4.8 Article

Energetic scaling in microbial growth

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2107668118

Keywords

microbial growth; thermodynamics; energy dissipation; energy scaling; thermodynamic efficiency

Funding

  1. Department of Biological and Agricultural Engineering and AgriLife Research at Texas AM University
  2. US Department of Agriculture National Institute of Food and Agriculture [1023954]
  3. European Research Council under the European Union's Horizon 2020 Research and Innovation Programme [101001608]
  4. European Research Council (ERC) [101001608] Funding Source: European Research Council (ERC)

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The study provides a systematic analysis of microbial growth thermodynamics, demonstrating the relationship between microbial energy conversion, dissipation mechanisms, and entropy production. It shows that dissipation mechanisms are linked to the electron donor uptake rate, leading to a proportional relationship between thermodynamic efficiency and electron donor uptake rate.
Microbial growth is a clear example of organization and structure arising in nonequilibrium conditions. Due to the complexity of the microbial metabolic network, elucidating the fundamental principles governing microbial growth remains a challenge. Here, we present a systematic analysis of microbial growth thermodynamics, leveraging an extensive dataset on energy-limited monoculture growth. A consistent thermodynamic framework based on reaction stoichiometry allows us to quantify how much of the available energy microbes can efficiently convert into new biomass while dissipating the remaining energy into the environment and producing entropy. We show that dissipation mechanisms can be linked to the electron donor uptake rate, a fact leading to the central result that the thermodynamic efficiency is related to the electron donor uptake rate by the scaling law eta proportional to M-1/2 ED and to the growth yield by eta proportional to Y4/5. These findings allow us to rederive the Pirt equation from a thermodynamic perspective, providing a means to compute its coefficients, as well as a deeper understanding of the relationship between growth rate and yield. Our results provide rather general insights into the relation between mass and energy conversion in microbial growth with potentially wide application, especially in ecology and biotechnology.

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