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Protein Thermodynamics Can Be Predicted Directly from Biological Growth Rates

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Listed:
  • Ross Corkrey
  • Tom A McMeekin
  • John P Bowman
  • David A Ratkowsky
  • June Olley
  • Tom Ross

Abstract

Life on Earth is capable of growing from temperatures well below freezing to above the boiling point of water, with some organisms preferring cooler and others hotter conditions. The growth rate of each organism ultimately depends on its intracellular chemical reactions. Here we show that a thermodynamic model based on a single, rate-limiting, enzyme-catalysed reaction accurately describes population growth rates in 230 diverse strains of unicellular and multicellular organisms. Collectively these represent all three domains of life, ranging from psychrophilic to hyperthermophilic, and including the highest temperature so far observed for growth (122°C). The results provide credible estimates of thermodynamic properties of proteins and obtain, purely from organism intrinsic growth rate data, relationships between parameters previously identified experimentally, thus bridging a gap between biochemistry and whole organism biology. We find that growth rates of both unicellular and multicellular life forms can be described by the same temperature dependence model. The model results provide strong support for a single highly-conserved reaction present in the last universal common ancestor (LUCA). This is remarkable in that it means that the growth rate dependence on temperature of unicellular and multicellular life forms that evolved over geological time spans can be explained by the same model.

Suggested Citation

  • Ross Corkrey & Tom A McMeekin & John P Bowman & David A Ratkowsky & June Olley & Tom Ross, 2014. "Protein Thermodynamics Can Be Predicted Directly from Biological Growth Rates," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-15, May.
    • Handle: RePEc:plo:pone00:0096100
    DOI: 10.1371/journal.pone.0096100
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    References listed on IDEAS

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    1. Bastien Boussau & Samuel Blanquart & Anamaria Necsulea & Nicolas Lartillot & Manolo Gouy, 2008. "Parallel adaptations to high temperatures in the Archaean eon," Nature, Nature, vol. 456(7224), pages 942-945, December.
    2. Ross Corkrey & June Olley & David Ratkowsky & Tom McMeekin & Tom Ross, 2012. "Universality of Thermodynamic Constants Governing Biological Growth Rates," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-8, February.
    3. Roberts, G. O. & Gilks, W. R., 1994. "Convergence of Adaptive Direction Sampling," Journal of Multivariate Analysis, Elsevier, vol. 49(2), pages 287-298, May.
    4. Heather L. True & Susan L. Lindquist, 2000. "A yeast prion provides a mechanism for genetic variation and phenotypic diversity," Nature, Nature, vol. 407(6803), pages 477-483, September.
    5. Lynn J. Rothschild & Rocco L. Mancinelli, 2001. "Life in extreme environments," Nature, Nature, vol. 409(6823), pages 1092-1101, February.
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    1. Lisson, S.N. & Tarbath, M. & Corkrey, R. & Pinkard, E.A. & Laycock, B. & Howden, S.M. & Botwright Acuña, T. & Makin, A., 2016. "Ambient climate and soil effects on the headspace under clear mulch film," Agricultural Systems, Elsevier, vol. 142(C), pages 41-50.

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