Control of a four-color sensing photoreceptor by a two-color sensing photoreceptor reveals complex light regulation in cyanobacteria

Abstract

Photoreceptors are biologically important for sensing changes in the color and intensity of ambient light and, for photosynthetic organisms, processing this light information to optimize food production through photosynthesis. Cyanobacteria are an evolutionarily and ecologically important prokaryotic group of oxygenic photosynthesizers that contain cyanobacteriochrome (CBCR) photoreceptors, whose family members sense nearly the entire visible spectrum of light colors. Some cyanobacteria contain 12 to 15 different CBCRs, and many family members contain multiple lightsensing domains. However, the complex interactions that must be occurring within and between these photoreceptors remain unexplored. Here we describe the regulation and photobiology of a unique CBCR called IflA (influenced by far-red light), demonstrating that a second CBCR called RcaE strongly regulates IflA abundance and that IflA uses two distinct photosensory domains to respond to four different light colors: blue, green, red, and farred. The absorption of red or far-red light by one domain affects the conformation of the other domain, and the rate of relaxation of one of these domains is influenced by the conformation of the other. Deletion of iflA results in delayed growth at low cell density, suggesting that IflA accelerates growth under this condition, apparently by sensing the ratio of red to far-red light in the environment. The types of complex photobiological interactions described here, both between unrelated CBCR family members and within photosensory domains of a single CBCR, may be advantageous for species using these photoreceptors in aquatic environments, where light color ratios are influenced by many biotic and abiotic factors. chromatic acclimation | chromatic adaptation | phytochrome | signal transduction | tetrapyrrole

Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation

“…5, orange line) nor ΔsesA (Fig. 4B, red line) aggregated, it appears that in the absence of SesC, only SesA is capable of triggering cell aggregation and that SesB can only negatively regulate cell aggregation to counteract the effects of SesA, although we cannot rule out that the expression of sesC might be impaired in ΔsesA, as described for RcaE/IflA (30). Cell aggregation of ΔsesB/ΔsesC is increased under blue light and decreased under teal-green light (Fig.…”

Genomic Survey and Biochemical Analysis of Recombinant Candidate Cyanobacteriochromes Reveals Enrichment for Near UV/Violet Sensors in the Halotolerant and Alkaliphilic Cyanobacterium Microcoleus IPPAS B353

“…This photocycle is shared with those of NpR5313g2 (25), FdIflA (50), and a recently discovered family of DXCF-derived CBCRs in which the conserved Asp residue is replaced with a nonionizable residue (53). Red/green CBCR-specific residues equivalent to Arg-301 (position VII) and Tyr-302 (position VIII) in AnPixJ2 (47) are both conserved in the red fluorescent single Cys CBCRs Mbr3854g2/g3 and NpF2164g5 (9), and the replacement of VIII Tyr with Pro in Slr1393g3 did not alter the red/green photoactivity of this CBCR (54), so their role in red/green photochromism is unclear.…”

“…In this regard, it is possible that PCB binding to the non-photoactive GAF2 and GAF3 domains could modulate signaling output by supporting progressive dimerization of tandem GAFs as proposed for TePixJ and NpF2164 (62). Light absorption by one GAF domain might also affect chromophorylation or photoconversion of another domain as suggested for the four-color sensor FdIflA from F. diplosiphon (50). Currently, it is not clear whether cooperative action as in NpF2164 or cross-activation as in FdIflA among multi-GAF domains are occurring in Mbr3854.…”

Phytochromes: An Atomic Perspective on Photoactivation and Signaling

“…For example, by autocatalytically isomerizing the p-conjugation system of the bound PCB to generate phycoviolobilin combined with a second, light-labile thioether linkage to the C10 carbon, CBCRs like Thermosynechococcus elongatus PixJ interconvert between blue and green-light-absorbing end states (Ishizuka et al, 2011;Rockwell et al, 2012b;Burgie et al, 2013) (Figures 2B and 2C). Some CBCRs harbor multiple GAF domains linked in tandem; each domain has the potential to bind their own bilin with different spectral end states, thus enabling integration of multiple light signals simultaneously (Nostoc punctiforme F2854 and Fd-Ifla;Chen et al, 2012;Rockwell et al, 2012a;Bussell and Kehoe, 2013; Figure 1). …”