Blue/green light-responsive cyanobacteriochromes are cell shade sensors in red light-replete niches

Photoautotrophic cyanobacteria have developed sophisticated light response systems to capture and utilize the energy and information of incident light [1]. Cyanobacteria-specific photoreceptors cyanobacteriochromes (CBCRs) are distantly related to more widespread phytochromes. CBCRs show the most diverse spectral properties among the naturally occurring photoreceptors, typified by a unique and prevailing blue/green light-absorbing variant [2-6]. However, where the CBCR-mediated colorful signaling systems function in nature has been elusive. We previously reported that the three CBCRs SesA/B/C synthesize/degrade a bacterial second messenger cyclic diguanylate (c-di-GMP) in response to blue/green light [6-8]. The cooperative action of SesA/B/C enables blue light-ON and green light-OFF regulation of the c-di-GMP-dependent cell aggregation of the thermophilic cyanobacterium Thermosynechococcus vulcanus [8, 9]. Here, we report that SesA/B/C can serve as a physiological sensor 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.