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Research Article
Differing thermal sensitivities of physiological processes alter ATP allocation
Francis T. C. Pan, Scott L. Applebaum, Donal T. Manahan
Journal of Experimental Biology 2021 224: jeb233379 doi: 10.1242/jeb.233379 Published 19 January 2021
Francis T. C. Pan
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA
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  • ORCID record for Francis T. C. Pan
Scott L. Applebaum
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA
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Donal T. Manahan
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA
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  • For correspondence: manahan@usc.edu
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ABSTRACT

Changes in environmental temperature affect rate processes at all levels of biological organization. Yet the thermal sensitivity of specific physiological processes that affect allocation of the ATP pool within a species is less well understood. In this study of developmental stages of the Pacific oyster, Crassostrea gigas, thermal sensitivities were measured for growth, survivorship, protein synthesis, respiration and transport of amino acids and ions. At warmer temperatures, larvae grew faster but suffered increased mortality. An analysis of temperature sensitivity (Q10 values) revealed that protein synthesis, the major ATP-consuming process in larvae of C. gigas, is more sensitive to temperature change (Q10 value of 2.9±0.18) than metabolic rate (Q10 of 2.0±0.15). Ion transport by Na+/K+-ATPase measured in vivo has a Q10 value of 2.1±0.09. The corresponding value for glycine transport is 2.4±0.23. Differing thermal responses for protein synthesis and respiration result in a disproportional increase in the allocation of available ATP to protein synthesis with rising temperature. A bioenergetic model is presented illustrating how changes in growth and temperature affect allocation of the ATP pool. Over an environmentally relevant temperature range for this species, the proportion of the ATP pool allocated to protein synthesis increases from 35 to 65%. The greater energy demand to support protein synthesis with increasing temperature will compromise energy availability to support other essential physiological processes. Defining the trade-offs of ATP demand will provide insights into understanding the adaptive capacity of organisms to respond to various scenarios of environmental change.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: F.T.P., S.L.A., D.T.M.; Methodology: F.T.P., S.L.A., D.T.M.; Validation: F.T.P., S.L.A., D.T.M.; Formal analysis: F.T.P., S.L.A., D.T.M.; Investigation: F.T.P., S.L.A., D.T.M.; Resources: D.T.M.; Data curation: F.T.P., S.L.A., D.T.M.; Writing - original draft: F.T.P., D.T.M.; Writing - review & editing: F.T.P., S.L.A., D.T.M.; Visualization: F.T.P., S.L.A., D.T.M.; Supervision: D.T.M.; Project administration: D.T.M.; Funding acquisition: D.T.M.

  • Funding

    This work was supported by a grant from the US National Science Foundation (EF 121220587).

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.233379.supplemental

  • Received July 16, 2020.
  • Accepted December 7, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Crassostrea gigas
  • Larvae
  • Metabolic rate
  • Protein synthesis
  • Temperature
  • Phenotypic variation

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Research Article
Differing thermal sensitivities of physiological processes alter ATP allocation
Francis T. C. Pan, Scott L. Applebaum, Donal T. Manahan
Journal of Experimental Biology 2021 224: jeb233379 doi: 10.1242/jeb.233379 Published 19 January 2021
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Research Article
Differing thermal sensitivities of physiological processes alter ATP allocation
Francis T. C. Pan, Scott L. Applebaum, Donal T. Manahan
Journal of Experimental Biology 2021 224: jeb233379 doi: 10.1242/jeb.233379 Published 19 January 2021

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