“…Cyanobacteria harbor up to several dozen different bilin-binding GAF domains (26), and a single CBCR protein often contains multiple GAF domains (27), suggesting that cyanobacteria utilize a highly complex photosensing system. Although some CBCRs have been shown to regulate the composition of photosynthetic antenna (4,(28)(29)(30)(31), cell morphology (32), phototaxis (33), and cell aggregation (34,35), the physiological role of most CBCRs remains unknown. RcaE and CcaS are members of the green/red CBCR subfamily and optimize the light-absorption maxima of the photosynthetic antenna complex phycobilisome via transcriptional regulation of its components in a process called "chromatic acclimation".…”

Section: Introductionmentioning

confidence: 99%

Structural basis of the protochromic green/red photocycle of the chromatic acclimation sensor RcaE

Nagae

Unno

Koizumi

et al. 2020

Preprint

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Cyanobacteriochromes (CBCRs) are bilin-binding photosensors of the phytochrome superfamily that show remarkable spectral diversity. The green/red CBCR subfamily is important for regulating chromatic acclimation of photosynthetic antenna in cyanobacteria and is applied for optogenetic control of gene expression in synthetic biology. They are suggested to combine the bilin C15-Z/C15-E photoisomerization with a change in the bilin protonation state to drive their absorption changes. However, structural information and direct evidence of the bilin protonation state are lacking. Here we report a high-resolution (1.63Å) crystal structure of the bilin-binding domain of the chromatic acclimation sensor RcaE in the red-absorbing photoproduct state. The bilin is buried within a “pan” consisting of hydrophobic residues, where the bilin configuration/conformation is C5-Z,syn/C10-Z,syn/C15-E,syn with the A–C rings co-planar and the D-ring tilted. Three pyrrole nitrogens of the A–C rings are covered in the α-face with a hydrophobic lid of Leu249 influencing the bilin pKa, whereas they are directly hydrogen-bonded in the β-face with the carboxyl group of Glu217. Glu217 is further connected to a cluster of waters forming a hole in the pan, which are in exchange with solvent waters in molecular dynamics simulation. We propose that the “holey pan” structure functions as a proton-exit/influx pathway upon photoconversion. NMR analysis demonstrated that the four pyrrole nitrogen atoms are indeed fully protonated in the red-absorbing state, but one of them, most likely the B-ring nitrogen, is deprotonated in the green-absorbing state. These findings deepen our understanding of the diverse spectral tuning mechanisms present in CBCRs.Significance StatementGreen/red CBCRs are one of the most important CBCR subfamilies owing to their physiological roles in cyanobacteria phylum and optogenetic applications. They are known to utilize a change in the bilin protonation state to drive the marked change in green/red absorption, but the structural basis of the protochromic green/red photocycle are not well understood. Here, we have determined the crystal structure of the chromatic acclimation sensor RcaE of this subfamily in the photoproduct state, demonstrating a unique conformation of the bilin and its interacting residues. In addition, we provide direct evidence of the protonation state of the bilin via NMR analysis. These findings bring insight to our understanding of the molecular mechanisms underlying the spectral diversity of CBCRs.

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Characterization of the genuine type 2 chromatic acclimation in the two Geminocystis cyanobacteria

Cited by 18 publications

References 50 publications

Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria

Diverse Chromatic Acclimation Processes Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria

Light Intensity and Nitrogen Concentration Impact on the Biomass and Phycoerythrin Production by Porphyridium purpureum

Structural basis of the protochromic green/red photocycle of the chromatic acclimation sensor RcaE

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