Temperature–amplitude coupling for stable biological rhythms at different temperatures

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.

A Robust and Self-Sustained Peripheral Circadian Oscillator Reveals Differences in Temperature Compensation Properties with Central Brain Clocks

“…Mean expression levels of all four reporters changed with temperature in a very similar manner, with low expression levels at the extremes (18°C and 29°C) and higher expression levels at 21°C and 25°C ( Figure S4 , Table S1 ), precluding any meaningful correlation between protein levels and transcription rates as was the case for the halteres. It has previously been reported that luciferase activity is temperature dependent, either increasing or decreasing with temperature (e.g., Kurosawa et al., 2017 ; McElroy and Seliger, 1961 ). Although we cannot rule out direct effects of temperature on luciferase activity, we do not observe consistent changes of luciferase activity with temperature.…”

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

“…It has previously been reported that luciferase activity is temperature-dependent, either increasing or decreasing with temperature (e.g. (Kurosawa et al, 2017;McElroy and Seliger, 1961)). Although we cannot rule out direct effects of temperature on luciferase activity, we do not observe consistent changes of luciferase activity with temperature.…”

Co-existing feedback loops generate tissue-specific circadian rhythms

“…Even this condensed network contains 17 regulations constituting multiple negative and positive feedback loops ( 13 ). To generate self-sustained oscillations, negative feedback loops are essential ( 14 , 15 ). Originally, the self-inhibitions of the period and cryptochrome genes have been considered as the primary negative feedback loops ( 16 ).…”