The bioenergetic cost of building a metazoan

All life forms depend on the conversion of energy into biomass used in growth and reproduction. For unicellular heterotrophs, the energetic cost associated with building a cell scales slightly sublinearly with cell weight. However, observations on multiple <i>Daphnia</i> species and numerous other metazoans suggest that although a similar size-specific scaling is retained in multicellular heterotrophs, there is a quantum leap in the energy required to build a replacement soma, presumably owing to the added investment in nonproductive features such as cell adhesion, support tissue, and intercellular communication and transport. Thus, any context-dependent ecological advantages that accompany the evolution of multicellularity come at a high baseline bioenergetic cost. At the phylogenetic level, for both unicellular and multicellular eukaryotes, the energetic expense per unit biomass produced declines with increasing adult size of a species, but there is a countergradient scaling within the developmental trajectories of individual metazoan species, with the cost of biomass production increasing with size. Translation of the results into the universal currency of adenosine triphosphate (ATP) hydrolyses provides insight into the demands on the electron-transport/ATP-synthase machinery per organism and on the minimum doubling times for biomass production imposed by the costs of duplicating the energy-producing infrastructure.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-11-07
DOI
https://doi.org/10.1073/pnas.2414742121
Citations
11
Primary Topic
Physiological and biochemical adaptations
Type
article
Field-Weighted Citation Impact
5.05

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article

The bioenergetic cost of building a metazoan

Michael F. Lynch
11 citations
Proceedings of the National Academy of Sciences
Physiological and biochemical adaptations
5.05
article

The bioenergetic cost of building a metazoan

Michael F. Lynch
article en
11 citations

Abstract

All life forms depend on the conversion of energy into biomass used in growth and reproduction. For unicellular heterotrophs, the energetic cost associated with building a cell scales slightly sublinearly with cell weight. However, observations on multiple <i>Daphnia</i> species and numerous other metazoans suggest that although a similar size-specific scaling is retained in multicellular heterotrophs, there is a quantum leap in the energy required to build a replacement soma, presumably owing to the added investment in nonproductive features such as cell adhesion, support tissue, and intercellular communication and transport. Thus, any context-dependent ecological advantages that accompany the evolution of multicellularity come at a high baseline bioenergetic cost. At the phylogenetic level, for both unicellular and multicellular eukaryotes, the energetic expense per unit biomass produced declines with increasing adult size of a species, but there is a countergradient scaling within the developmental trajectories of individual metazoan species, with the cost of biomass production increasing with size. Translation of the results into the universal currency of adenosine triphosphate (ATP) hydrolyses provides insight into the demands on the electron-transport/ATP-synthase machinery per organism and on the minimum doubling times for biomass production imposed by the costs of duplicating the energy-producing infrastructure.

Proceedings of the National Academy of SciencesVol. 121(46)
Arizona State University (US)
National Science Foundation, Gordon and Betty Moore Foundation, National Institutes of Health, Division of Integrative Organismal Systems, Division of Environmental Biology
Openalex Percentile: Top 5%
Physiological and biochemical adaptations
5.05
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