Temperature compensation through systems biology

Abstract

Temperature is an environmental factor, which influences most of the chemical processes occurring in living and nonliving systems. Van't Hoff's rule states that reaction rates increase by a factor (the Q 10) of two or more when the temperature is increased by 10 °C [1]. Despite this strong influence of temperature on individual reactions, many organisms are able to keep some of their metabolic fluxes at an approximately constant level over an extended temperature range. Examples are the oxygen consumption rates of ectoterms living in costal zones [2] and of fish [3], the period lengths of all circadian [4] and some ultradian [5,6] rhythms, photosynthesis in cold-adapted plants [7,8], homeostasis during fever [9], or the regulation of heat shock proteins [10]. In 1957, Hastings and Sweeney suggested that in biological clocks such temperature compensation may occur as the result of opposing reactions within the metabolic network [11]. Later kinetic analysis of the problem [12] reached essentially the same conclusion, and predictions of the theory have been tested by experiments using Neurospora's circadian clock [13] and chemical oscillators [14,15]. In this study, we use metabolic and hierarchical control analysis [16-22] to show how certain steady-state fluxes in static reaction networks can be temperature compensated according to a similar principle, and how dynamic networks have an additional repertoire of mechanisms. This study is mostly theoretical, but we use the temperature adaptation of yeast cells and of photosynthesis as illustrations. These and other Temperature has a strong influence on most individual biochemical reactions. Despite this, many organisms have the remarkable ability to keep certain physiological fluxes approximately constant over an extended temperature range. In this study, we show how temperature compensation can be considered as a pathway phenomenon rather than the result of a single-enzyme property. Using metabolic control analysis, it is possible to identify reaction networks that exhibit temperature compensation. Because most activation enthalpies are positive, temperature compensation of a flux can occur when certain control coefficients are negative. This can be achieved in networks with branching reactions or if the first irreversible reaction is regulated by a feedback loop. Hierarchical control analysis shows that networks that are dynamic through regulated gene expression or signal trans-duction may offer additional possibilities to bring the apparent activation enthalpies close to zero and lead to temperature compensation. A calori-metric experiment with yeast provides evidence that such a dynamic temperature adaptation can actually occur.

Protein sequestration versus Hill‐type repression in circadian clock models

“…5), the major difference between HT and PS models has not been reported or investigated, to our knowledge. Future work can also investigate whether PS models follow the entrainment properties [37,45,47,142,[156][157][158] or temperature compensation mechanisms [38,40,42,[159][160][161][162][163][164][165][166] identified with HT models. Furthermore, stochastic simulations of HT models commonly indicate that circadian clocks can maintain rhythms even with low numbers of molecules [167][168][169][170].…”

Adaptive dynamics with a single two-state protein

“…In metabolic networks, a mechanism similar to BioNetUnit could provide adaptation in a system where an enzyme converts a substrate that is steadily produced by an upstream reaction to another one which is used up in a subsequent reaction; in other words, the same structure as in figure 1a with P and P a corresponding to substrates and with the hydrolysis rate set to zero. It is possible that such enzymatic reactions are involved in temperature compensation (Ruoff et al 2007).…”

“…Interestingly, the assumption regarding the actions of CheR and CheB generates a system that balances a zero-order reaction against a first-order reaction (Alon 2006), as seen in the BioNetUnit. Both incoherent feed-forward (Yi et al 2000;Tyson et al 2003;Behar et al 2007) and balancing a zero-order against a first-order reaction (Alon 2006;Ruoff et al 2007) are suggested to involve adaptive dynamics. Incorporating both these proposed outlines in a primitive way, BioNetUnit stands out possibly as the simplest adaptive biochemical system.…”

Metabolism in the age of ‘omes’

“…The remarkable finding in this study is that hierarchical regulation and direct temperature effects both make modest contributions, whereas metabolic regulation is mainly responsible for temperature-induced changes in J in yeast. Application of the 'systems approach' to temperature effects on metabolism by this group has led to a theoretical framework for thermal compensation (Ruoff et al, 2007), a subject of decades-long interest to comparative physiologists (Hochachka and Somero, 2002).…”