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      A general theory for temperature dependence in biology

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          Significance

          One of the most fundamental physical constraints on living systems is temperature. Despite its importance, a simple, mechanistic, and general theory that fully predicts the response to temperature across all scales has not yet been derived. Here we develop such a theory based on the fundamental chemical kinetics and statistical physics governing the biochemical reactions that support life. Our mathematical framework includes an explanation for why temperature response curves have a maximum or minimum value and the derivation of a single universal curve onto which data for the temperature dependence of diverse biological quantities covering all levels of organization, collapse. The theory has multiple potential applications including predicting responses to global warming, yields of industrial processes, and epidemic outbreaks.

          Abstract

          At present, there is no simple, first principles–based, and general model for quantitatively describing the full range of observed biological temperature responses. Here we derive a general theory for temperature dependence in biology based on Eyring–Evans–Polanyi’s theory for chemical reaction rates. Assuming only that the conformational entropy of molecules changes with temperature, we derive a theory for the temperature dependence of enzyme reaction rates which takes the form of an exponential function modified by a power law and that describes the characteristic asymmetric curved temperature response. Based on a few additional principles, our model can be used to predict the temperature response above the enzyme level, thus spanning quantum to classical scales. Our theory provides an analytical description for the shape of temperature response curves and demonstrates its generality by showing the convergence of all temperature dependence responses onto universal relationships—a universal data collapse—under appropriate normalization and by identifying a general optimal temperature, around 25 C, characterizing all temperature response curves. The model provides a good fit to empirical data for a wide variety of biological rates, times, and steady-state quantities, from molecular to ecological scales and across multiple taxonomic groups (from viruses to mammals). This theory provides a simple framework to understand and predict the impact of temperature on biological quantities based on the first principles of thermodynamics, bridging quantum to classical scales.

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          Most cited references72

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          TOWARD A METABOLIC THEORY OF ECOLOGY

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            A method for the solution of certain non-linear problems in least squares

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              Effects of size and temperature on metabolic rate.

              We derive a general model, based on principles of biochemical kinetics and allometry, that characterizes the effects of temperature and body mass on metabolic rate. The model fits metabolic rates of microbes, ectotherms, endotherms (including those in hibernation), and plants in temperatures ranging from 0 degrees to 40 degrees C. Mass- and temperature-compensated resting metabolic rates of all organisms are similar: The lowest (for unicellular organisms and plants) is separated from the highest (for endothermic vertebrates) by a factor of about 20. Temperature and body size are primary determinants of biological time and ecological roles.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                18 July 2022
                26 July 2022
                18 January 2023
                : 119
                : 30
                : e2119872119
                Affiliations
                [1] aDepartamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile , CP 8331150 Santiago, Chile;
                [2] bThe Santa Fe Institute , Santa Fe, NM 87501;
                [3] cDepartamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile , CP 8331150 Santiago, Chile;
                [4] dCenter for Climate and Resilience Research, FONDAP (Fondo de Financiamiento de Centros de Investigación en Áreas Prioritarias), University of Chile , CP 8370449 Santiago, Chile;
                [5] eCenter for Genome Regulation, FONDAP, Faculty of Science, University of Chile , CP 7800003 Santiago, Chile;
                [6] fInstituto de Ecología y Biodiversidad , CP 7800003 Santiago, Chile;
                [7] gCentro de Cambio Global Universidad Católica, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile , CP 8331150 Santiago, Chile;
                [8] hInstituto de Sistemas Complejos de Valparaíso , CP 2340000 Valparaíso, Chile;
                [9] iCentro de Modelamiento Matemático, Universidad de Chile, International Research Laboratory 2807, CNRS , CP 8370456 Santiago, Chile
                Author notes
                2To whom correspondence may be addressed. Email: pmarquet@ 123456bio.puc.cl or jiarroyo@ 123456uc.cl .

                Contributed by Pablo Marquet; received October 31, 2021; accepted April 7, 2022; reviewed by Raymond Huey and Andrea Rinaldo

                Author contributions: J.I.A. and P.A.M. designed research; J.I.A., C.P.K., G.B.W., and P.A.M. performed research; J.I.A., C.P.K., G.B.W., and P.A.M. contributed new reagents/analytic tools; J.I.A. analyzed data; and J.I.A., B.D., C.P.K., G.B.W., and P.A.M. wrote the paper.

                1Present address: Centro de Modelamiento Matemático, Universidad de Chile, International Research Laboratory 2807, CNRS, CP 8370456 Santiago, Chile.

                Author information
                https://orcid.org/0000-0002-9371-8083
                Article
                202119872
                10.1073/pnas.2119872119
                9335213
                35858416
                906df029-cd53-4463-bab7-be3a8b3f180c
                Copyright © 2022 the Author(s). Published by PNAS.

                This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 07 April 2022
                Page count
                Pages: 7
                Funding
                Funded by: Agencia Nacional de Investigación y Desarrollo (ANID) 501100020884
                Award ID: 21130515
                Award Recipient : Ignacio Arroyo
                Funded by: ANID-FONDECYT
                Award ID: 1200925
                Award Recipient : Ignacio Arroyo Award Recipient : Pablo A Marquet
                Funded by: AFB
                Award ID: ACE210006
                Award Recipient : Ignacio Arroyo Award Recipient : Pablo A Marquet
                Funded by: NSF
                Award ID: 1838420
                Award Recipient : Ignacio Arroyo Award Recipient : Pablo A Marquet
                Funded by: NSF
                Award ID: 1840301
                Award Recipient : Ignacio Arroyo Award Recipient : Pablo A Marquet
                Funded by: BASAL funds for centers of excellence from ANID-Chile
                Award ID: FB210005
                Award Recipient : Ignacio Arroyo Award Recipient : Pablo A Marquet
                Categories
                414
                Biological Sciences
                Ecology

                temperature kinetics,scaling,metabolic theory
                temperature kinetics, scaling, metabolic theory

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