Abstract
Most biological processes accelerate with temperature, for example cell division. In contrast, the circadian rhythm period is robust to temperature fluctuation, termed temperature compensation. Temperature compensation is peculiar because a system-level property (i.e., the circadian period) is stable under varying temperature while individual components of the system (i.e., biochemical reactions) are usually temperature-sensitive. To understand the mechanism for period stability, we measured the time series of circadian clock transcripts in cultured C6 glioma cells. The amplitudes of Cry1 and Dbp circadian expression increased significantly with temperature. In contrast, other clock transcripts demonstrated no significant change in amplitude. To understand these experimental results, we analyzed mathematical models with different network topologies. It was found that the geometric mean amplitude of gene expression must increase to maintain a stable period with increasing temperatures and reaction speeds for all models studied. To investigate the generality of this temperature–amplitude coupling mechanism for period stability, we revisited data on the yeast metabolic cycle (YMC) period, which is also stable under temperature variation. We confirmed that the YMC amplitude increased at higher temperatures, suggesting temperature-amplitude coupling as a common mechanism shared by circadian and 4 h-metabolic rhythms.
Highlights
Many physiological processes are sensitive to temperature
Experiments conducted over the last few decades in insects, mammals, and plants have demonstrated that biological rhythms are governed by cyclical changes in gene expression
The topologies of the regulatory network structures for these rhythms differ between species, suggesting that the mechanisms for period stability with temperature are not conserved
Summary
Many physiological processes are sensitive to temperature. At the biochemical level, the speed of the reactions tends to increase two- to three-fold with a 10 ̊C temperature rise [1]. Cell growth accelerates with temperature, and the cell cycle period of NIH3T3 cells decreases to one-third as the temperature rises by 10 ̊C [2]. The circadian rhythm period is robust to temperature [1,3]. This property, so-called temperature compensation, is observed in both species without and with strong thermal homeostasis (poikilotherms and homeotherms). The circadian period of mammalian NIH3T3 cells remains roughly unchanged over a wide range of temperatures [2]. The period of the yeast metabolic cycle (YMC), approximately 4 h under certain experimental conditions, is robust to temperature [5]
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