Universality of Thermodynamic Constants Governing Biological Growth Rates

Corkrey, Ross; Olley, June; Ratkowsky, David A.; McMeekin, TA; Ross, Tom

doi:10.1371/journal.pone.0032003

Cited by 69 publications

(91 citation statements)

References 39 publications

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“…The magnitude of performance at any point along the curve can vary from organism to organism. The generality of unimodal responses to temperature was recently corroborated by two broad surveys: one of a variety of traits at different levels of biological organization across a wide range of taxa (Dell et al, 2011) and the other of thermal dependency of growth rates across the three domains of life (Corkrey et al, 2012). Later, we raise concerns regarding the applicability of performance curves in variable environments, but given their widespread use in the literature they warrant a detailed review.…”

Section: Introductionmentioning

confidence: 75%

Thermal variation, thermal extremes and the physiological performance of individuals

Dowd

King

Denny

2015

Journal of Experimental Biology

204

209

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In this review we consider how small-scale temporal and spatial variation in body temperature, and biochemical/physiological variation among individuals, affect the prediction of organisms' performance in nature. For 'normal' body temperatures -benign temperatures near the species' mean -thermal biology traditionally uses performance curves to describe how physiological capabilities vary with temperature. However, these curves, which are typically measured under static laboratory conditions, can yield incomplete or inaccurate predictions of how organisms respond to natural patterns of temperature variation. For example, scale transition theory predicts that, in a variable environment, peak average performance is lower and occurs at a lower mean temperature than the peak of statically measured performance. We also demonstrate that temporal variation in performance is minimized near this new 'optimal' temperature. These factors add complexity to predictions of the consequences of climate change. We then move beyond the performance curve approach to consider the effects of rare, extreme temperatures. A statistical procedure (the environmental bootstrap) allows for longterm simulations that capture the temporal pattern of extremes (a Poisson interval distribution), which is characterized by clusters of events interspersed with long intervals of benign conditions. The bootstrap can be combined with biophysical models to incorporate temporal, spatial and physiological variation into evolutionary models of thermal tolerance. We conclude with several challenges that must be overcome to more fully develop our understanding of thermal performance in the context of a changing climate by explicitly considering different forms of small-scale variation. These challenges highlight the need to empirically and rigorously test existing theories.

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Section: Introductionmentioning

confidence: 75%

Thermal variation, thermal extremes and the physiological performance of individuals

Dowd

King

Denny

2015

Journal of Experimental Biology

204

209

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“…Data that conform to the Arrhenius equation are often explained by assuming that the shape of the TPC for aerobic metabolism at the cellular level is governed by the thermal dependence of a single underlying process, for example, a rate-limiting step in the biochemical network (Corkrey et al, 2012). Similarly, cases in which significant discontinuities (ABTs) below the T opt are detected in the TPCs are often attributed to the effects of temperature-induced changes in membrane structure that influence the function of the mitochondrial electron transport chain and thus these explanations also tend to focus on single key processes and their interaction with the cellular environment.…”

Section: Effects Of Temperature At the Level Of Single Proteinsmentioning

confidence: 99%

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

Schulte¹

2015

Journal of Experimental Biology

555

451

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Because of its profound effects on the rates of biological processes such as aerobic metabolism, environmental temperature plays an important role in shaping the distribution and abundance of species. As temperature increases, the rate of metabolism increases and then rapidly declines at higher temperatures -a response that can be described using a thermal performance curve (TPC). Although the shape of the TPC for aerobic metabolism is often attributed to the competing effects of thermodynamics, which can be described using the Arrhenius equation, and the effects of temperature on protein stability, this account represents an over-simplification of the factors acting even at the level of single proteins. In addition, it cannot adequately account for the effects of temperature on complex multistep processes, such as aerobic metabolism, that rely on mechanisms acting across multiple levels of biological organization. The purpose of this review is to explore our current understanding of the factors that shape the TPC for aerobic metabolism in response to acute changes in temperature, and to highlight areas where this understanding is weak or insufficient. Developing a more strongly grounded mechanistic model to account for the shape of the TPC for aerobic metabolism is crucial because these TPCs are the foundation of several recent attempts to predict the responses of species to climate change, including the metabolic theory of ecology and the hypothesis of oxygen and capacity-limited thermal tolerance.

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“…The decline in the rate of activity in biological systems above T opt has been attributed to enzyme denaturation at higher temperatures coupled with complex regulatory temperature responses in the cell. Corkrey et al (2012) modelled these effects on the basis of a single 'master enzyme' where the complex negative effects above T opt are rolled into an enzyme denaturation term. However, enzyme denaturation is not a coherent explanation in soil systems as enzyme denaturation generally occurs at higher temperatures than those that are commonly observed in soils.…”

Section: Introductionmentioning

confidence: 99%

Thermodynamic theory explains the temperature optima of soil microbial processes and high Q₁₀ values at low temperatures

Schipper

Hobbs

Rutledge

et al. 2014

Global Change Biology

176

158

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Our current understanding of the temperature response of biological processes in soil is based on the Arrhenius equation. This predicts an exponential increase in rate as temperature rises, whereas in the laboratory and in the field, there is always a clearly identifiable temperature optimum for all microbial processes. In the laboratory, this has been explained by denaturation of enzymes at higher temperatures, and in the field, the availability of substrates and water is often cited as critical factors. Recently, we have shown that temperature optima for enzymes and microbial growth occur in the absence of denaturation and that this is a consequence of the unusual heat capacity changes associated with enzymes. We have called this macromolecular rate theory -MMRT (Hobbs et al., 2013, ACS Chem. Biol. 8:2388). Here, we apply MMRT to a wide range of literature data on the response of soil microbial processes to temperature with a focus on respiration but also including different soil enzyme activities, nitrogen and methane cycling. Our theory agrees closely with a wide range of experimental data and predicts temperature optima for these microbial processes. MMRT also predicted high relative temperature sensitivity (as assessed by Q 10 calculations) at low temperatures and that Q 10 declined as temperature increases in agreement with data synthesis from the literature. Declining Q 10 and temperature optima in soils are coherently explained by MMRT which is based on thermodynamics and heat capacity changes for enzyme-catalysed rates. MMRT also provides a new perspective, and makes new predictions, regarding the absolute temperature sensitivity of ecosystems -a fundamental component of models for climate change.

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Universality of Thermodynamic Constants Governing Biological Growth Rates

Cited by 69 publications

References 39 publications

Thermal variation, thermal extremes and the physiological performance of individuals

Thermal variation, thermal extremes and the physiological performance of individuals

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

Thermodynamic theory explains the temperature optima of soil microbial processes and high Q₁₀ values at low temperatures

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Universality of Thermodynamic Constants Governing Biological Growth Rates

Cited by 69 publications

References 39 publications

Thermal variation, thermal extremes and the physiological performance of individuals

Thermal variation, thermal extremes and the physiological performance of individuals

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

Thermodynamic theory explains the temperature optima of soil microbial processes and high Q10 values at low temperatures

Contact Info

Product

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Thermodynamic theory explains the temperature optima of soil microbial processes and high Q₁₀ values at low temperatures