Research Article: Temperature–amplitude coupling for stable biological rhythms at different temperatures

Date Published: June 8, 2017

Publisher: Public Library of Science

Author(s): Gen Kurosawa, Atsuko Fujioka, Satoshi Koinuma, Atsushi Mochizuki, Yasufumi Shigeyoshi, Attila Csikász-Nagy

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.

Partial Text: 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]. At the system level, 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]. In contrast, the circadian rhythm period is robust to temperature [1,3]. Notably, this property, so-called temperature compensation, is observed in both species without and with strong thermal homeostasis (poikilotherms and homeotherms). The definition of temperature compensation is that the oscillator period is constant at different but constant temperatures (0.85http://doi.org/10.1371/journal.pcbi.1005501