Growth, metabolic partitioning, and the size of microorganisms
Open accessAbstract
Population growth rate is a fundamental ecological and evolutionary characteristic of living organisms, but individuals must balance the metabolism devoted to biosynthesis and reproduction against the maintenance of existing structure and other functionality. Here we present a mathematical model that relates metabolic partitioning to the form of growth. The model captures the observed growth trajectory of single cells and individuals for a variety of species and taxa spanning prokaryotes, unicellular eukaryotes, and small multicellular eukaryotes. Our analysis suggests that the per-unit costs of biosynthesis and maintenance are conserved across prokaryotes and eukaryotes. However, the relative metabolic expenditure on growth and maintenance of whole organisms clearly differentiates taxa: prokaryotes spend an increasing fraction of their entire metabolism on growth with increasing cell size, whereas eukaryotes devote a diminishing fraction. These differences allow us to predict the minimum and maximum size for each taxonomic group, anticipating observed evolutionary life-history transitions. The framework provides energetic insights into taxonomic tradeoffs related to growth and metabolism and constrains traits that are important for size-structured modeling of microbial communities and their ecological and biogeochemical effects.
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Energy is a key consideration in the evolutionary optimization of organisms.
“Other arguments related to metabolic scaling indicate that energy is a key consideration in the evolutionary optimization of organisms [43,44,104,105].”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [105]
Because of the nature of these transitions, they are likely to be relevant in our understanding of macroevolutionary processes, ranging from punctuated equilibrium to the hierarchical nature of evolutionary change and the role that constraints play in setting transition points.
“Because of the nature of these transitions, they are likely to be relevant in our understanding of macroevolutionary processes, ranging from punctuated equilibrium [318] to the hierarchical nature of evolutionary change [346,347] and the role that constraints play in setting transition points [105,348,349].”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [105]
Cites
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Invariant Distribution of Promoter Activities in Escherichia coli
Zaslaver, A., Kaplan, S., Bren, A., Jinich, A., Mayo, A., Dekel, E., Alon, U., & Itzkovitz, S. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000545 · Cited by 92 · see citing works
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The thermodynamic efficiency of computations made in cells across the range of life
Kempes, C. P., Wolpert, D., Cohen, Z., & Pérez-Mercader, J. (2017) · Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rsta.2016.0343 · Cited by 68 · see citing works
Self-citationThe Scales That Limit: The Physical Boundaries of Evolution
Kempes, C. P., Koehl, M. A. R., & West, G. B. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00242 · Cited by 58 · see citing works
Self-citationFundamental constraints to the logic of living systems
Solé, R., Kempes, C. P., Corominas-Murtra, B., De Domenico, M., Kolchinsky, A., Lachmann, M., Libby, E., Saavedra, S., Smith, E., & Wolpert, D. (2024) · Interface Focus · doi:10.1098/rsfs.2024.0010 · Cited by 34 · see citing works
Self-citationScaling laws in enzyme function reveal a new kind of biochemical universality
Gagler, D. C., Karas, B., Kempes, C. P., Malloy, J., Mierzejewski, V., Goldman, A. D., Kim, H., & Walker, S. I. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2106655119 · Cited by 34 · see citing works
Self-citationGeneralized Stoichiometry and Biogeochemistry for Astrobiological Applications
Kempes, C. P., Follows, M. J., Smith, H., Graham, H., House, C. H., & Levin, S. A. (2021) · Bulletin of Mathematical Biology · doi:10.1007/s11538-021-00877-5 · Cited by 19 · see citing works
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- Authors
- Kempes, C. P., Dutkiewicz, S., & Follows, M. J.
- Affiliations
- Massachusetts Institute of Technology (US)
- University of New Mexico (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-12-27
- Volume
- 109
- Issue
- 2
- Pages
- 495-500
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3258615
- OpenAlex
- W1971529705
- Cited by
- 132
- References
- 2
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 17 · 2023: 8 · 2022: 10 · 2021: 13 · 2020: 7 · 2019: 13 · 2018: 8 · 2017: 9 · 2016: 7 · 2015: 4 · 2014: 6 · 2013: 5 · 2012: 1
- FWCI
- 3.67
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation
- National Aeronautics and Space Administration
- Gordon and Betty Moore Foundation
- Massachusetts Institute of Technology
- Topics
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- microbial growth, cell size, maintenance costs, biosynthesis, growth rate, prokaryotes, unicellular eukaryotes, multicellular eukaryotes, life-history trade-offs
- MeSH terms
- Energy Metabolism, Biological Evolution, Models, Biological, Population Density, Prokaryotic Cells, Species Specificity, Biosynthetic Pathways, Eukaryota
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