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Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes

Author

Listed:
  • Joe J. Lim

    (University of Washington)

  • Christian Diener

    (Institute for Systems Biology)

  • James Wilson

    (Institute for Systems Biology)

  • Jacob J. Valenzuela

    (Institute for Systems Biology)

  • Nitin S. Baliga

    (Institute for Systems Biology
    University of Washington
    Lawrence Berkeley National Laboratory
    University of Washington)

  • Sean M. Gibbons

    (Institute for Systems Biology
    University of Washington
    University of Washington
    University of Washington)

Abstract

Longitudinal sampling of the stool has yielded important insights into the ecological dynamics of the human gut microbiome. However, human stool samples are available approximately once per day, while commensal population doubling times are likely on the order of minutes-to-hours. Despite this mismatch in timescales, much of the prior work on human gut microbiome time series modeling has assumed that day-to-day fluctuations in taxon abundances are related to population growth or death rates, which is likely not the case. Here, we propose an alternative model of the human gut as a stationary system, where population dynamics occur internally and the bacterial population sizes measured in a bolus of stool represent a steady-state endpoint of these dynamics. We formalize this idea as stochastic logistic growth. We show how this model provides a path toward estimating the growth phases of gut bacterial populations in situ. We validate our model predictions using an in vitro Escherichia coli growth experiment. Finally, we show how this method can be applied to densely-sampled human stool metagenomic time series data. We discuss how these growth phase estimates may be used to better inform metabolic modeling in flow-through ecosystems, like animal guts or industrial bioreactors.

Suggested Citation

  • Joe J. Lim & Christian Diener & James Wilson & Jacob J. Valenzuela & Nitin S. Baliga & Sean M. Gibbons, 2023. "Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41424-1
    DOI: 10.1038/s41467-023-41424-1
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    References listed on IDEAS

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    1. Lawrence A. David & Corinne F. Maurice & Rachel N. Carmody & David B. Gootenberg & Julie E. Button & Benjamin E. Wolfe & Alisha V. Ling & A. Sloan Devlin & Yug Varma & Michael A. Fischbach & Sudha B. , 2014. "Diet rapidly and reproducibly alters the human gut microbiome," Nature, Nature, vol. 505(7484), pages 559-563, January.
    2. Sean M Gibbons & Sean M Kearney & Chris S Smillie & Eric J Alm, 2017. "Two dynamic regimes in the human gut microbiome," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-20, February.
    3. Luke R. Thompson & Jon G. Sanders & Daniel McDonald & Amnon Amir & Joshua Ladau & Kenneth J. Locey & Robert J. Prill & Anupriya Tripathi & Sean M. Gibbons & Gail Ackermann & Jose A. Navas-Molina & Ste, 2017. "A communal catalogue reveals Earth’s multiscale microbial diversity," Nature, Nature, vol. 551(7681), pages 457-463, November.
    4. Amir Bashan & Travis E. Gibson & Jonathan Friedman & Vincent J. Carey & Scott T. Weiss & Elizabeth L. Hohmann & Yang-Yu Liu, 2016. "Universality of human microbial dynamics," Nature, Nature, vol. 534(7606), pages 259-262, June.
    5. Jacopo Grilli, 2020. "Macroecological laws describe variation and diversity in microbial communities," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    6. Stephen Nayfach & Zhou Jason Shi & Rekha Seshadri & Katherine S. Pollard & Nikos C. Kyrpides, 2019. "New insights from uncultivated genomes of the global human gut microbiome," Nature, Nature, vol. 568(7753), pages 505-510, April.
    7. Christian Schulz & Tjasa Kumelj & Emil Karlsen & Eivind Almaas, 2021. "Genome-scale metabolic modelling when changes in environmental conditions affect biomass composition," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-22, May.
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