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Download Hi-Res ImageDownload to MS-PowerPointCite This:ACS Chem. Biol. 2013, 8, 11, 2388-2393
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Change in Heat Capacity for Enzyme Catalysis Determines Temperature Dependence of Enzyme Catalyzed Rates

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† Department of Biological Sciences, Faculty of Science and Engineering, University of Waikato, Hamilton 3240, New Zealand
‡ Biomolecular Interaction Centre and Department of Chemistry, University of Canterbury, Christchurch 8041, New Zealand
§ Department of Earth and Ocean Sciences, Faculty of Science and Engineering, University of Waikato, Hamilton 3240, New Zealand
*(V.L.A.) E-mail: [email protected]. Tel: +64 7 838 4679.
Cite this: ACS Chem. Biol. 2013, 8, 11, 2388–2393
Publication Date (Web):September 9, 2013
https://doi.org/10.1021/cb4005029
Copyright © 2013 American Chemical Society
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Abstract

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The increase in enzymatic rates with temperature up to an optimum temperature (Topt) is widely attributed to classical Arrhenius behavior, with the decrease in enzymatic rates above Topt ascribed to protein denaturation and/or aggregation. This account persists despite many investigators noting that denaturation is insufficient to explain the decline in enzymatic rates above Topt. Here we show that it is the change in heat capacity associated with enzyme catalysis (ΔC‡p) and its effect on the temperature dependence of ΔG‡ that determines the temperature dependence of enzyme activity. Through mutagenesis, we demonstrate that the Topt of an enzyme is correlated with ΔC‡p and that changes to ΔC‡p are sufficient to change Topt without affecting the catalytic rate. Furthermore, using X-ray crystallography and molecular dynamics simulations we reveal the molecular details underpinning these changes in ΔC‡p. The influence of ΔC‡p on enzymatic rates has implications for the temperature dependence of biological rates from enzymes to ecosystems.

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Data collection and refinement statistics for MalL enzymes; ΔC‡p values for microorganism growth rates; details of enzymes datasets included in Figure 3; key differences between the crystal structures of wildtype MalL, V200S, and G202P; ΔC‡p,obs values for the temperature dependence of microorganism growth rates.. This material is available free of charge via the Internet at http://pubs.acs.org.

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  3. Harmen B. B. Steele, Margaret M. Elmer-Dixon, James T. Rogan, J. B. Alexander Ross, Bruce E. Bowler. The Human Cytochrome c Domain-Swapped Dimer Facilitates Tight Regulation of Intrinsic Apoptosis. Biochemistry 2020, 59 (22) , 2055-2068. https://doi.org/10.1021/acs.biochem.0c00326
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  6. Teresa F. G. Machado, Tracey M. Gloster, Rafael G. da Silva. Linear Eyring Plots Conceal a Change in the Rate-Limiting Step in an Enzyme Reaction. Biochemistry 2018, 57 (49) , 6757-6761. https://doi.org/10.1021/acs.biochem.8b01099
  7. Vern L. Schramm. Enzymatic Transition States and Drug Design. Chemical Reviews 2018, 118 (22) , 11194-11258. https://doi.org/10.1021/acs.chemrev.8b00369
  8. Dan Davidi, Liam M. Longo, Jagoda Jabłońska, Ron Milo, Dan S. Tawfik. A Bird’s-Eye View of Enzyme Evolution: Chemical, Physicochemical, and Physiological Considerations. Chemical Reviews 2018, 118 (18) , 8786-8797. https://doi.org/10.1021/acs.chemrev.8b00039
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  11. Ross S. Firestone, Scott A. Cameron, Jerome M. Karp, Vickery L. Arcus, and Vern L. Schramm . Heat Capacity Changes for Transition-State Analogue Binding and Catalysis with Human 5′-Methylthioadenosine Phosphorylase. ACS Chemical Biology 2017, 12 (2) , 464-473. https://doi.org/10.1021/acschembio.6b00885
  12. James E. Longbotham, Samantha J. O. Hardman, Stefan Görlich, Nigel S. Scrutton, and Sam Hay . Untangling Heavy Protein and Cofactor Isotope Effects on Enzyme-Catalyzed Hydride Transfer. Journal of the American Chemical Society 2016, 138 (41) , 13693-13699. https://doi.org/10.1021/jacs.6b07852
  13. Ulrike Breitinger, Heinrich Sticht, and Hans-Georg Breitinger . Modulation of Recombinant Human α1 Glycine Receptors by Mono- and Disaccharides: A Kinetic Study. ACS Chemical Neuroscience 2016, 7 (8) , 1077-1087. https://doi.org/10.1021/acschemneuro.6b00044
  14. Vickery L. Arcus, Erica J. Prentice, Joanne K. Hobbs, Adrian J. Mulholland, Marc W. Van der Kamp, Christopher R. Pudney, Emily J. Parker, and Louis A. Schipper . On the Temperature Dependence of Enzyme-Catalyzed Rates. Biochemistry 2016, 55 (12) , 1681-1688. https://doi.org/10.1021/acs.biochem.5b01094
  15. Jaka Sočan, Miha Purg, Johan Åqvist. Computer simulations explain the anomalous temperature optimum in a cold-adapted enzyme. Nature Communications 2020, 11 (1) https://doi.org/10.1038/s41467-020-16341-2
  16. Bridget K. Murphy, Joseph R. Stinziano. A derivation error that affects carbon balance models exists in the current implementation of the modified Arrhenius function. New Phytologist 2020, 123 https://doi.org/10.1111/nph.16883
  17. Zhongkui Luo, Zuoxin Tang, Xiaowei Guo, Jiang Jiang, Osbert Jianxin Sun. Non-monotonic and distinct temperature responses of respiration of soil microbial functional groups. Soil Biology and Biochemistry 2020, 148 , 107902. https://doi.org/10.1016/j.soilbio.2020.107902
  18. Jasmine M. Robinson, Shaun L. L. Barker, Vickery L. Arcus, Samuel R. McNally, Louis A. Schipper. Contrasting temperature responses of soil respiration derived from soil organic matter and added plant litter. Biogeochemistry 2020, 150 (1) , 45-59. https://doi.org/10.1007/s10533-020-00686-3
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  20. Charlotte J. Alster, Joseph C. Fischer, Steven D. Allison, Kathleen K. Treseder. Embracing a new paradigm for temperature sensitivity of soil microbes. Global Change Biology 2020, 26 (6) , 3221-3229. https://doi.org/10.1111/gcb.15053
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  24. Linus O. Johannissen, Andreea I. Iorgu, Nigel S. Scrutton, Sam Hay. What are the signatures of tunnelling in enzyme-catalysed reactions?. Faraday Discussions 2020, 221 , 367-378. https://doi.org/10.1039/C9FD00044E
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  26. Philipp Noll, Lars Lilge, Rudolf Hausmann, Marius Henkel. Modeling and Exploiting Microbial Temperature Response. Processes 2020, 8 (1) , 121. https://doi.org/10.3390/pr8010121
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  33. Anne E. Taylor, David D. Myrold, Peter J. Bottomley. Temperature affects the kinetics of nitrite oxidation and nitrification coupling in four agricultural soils. Soil Biology and Biochemistry 2019, 136 , 107523. https://doi.org/10.1016/j.soilbio.2019.107523
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  39. Marc W. van der Kamp, Erica J. Prentice, Kirsty L. Kraakman, Michael Connolly, Adrian J. Mulholland, Vickery L. Arcus. Dynamical origins of heat capacity changes in enzyme-catalysed reactions. Nature Communications 2018, 9 (1) https://doi.org/10.1038/s41467-018-03597-y
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  50. Dimitrios - Georgios Kontopoulos, Bernardo García-Carreras, Sofía Sal, Thomas P. Smith, Samraat Pawar. Use and misuse of temperature normalisation in meta-analyses of thermal responses of biological traits. PeerJ 2018, 6 , e4363. https://doi.org/10.7717/peerj.4363
  51. Etienne Low-Décarie, Tobias G. Boatman, Noah Bennett, Will Passfield, Antonio Gavalás-Olea, Philipp Siegel, Richard J. Geider. Predictions of response to temperature are contingent on model choice and data quality. Ecology and Evolution 2017, 7 (23) , 10467-10481. https://doi.org/10.1002/ece3.3576
  52. Ghjuvan Micaelu Grimaud, Francis Mairet, Antoine Sciandra, Olivier Bernard. Modeling the temperature effect on the specific growth rate of phytoplankton: a review. Reviews in Environmental Science and Bio/Technology 2017, 16 (4) , 625-645. https://doi.org/10.1007/s11157-017-9443-0
  53. Mariane Rotta, Luis F. S. M. Timmers, Carlos Sequeiros-Borja, Cristiano V. Bizarro, Osmar N. de Souza, Diogenes S. Santos, Luiz A. Basso. Observed crowding effects on Mycobacterium tuberculosis 2-trans-enoyl-ACP (CoA) reductase enzyme activity are not due to excluded volume only. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/s41598-017-07266-w
  54. Hannah B. L. Jones, Stephen A Wells, Erica J Prentice, Anthony Kwok, Liyin L Liang, Vickery L Arcus, Christopher R Pudney. A complete thermodynamic analysis of enzyme turnover links the free energy landscape to enzyme catalysis. The FEBS Journal 2017, 284 (17) , 2829-2842. https://doi.org/10.1111/febs.14152
  55. Laura Silva, Giovanni Vladilo, Patricia M. Schulte, Giuseppe Murante, Antonello Provenzale. From climate models to planetary habitability: temperature constraints for complex life. International Journal of Astrobiology 2017, 16 (3) , 244-265. https://doi.org/10.1017/S1473550416000215
  56. Johan Åqvist, Geir Villy Isaksen, Bjørn Olav Brandsdal. Computation of enzyme cold adaptation. Nature Reviews Chemistry 2017, 1 (7) https://doi.org/10.1038/s41570-017-0051
  57. Thomas M. Luhring, John P. DeLong. Scaling from Metabolism to Population Growth Rate to Understand How Acclimation Temperature Alters Thermal Performance. Integrative and Comparative Biology 2017, 57 (1) , 103-111. https://doi.org/10.1093/icb/icx041
  58. J. P. DeLong, J. P. Gibert, T. M. Luhring, G. Bachman, B. Reed, A. Neyer, K. L. Montooth. The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates. Ecology and Evolution 2017, 7 (11) , 3940-3950. https://doi.org/10.1002/ece3.2955
  59. Anne E Taylor, Andrew T Giguere, Conor M Zoebelein, David D Myrold, Peter J Bottomley. Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. The ISME Journal 2017, 11 (4) , 896-908. https://doi.org/10.1038/ismej.2016.179
  60. J. M. Robinson, T. A. O’Neill, J. Ryburn, L. L. Liang, V. L. Arcus, L. A. Schipper. Rapid laboratory measurement of the temperature dependence of soil respiration and application to changes in three diverse soils through the year. Biogeochemistry 2017, 133 (1) , 101-112. https://doi.org/10.1007/s10533-017-0314-0
  61. Vy Nguyen, Christopher Wilson, Marc Hoemberger, John B. Stiller, Roman V. Agafonov, Steffen Kutter, Justin English, Douglas L. Theobald, Dorothee Kern. Evolutionary drivers of thermoadaptation in enzyme catalysis. Science 2017, 355 (6322) , 289-294. https://doi.org/10.1126/science.aah3717
  62. Carlos A. Sierra, Saadatullah Malghani, Henry W. Loescher. Interactions among temperature, moisture, and oxygen concentrations in controlling decomposition rates in a boreal forest soil. Biogeosciences 2017, 14 (3) , 703-710. https://doi.org/10.5194/bg-14-703-2017
  63. Charlotte J. Alster, Peter Baas, Matthew D. Wallenstein, Nels G. Johnson, Joseph C. von Fischer. Temperature Sensitivity as a Microbial Trait Using Parameters from Macromolecular Rate Theory. Frontiers in Microbiology 2016, 7 https://doi.org/10.3389/fmicb.2016.01821
  64. S. Sandeep, K. M. Manjaiah, M. R. Mayadevi, A. K. Singh. Monitoring temperature sensitivity of soil organic carbon decomposition under maize–wheat cropping systems in semi-arid India. Environmental Monitoring and Assessment 2016, 188 (8) https://doi.org/10.1007/s10661-016-5455-4
  65. Masayuki Okuyama, Wataru Saburi, Haruhide Mori, Atsuo Kimura. α-Glucosidases and α-1,4-glucan lyases: structures, functions, and physiological actions. Cellular and Molecular Life Sciences 2016, 73 (14) , 2727-2751. https://doi.org/10.1007/s00018-016-2247-5
  66. Charlotte J. Alster, Akihiro Koyama, Nels G. Johnson, Matthew D. Wallenstein, Joseph C. von Fischer. Temperature sensitivity of soil microbial communities: An application of macromolecular rate theory to microbial respiration. Journal of Geophysical Research: Biogeosciences 2016, 121 (6) , 1420-1433. https://doi.org/10.1002/2016JG003343
  67. Samraat Pawar, Anthony I. Dell, Van M. Savage, Jennifer L. Knies. Real versus Artificial Variation in the Thermal Sensitivity of Biological Traits. The American Naturalist 2016, 187 (2) , E41-E52. https://doi.org/10.1086/684590
  68. Helen R. Broom, Jessica A. O. Rumfeldt, Kenrick A. Vassall, Elizabeth M. Meiering. Destabilization of the dimer interface is a common consequence of diverse ALS-associated mutations in metal free SOD1. Protein Science 2015, 24 (12) , 2081-2089. https://doi.org/10.1002/pro.2803
  69. Vickery L. Arcus, Christopher R. Pudney. Change in heat capacity accurately predicts vibrational coupling in enzyme catalyzed reactions. FEBS Letters 2015, 589 (17) , 2200-2206. https://doi.org/10.1016/j.febslet.2015.06.042
  70. Louis A. Schipper, Joanne K. Hobbs, Susanna Rutledge, Vickery L. Arcus. Thermodynamic theory explains the temperature optima of soil microbial processes and high Q10 values at low temperatures. Global Change Biology 2014, 20 (11) , 3578-3586. https://doi.org/10.1111/gcb.12596

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