IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41424-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41424-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41424-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Lena Takayasu & Wataru Suda & Eiichiro Watanabe & Shinji Fukuda & Kageyasu Takanashi & Hiroshi Ohno & Misako Takayasu & Hideki Takayasu & Masahira Hattori, 2017. "A 3-dimensional mathematical model of microbial proliferation that generates the characteristic cumulative relative abundance distributions in gut microbiomes," PLOS ONE, Public Library of Science, vol. 12(8), pages 1-20, August.
    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. Li Zhang & Karen R. Jonscher & Zuyuan Zhang & Yi Xiong & Ryan S. Mueller & Jacob E. Friedman & Chongle Pan, 2022. "Islet autoantibody seroconversion in type-1 diabetes is associated with metagenome-assembled genomes in infant gut microbiomes," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Giuseppe Malgioglio & Giulio Flavio Rizzo & Sebastian Nigro & Vincent Lefebvre du Prey & Joelle Herforth-Rahmé & Vittoria Catara & Ferdinando Branca, 2022. "Plant-Microbe Interaction in Sustainable Agriculture: The Factors That May Influence the Efficacy of PGPM Application," Sustainability, MDPI, vol. 14(4), pages 1-28, February.
    5. Kenneth A. Wilson & Sudipta Bar & Eric B. Dammer & Enrique M. Carrera & Brian A. Hodge & Tyler A. U. Hilsabeck & Joanna Bons & George W. Brownridge & Jennifer N. Beck & Jacob Rose & Melia Granath-Pane, 2024. "OXR1 maintains the retromer to delay brain aging under dietary restriction," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Hunter R Johnson & Donovan D Trinidad & Stephania Guzman & Zenab Khan & James V Parziale & Jennifer M DeBruyn & Nathan H Lents, 2016. "A Machine Learning Approach for Using the Postmortem Skin Microbiome to Estimate the Postmortem Interval," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-23, December.
    7. Sandra M. Holmberg & Rachel H. Feeney & Vishnu Prasoodanan P.K. & Fabiola Puértolas-Balint & Dhirendra K. Singh & Supapit Wongkuna & Lotte Zandbergen & Hans Hauner & Beate Brandl & Anni I. Nieminen & , 2024. "The gut commensal Blautia maintains colonic mucus function under low-fiber consumption through secretion of short-chain fatty acids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Iris Chen & Yogeshwar D Kelkar & Yu Gu & Jie Zhou & Xing Qiu & Hulin Wu, 2017. "High-dimensional linear state space models for dynamic microbial interaction networks," PLOS ONE, Public Library of Science, vol. 12(11), pages 1-20, November.
    9. Joanna F Dipnall & Julie A Pasco & Michael Berk & Lana J Williams & Seetal Dodd & Felice N Jacka & Denny Meyer, 2016. "Into the Bowels of Depression: Unravelling Medical Symptoms Associated with Depression by Applying Machine-Learning Techniques to a Community Based Population Sample," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-19, December.
    10. Vinod Nikhra, 2019. "Therapeutic Potential of Gut Microbiome Manipulation: Concepts in Fecal Microbiota Transplantation," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 1-9, June.
    11. Dekaj, Ermanda & Gjini, Erida, 2024. "Pneumococcus and the stress-gradient hypothesis: A trade-off links R0 and susceptibility to co-colonization across countries," Theoretical Population Biology, Elsevier, vol. 156(C), pages 77-92.
    12. Huimin Ye & Sabrina Borusak & Claudia Eberl & Julia Krasenbrink & Anna S. Weiss & Song-Can Chen & Buck T. Hanson & Bela Hausmann & Craig W. Herbold & Manuel Pristner & Benjamin Zwirzitz & Benedikt War, 2023. "Ecophysiology and interactions of a taurine-respiring bacterium in the mouse gut," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Amanda H Pendegraft & Boyi Guo & Nengjun Yi, 2019. "Bayesian hierarchical negative binomial models for multivariable analyses with applications to human microbiome count data," PLOS ONE, Public Library of Science, vol. 14(8), pages 1-23, August.
    14. Hannaford, Naomi E. & Heaps, Sarah E. & Nye, Tom M.W. & Curtis, Thomas P. & Allen, Ben & Golightly, Andrew & Wilkinson, Darren J., 2023. "A sparse Bayesian hierarchical vector autoregressive model for microbial dynamics in a wastewater treatment plant," Computational Statistics & Data Analysis, Elsevier, vol. 179(C).
    15. Robin D Couch & Allyson Dailey & Fatima Zaidi & Karl Navarro & Christopher B Forsyth & Ece Mutlu & Phillip A Engen & Ali Keshavarzian, 2015. "Alcohol Induced Alterations to the Human Fecal VOC Metabolome," PLOS ONE, Public Library of Science, vol. 10(3), pages 1-24, March.
    16. Elio L Herzog & Melania Wäfler & Irene Keller & Sebastian Wolf & Martin S Zinkernagel & Denise C Zysset-Burri, 2021. "The importance of age in compositional and functional profiling of the human intestinal microbiome," PLOS ONE, Public Library of Science, vol. 16(10), pages 1-13, October.
    17. Lu Wu & Xu-Wen Wang & Zining Tao & Tong Wang & Wenlong Zuo & Yu Zeng & Yang-Yu Liu & Lei Dai, 2024. "Data-driven prediction of colonization outcomes for complex microbial communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    18. Mika Saarenpää & Marja I. Roslund & Riikka Puhakka & Mira Grönroos & Anirudra Parajuli & Nan Hui & Noora Nurminen & Olli H. Laitinen & Heikki Hyöty & Ondrej Cinek & Aki Sinkkonen & the ADELE Research , 2021. "Do Rural Second Homes Shape Commensal Microbiota of Urban Dwellers? A Pilot Study among Urban Elderly in Finland," IJERPH, MDPI, vol. 18(7), pages 1-19, April.
    19. Alice Risely & Kerstin Wilhelm & Tim Clutton-Brock & Marta B. Manser & Simone Sommer, 2021. "Diurnal oscillations in gut bacterial load and composition eclipse seasonal and lifetime dynamics in wild meerkats," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    20. Narongrit Sritana & Atitaya Phungpinij, 2024. "Analysis of Oral Microbiota in Elderly Thai Patients with Alzheimer’s Disease and Mild Cognitive Impairment," IJERPH, MDPI, vol. 21(9), pages 1-15, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41424-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.