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.2020 Mar 27;23(3):100936.
doi: 10.1016/j.isci.2020.100936. Epub 2020 Feb 25.

Blue-/Green-Light-Responsive Cyanobacteriochromes Are Cell Shade Sensors in Red-Light Replete Niches

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Blue-/Green-Light-Responsive Cyanobacteriochromes Are Cell Shade Sensors in Red-Light Replete Niches

Gen Enomoto et al. iScience..

Abstract

Cyanobacteriochrome (CBCRs) photoreceptors show various photochemical properties, but their ecophysiological functions remain elusive. Here, we report that the blue/green CBCRs SesA/B/C can serve as physiological sensors of cell density. Because cyanobacterial cells show lower transmittance of blue light than green light, higher cell density gives more green-light-enriched irradiance to cells. The cell-density-dependent suppression of cell aggregation under blue-/green-mixed light and white light conditions support this idea. Such a sensing mechanism may provide information about the cell position in cyanobacterial mats in hot springs, the natural habitat of Thermosynechococcus. This cell-position-dependent SesA/B/C-mediated regulation of cellular sessility (aggregation) might be ecophysiologically essential for the reorganization and growth of phototrophic mats. We also report that the green-light-induced dispersion of cell aggregates requires red-light-driven photosynthesis. Blue/green CBCRs might work as shade detectors in a different niche than red/far-red phytochromes, which may be why CBCRs have evolved in cyanobacteria.

Keywords: Biological Sciences; Microbiology; Sensor.

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

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Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
The Light Ratio of Blue to Green Light Perceived by SesA/B/C CBCRs Can be an Indicator of Self-Shading (A) The cell absorption spectrum ofThermosynechococcusvulcanus (upper) and the difference spectra of the reversible photoconversion of SesA/B/C holoproteins (lower). The lower panel was created using the data reported in Ref. 7. The region of 420 nm–440 nm was highlighted in a blue shade and that of 520 nm–540 nm was highlighted in a green shade. (B) The transmittance ratio of blue light (439 nm) to green light (540 nm) and the image of the liquid culture ofT. vulcanus.
Figure 2
Figure 2
SesA/B/C-Mediated Blue/Green Light Signaling Senses Cell Density to Regulate Cell Aggregation under Both Blue Ligh and Green Light (A) Effects of cell population density on cell aggregation under LED irradiation. The horizontal axis shows the initial cell density, and the vertical axis shows the aggregation index (percentage of aggregated cells) after 48 h of cultivation at low temperatures of 31°C in the presence of red light (634 nm, 30 μE m−2 s−1). The intensity of signaling light is indicated as labels; B10TG2: blue light (448 nm, 10 μE m−2 s−1) + teal-green light (507 nm, 2 μE m−2 s−1). Data are represented as the mean ± SEM. See also Figure S2. (B) Cell aggregation under the four different intensities of the white light fluorescent lamp. Data are represented as the mean ± SEM. See also Figure S1.
Figure 3
Figure 3
Red-Light-Driven Photosynthesis is Necessary to Support the Reversible Formation and Dispersion of Cell Aggregates (A) Reversible formation and dispersion of cell aggregation induced by switching blue light and teal-green light every 24 h in the presence or absence of the background red light irradiation. Data are represented as the mean ± SD. (B) Effects of the photosynthesis inhibitor DCMU on the formation and dispersion of cell aggregates. DCMU (final concentration 10 μM) was added at the indicated time. Data are represented as the mean ± SD.
Figure 4
Figure 4
SesA/B/C Invoke Heterogeneity of C-di-GMP Signaling in a Cyanobacterial Community and Act in Different Layers than Red/Far-Red Light-Responsive Phytochromes (A) A hypothesis of dynamic cell movements inside a microbial mat. Under natural light conditions, the internal cells in a floc will sense a green light-rich environment and turn off c-di-GMP signaling, favoring the motile-planktonic lifestyle. If the internal c-di-GMP-OFF cells retain positive phototactic motility, they may move and reach the upper region, resulting in the reorganization of the heterogeneous c-di-GMP levels in the floc. This would invoke sequential cellular movements in the cyanobacterial community. (B) A hypothesis of niche differentiation of photoreceptors. Blue light rapidly attenuates in the top layer of photosynthetic microbial mats (Jorgensen et al., 1987, Ohkubo and Miyashita, 2017). Blue/green cyanobacteriochromes may be a shade detector in an upper layer of microbial mats, where sufficient red light is still available. On the other hand, phytochromes may be effective in a darker deep area, where red light diminishes, and therefore cyanobacteria cannot out-compete other bacterial species.
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References

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