Multispectral regulation of chromatic acclimation by integration of the Rca system and the conserved dpx operon

Type III Chromatic Acclimation (CA3) in Fremyella diplosiphon has traditionally served as a model for cyanobacterial acclimation to red and green light. CA3 is controlled by the red-green responsive Rca phosphorelay system, including the cyanobacteriochrome RcaE. However, regulation of pigmentation persists in the absence of RcaE, which is attributed to the Cgi system. Nothing is known about how the Cgi regulatory system senses light color to differentially regulate pigment expression. DpxA is a teal/yellow-sensing cyanobacteriochrome that regulates cell pigmentation through an unknown regulatory pathway. Here, we show that DpxA and RcaE collectively control the vast majority of chromatic acclimation across the visible spectrum, implicating DpxA as the likely sensor for the Cgi system. The genetic context of DpxA is identified as part of a 3-gene operon alongside a response regulator (DpxB) and a hybrid histidine kinase (DpxC). The impact of the Dpx proteins is modulated by the RcaE-mediated genetic background, suggesting an integrated sensory response by the Dpx and Rca pathways. Beyond mechanistic insights, phylogenomic analysis reveals that the dpx operon is conserved across distantly related cyanobacterial species, including those incapable of CA3. These findings suggest the dpx operon was distributed via horizontal gene transfer, likely providing cell adaptation to diverse environmental niches through regulation of processes beyond color acclimation.IMPORTANCEThe ability to accurately sense and integrate multiple environmental cues is fundamental to bacterial behavior and survival. Type III Chromatic Acclimation (CA3) in Fremyella diplosiphon is an ideal model for signal integration because of its well-defined light cues, numerous predicted photoreceptors, and reliable physiological output. This study reveals that CA3 is governed by an interconnected, multispectral sensory network. We demonstrate that the conserved dpxABC operon-and its sensor DpxA-integrates with the Rca pathway into a coordinated acclimation response. Furthermore, the dpx operon is conserved across phylogenetically distant cyanobacteria, suggesting physiological benefits beyond CA3. These findings underscore the complexity of prokaryotic light signal integration, wherein multiple cues are synthesized into cohesive physiological responses.