Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light‐responsive promoters

Abstract

SummaryComplementary chromatic adaptation (CCA) provides cyanobacteria with the ability to shift between red and blue-green phenotypes that are optimized for absorption of different wavelengths of light. Controlled by the ratio of green to red light, this process results from differential expression of two groups of operons, many of which encode proteins involved in photosynthetic light harvesting antennae biogenesis. In the freshwater species Fremyella diplosiphon, the inverse regulation of these two classes is complex and occurs through different mechanisms. It also involves a two-component pathway that includes a phytochrome-class photoreceptor and the response regulator RcaC. Here we uncover the mechanism through which this system controls CCA by demonstrating that RcaC binds to the L Box within promoters of both classes of light-regulated operons. We provide functional evidence that complementary regulation of these operons occurs by RcaC's simultaneous activation and repression of transcription in red light. We identify rcaC and L Boxes in the genome of a marine cyanobacterium capable of CCA, suggesting widespread use of this control system. These results provide important insights into the longstanding enigma of CCA regulation and complete the first description of an entire two-component system controlled by a phytochrome-class photoreceptor.

Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression

“…4A). The enzyme activity in WT cells grown in green light was 10 times higher than in cells grown in red light and was significantly higher in a rcaE null mutant than in WT during growth in red light due to the loss of repression by the Rca system (15), results that mirror previous cpeC transcript-level measurements (13,18). The deletion of infCa in a WT background led to a 2.5-fold increase in β-glucuronidase activity relative to WT during growth in red light (Fig.…”

“…The regulator for complementary chromatic adaptation (Rca) pathway is a complex two-component system consisting of the photoreceptor/ sensor RcaE (9, 10) and two response regulators, RcaF and RcaC (11,12). The activation of this pathway in red light leads to increased expression of phycocyanin-encoding genes and partial repression of the cpeCDESTR operon (hereafter cpeC) (13)(14)(15), which encodes the phycoerythrin linkers, lyases, and a regulator of phycoerythrin expression (13,16). The second Type III chromatic acclimation regulatory system is the control of green light induction (Cgi) pathway, which is responsible for the remainder of cpeC repression during red light growth (13,(17)(18)(19)(20).…”

Shedding new light on the regulation of complementary chromatic adaptation

“…Notably, in silico analysis of the genome of Synechococcus sp. PCC 7335, a marine cyanobacterium that exhibits CCA, resulted in the identification of L boxes upstream of RL-induced genes and in inverse orientation upstream of a gene not expressed during RL, which suggests a common CCA regulatory mechanism among diverse cyanobacteria [5]. Even more recently it was reported that OmpRclass RR RcaC acts as a DNA-binding transcription factor that regulates expression of cpcB2, pcyA and cpeC in response to RL [5].…”

“…PCC 7335, a marine cyanobacterium that exhibits CCA, resulted in the identification of L boxes upstream of RL-induced genes and in inverse orientation upstream of a gene not expressed during RL, which suggests a common CCA regulatory mechanism among diverse cyanobacteria [5]. Even more recently it was reported that OmpRclass RR RcaC acts as a DNA-binding transcription factor that regulates expression of cpcB2, pcyA and cpeC in response to RL [5]. A truncated version of RcaC containing the N-terminal receiver domain and the DNA-binding domain was shown to bind L-boxes in cpcB2, pcyA and cpeC promoters [5].…”

“…Most recently reviewed in 2006 by Kehoe and Gutu [3], a number of seminal insights have been made regarding the regulation of CCA during the past few years. These advances include progress in our understanding of the mechanisms utilized by transcriptional regulators that control CCA responses [4,5], and the identification of novel roles for sensory photoreceptors involved in the regulation of distinct aspects of the CCA process [6], in addition to other related novel developments [7][8][9][10][11][12]. The photoregulation of pigmentation -i.e.…”