Metabolic control of transcriptional-translational control loops (TTCL) by circadian oscillations in the redox- and phosphorylation state of cells

Abstract

Evolution from prokaryotic to eukaryotic organisms was paralleled by a corresponding evolution in energy metabolism. From primeval fermentation, energy conservation progressed to anaerobic photosynthesis and then to carbon dioxide fixation with acceptance of electrons by water and the evolution of oxygen. In a progressively oxygenic biosphere, respiration developed with oxygen as a terminal electron acceptor. Evolving life was paralleled by a corresponding evolution of tropospheric O2/CO2 composition and the feedback of oxygen on life processes via reactive oxygen and reactive nitrogen species, which as signalling molecules became crucial for the control of development of pro- and eukaryotic living systems. Adaptation to the seasonal variation in daylength resulted in photoperiodic control of development with a circadian rhythm in energy conservation and transformation to optimise energy harvesting by photosynthesis. Photosynthesis on the other hand acts as a light-dependent metabolic regulator via redox signals in addition to specific photoreceptors like phytochromes and cryptochromes. Finally, redox control integrates rhythmic gene expression in chloroplasts, mitochondria and the nucleus. The circadian rhythmic cell (cyanobacterial and eukaryotic) is a hydro-electro-chemical oscillator synchronised by the daily light – dark cycle with temporal compartmentation of metabolism and a network of metabolic sequences to compensate for oxidative stress in adapting to the light environment e.g. by separating N-fixation from oxygen production. In Chenopodium rubrum L. a circadian rhythm in overall energy transduction has been observed. This rhythm results from an oscillatory network between glycolysis and oxidative phosphorylation coupled to photophosphorylation. This network produces a circadian rhythm in adenylate energy charge and redox state (NADP/NADPH2). The nucleotide ratios themselves could, as rate effectors in compartmental feedback, fulfil the requirements for precise temperature-compensated time keeping. The integration of metabolic activity of Chenopodium plants on a hydraulic-electrochemical level is represented by a diurnal rhythm in compound surface membrane resting potential. Using molecular genetic techniques, research of the last 30 years has come to the conclusion that the core oscillator of circadian systems should reside in transcriptional and translational control loops (TTCL) involved in feedback regulation of clock genes. Considering the evolution of metabolic networks in response to environmental constraints, we proposed (Wagner & Cumming 1970; Wagner et al. 1998) that circadian rhythms in redox state and phosphorylation potential, as an output from the network of energy transduction (Singh 1998), should be gating the TTCL for the circadian rhythmic production of proteins needed in the metabolic networks. A similar concept has been advanced for metabolic control of human circadian rhythms, assuming that the redox state of cells should be the driving effector (Rutter et al. 2002) of the physiological clock.