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Functional convergence in slow-growing microbial communities arises from thermodynamic constraints

The ISME Journal volume 17, pages 1482–1494 (2023)Cite this article

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Abstract

The dynamics of microbial communities is complex, determined by competition for metabolic substrates and cross-feeding of byproducts. Species in the community grow by harvesting energy from chemical reactions that transform substrates to products. In many anoxic environments, these reactions are close to thermodynamic equilibrium and growth is slow. To understand the community structure in these energy-limited environments, we developed a microbial community consumer-resource model incorporating energetic and thermodynamic constraints on an interconnected metabolic network. The central element of the model is product inhibition, meaning that microbial growth may be limited not only by depletion of metabolic substrates but also by accumulation of products. We demonstrate that these additional constraints on microbial growth cause a convergence in the structure and function of the community metabolic network—independent of species composition and biochemical details—providing a possible explanation for convergence of community function despite taxonomic variation observed in many natural and industrial environments. Furthermore, we discovered that the structure of community metabolic network is governed by the thermodynamic principle of maximum free energy dissipation. Our results predict the decrease of functional convergence in faster growing communities, which we validate by analyzing experimental data from anaerobic digesters. Overall, the work demonstrates how universal thermodynamic principles may constrain community metabolism and explain observed functional convergence in microbial communities.

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Fig. 1: Model of communities in energy-limited environments.
Fig. 2: Functional convergence despite taxonomic variation.
Fig. 3: The maximum dissipation principle determines the community metabolic network.
Fig. 4: Functional convergence and the strength of thermodynamic constraints decreases in fast-growing communities.
Fig. 5: Metabolic convergence in experimental anaerobic digesters weakens with dilution rate.
Fig. 6: Functional convergence decreases with increasing reaction energies.

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Data availability

Experimental data analyzed were obtained from ref. [53].

Code availability

Code used for simulation and analysis can be found at https://github.com/maslov-group/Thermodynamics_functional_convergence.git.

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Acknowledgements

The authors thank Avi Flamholz for valuable comments and feedback on the manuscript. This research was supported in part by NSF Grant No. PHY-1748958 and the Gordon and Betty Moore Foundation Grant No. 2919.02.

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Authors and Affiliations

  1. Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Ashish B. George, Tong Wang & Sergei Maslov

  2. Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Ashish B. George

  3. Department of Physics, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Tong Wang & Sergei Maslov

  4. Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, 02115, USA

    Tong Wang

  5. Department of Bioengineering, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Sergei Maslov

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All authors helped devise the study; ABG performed the research and analyzed the data; SM supervised the research; ABG wrote the manuscript with help from SM and TW.

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Correspondence to Sergei Maslov.

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George, A.B., Wang, T. & Maslov, S. Functional convergence in slow-growing microbial communities arises from thermodynamic constraints. ISME J 17, 1482–1494 (2023). https://doi.org/10.1038/s41396-023-01455-4

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