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. 2016 Feb 9;7(1):e02130-15.
doi: 10.1128/mBio.02130-15.

Two Cyanobacterial Photoreceptors Regulate Photosynthetic Light Harvesting by Sensing Teal, Green, Yellow, and Red Light

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Free PMC article

Two Cyanobacterial Photoreceptors Regulate Photosynthetic Light Harvesting by Sensing Teal, Green, Yellow, and Red Light

Lisa B Wiltbank et al. mBio. .
Free PMC article

Abstract

The genomes of many photosynthetic and nonphotosynthetic bacteria encode numerous phytochrome superfamily photoreceptors whose functions and interactions are largely unknown. Cyanobacterial genomes encode particularly large numbers of phytochrome superfamily members called cyanobacteriochromes. These have diverse light color-sensing abilities, and their functions and interactions are just beginning to be understood. One of the best characterized of these functions is the regulation of photosynthetic light-harvesting antenna composition in the cyanobacterium Fremyella diplosiphon by the cyanobacteriochrome RcaE in response to red and green light, a process known as chromatic acclimation. We have identified a new cyanobacteriochrome named DpxA that maximally senses teal (absorption maximum, 494 nm) and yellow (absorption maximum, 568 nm) light and represses the accumulation of a key light-harvesting protein called phycoerythrin, which is also regulated by RcaE during chromatic acclimation. Like RcaE, DpxA is a two-component system kinase, although these two photoreceptors can influence phycoerythrin expression through different signaling pathways. The peak responsiveness of DpxA to teal and yellow light provides highly refined color discrimination in the green spectral region, which provides important wavelengths for photosynthetic light harvesting in cyanobacteria. These results redefine chromatic acclimation in cyanobacteria and demonstrate that cyanobacteriochromes can coordinately impart sophisticated light color sensing across the visible spectrum to regulate important photosynthetic acclimation processes.

Importance: The large number of cyanobacteriochrome photoreceptors encoded by cyanobacterial genomes suggests that these organisms are capable of extremely complex light color sensing and responsiveness, yet little is known about their functions and interactions. Our work uncovers previously undescribed cooperation between two photoreceptors with very different light color-sensing capabilities that coregulate an important photosynthetic light-harvesting protein in response to teal, green, yellow, and red light. Other cyanobacteriochromes that have been shown to interact functionally sense wavelengths of light that are close to each other, which makes it difficult to clearly identify their physiological roles in the cell. Our finding of two photoreceptors with broad light color-sensing capabilities and clearly defined physiological roles provides new insights into complex light color sensing and its regulation.

Figures

FIG 1
FIG 1
Phenotype of a ΔdpxA mutant. (A) Whole-cell absorbance scans of wild-type (WT) and ΔdpxA cells after growth in natural-spectrum white light. Phycoerythrin (PE) and phycocyanin (PC) peaks are labeled. Spectra were normalized to the chlorophyll absorption peaks at both 440 nm and 680 nm, and each scan is an average from six independent experiments. Inset: photograph of wild-type and ΔdpxA cells after growth in natural-spectrum white light. (B) Western blot analysis using the soluble fraction of cell lysates of wild-type and ΔdpxA cells after growth in natural-spectrum white light. Mean values (below) and representative blots (above) are shown for PE (left) and PC (right). For each replicate, the same cell lysate was used for the antiphycoerythrin and antiphycocyanin assay blots. Values provided are normalized by the protein content value, quantified from the stained protein gel, from three independent protein extractions and Western blot replicates. ΔdpxA mutant values were set to 100%. Standard errors of the means are shown.
FIG 2
FIG 2
Light absorption and kinase activity of DpxA in response to yellow and blue light. (A) Difference spectrum of purified DpxA between protein exposed to yellow (λmax, 579 nm) minus blue light (λmax, 466 nm). Insets: photographs of purified protein exposed to yellow (top) and blue (bottom) light. (B) Autophosphorylation of purified DpxA preirradiated to the DpxAy (yellow line) or DpxAt (blue line) forms. The DpxAt 32P incorporation value at 20 min was set to 1.0. Each point is the average from three independent experiments, and standard errors of the means are shown. Inset: representative image of one experiment. Images shown are from the same gel.
FIG 3
FIG 3
Effect of DpxA on phycoerythrin levels across the visible spectrum. Whole-cell absorbance scans of wild-type and ΔdpxA cells grown in blue (λmax, 466 nm) (A), green (λmax, 520 nm) (B), yellow (λmax, 579 nm) (C), or red (λmax, 645 nm) (D) light at 12 µmol photons m−2 s−1. Cell cultures were scanned in late logarithmic growth phase, and each scan is an average from six independent experiments. Spectra were normalized to the chlorophyll absorption peaks at both 440 nm and 680 nm. PC, phycocyanin.
FIG 4
FIG 4
DpxA and RcaE photostationary states after light treatments across the visible spectrum. Absorbance scans of purified full-length DpxA (dashed lines) and the RcaE GAF domain (solid lines) after treatment with light of the wavelength indicated. The colored vertical lines indicate the peak wavelengths of light to which the proteins were exposed. Insets: photographs of purified DpxA (left) and RcaE (right) in the light color specified.
FIG 5
FIG 5
Absorbance spectra of DpxAt (teal line), DpxAy (yellow line), RcaEg (green line), and RcaEr (red line). Each form is indicated by a colored oval above its peak absorption wavelength, which is provided below the oval. The regions of the spectrum maximally absorbed by DpxAy and RcaEr are the wavelengths where phycoerythrin is repressed by DpxA and RcaE, respectively.

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