Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock

Abstract

Circadian rhythms are endogenous cellular programs that time metabolic and behavioral events to occur at optimal times in the daily cycle. Light and dark cycles synchronize the endogenous clock with the external environment through a process called entrainment. Previously, we identified the bacteriophytochrome-like circadian input kinase CikA as a key factor for entraining the clock in the cyanobacterium Synechococcus elongatus PCC 7942. Here, we present evidence that CikA senses not light but rather the redox state of the plastoquinone pool, which, in photosynthetic organisms, varies as a function of the light environment. Furthermore, CikA associates with the Kai proteins of the circadian oscillator, and it influences the phosphorylation state of KaiC during resetting of circadian phase by a dark pulse. The abundance of CikA varies inversely with light intensity, and its stability decreases in the presence of the quinone analog 2,5-dibromo-3-methyl-6-isopropylp-benzoquinone (DBMIB). The pseudo-receiver domain of CikA is crucial for sensitivity to DBMIB, and it binds the quinone directly, a demonstration of a previously unrecognized ligand-binding role for the receiver fold. Our results suggest that resetting the clock in S. elongatus is metabolism-dependent and that it is accomplished through the interaction of the circadian oscillator with CikA.biological rhythms ͉ photosynthetic electron transport ͉ pseudo-receiver ͉ redox ͉ Synechococcus elongatus

Biological Rhythms Workshop IA: Molecular Basis of Rhythms Generation

“…Accumulation of CikA occurs during the night (Ivleva et al 2006), and low levels of CikA protein are present at higher light intensities. Levels of CikA protein are locked at the low level that is associated with high light in strains deficient in ldpA (Ivleva et al 2005).…”

“…Both CikA and LdpA have been shown to be part of the Kai protein complex (along with the output protein SasA, discussed below), and at least CikA influences the phosphorylation state of KaiC (Ivleva et al 2005(Ivleva et al , 2006. The assembly and disassembly of this large heteromultimeric protein complex, termed the "periodosome," appear to be a driving force behind the cyanobacterial circadian system as a whole.…”

“…Levels of CikA protein are locked at the low level that is associated with high light in strains deficient in ldpA (Ivleva et al 2005). Degradation of CikA can be stimulated by the direct binding of a quinone analog 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB) to the pseudo-receiver domain of the protein (Ivleva et al 2006). DBMIB affects electron transport in the photosynthetic apparatus to produce an excess of electrons (reduction), which reflects the redox state of the cell.…”

PRR3 Is a Vascular Regulator of TOC1 Stability in theArabidopsisCircadian Clock

“…The regulation of transcription is not the only mechanism that controls clock progression, as modulation of protein stability has emerged as an important aspect of the circadian clockwork (Millar, 2000;Harms et al, 2004;Shu and Hong-Hui, 2004;Liu, 2005;Ivleva et al, 2006;Dardente and Cermakian, 2007;Farre and Kay, 2007;Gallego and Virshup, 2007). ZEITLUPE (ZTL), the founding member of the protein family characterized by a LIGHT, OXYGEN, or VOLTAGE (LOV) domain, an F-box motif, and kelch repeats, mediates the degradation of TOC1 via the formation of a multiprotein Skp/Cullin1/F-box complex that catalyzes the ubiquitylation of proteins destined for proteasomal degradation (Kiyosue and Wada, 2000;Somers et al, 2000Somers et al, , 2004Schultz et al, 2001;Han et al, 2004;Fukamatsu et al, 2005;Kevei et al, 2006).…”

Apo-bacteriophytochromes modulate bacterial photosynthesis in response to low light

“…We believe that this chromophore is bacteriochlorophyll bound by the LH peptides, which absorbs light and transmits it to the reaction center, where it is used to reduce quinones in the membrane. In other systems, the redox status of the quinone pool changes under different light intensities, and light intensity is sensed as a change in the redox state of the quinone pool (35)(36)(37)(38)(39)(40). We hypothesize that light intensity is sensed as a redox signal by R. palustris, and that this redox signal combined with the pool of active BphPs (even in the absence of BV) is sufficient for LH4 synthesis.…”