IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27023-y.html
   My bibliography  Save this article

Complementary resource preferences spontaneously emerge in diauxic microbial communities

Author

Listed:
  • Zihan Wang

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Akshit Goyal

    (Massachusetts Institute of Technology)

  • Veronika Dubinkina

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Ashish B. George

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Tong Wang

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Yulia Fridman

    (National Research Center “Kurchatov Institute”)

  • Sergei Maslov

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

Abstract

Many microbes grow diauxically, utilizing the available resources one at a time rather than simultaneously. The properties of communities of microbes growing diauxically remain poorly understood, largely due to a lack of theory and models of such communities. Here, we develop and study a minimal model of diauxic microbial communities assembling in a serially diluted culture. We find that unlike co-utilizing communities, diauxic community assembly repeatably and spontaneously leads to communities with complementary resource preferences, namely communities where species prefer different resources as their top choice. Simulations and theory explain that the emergence of complementarity is driven by the disproportionate contribution of the top choice resource to the growth of a diauxic species. Additionally, we develop a geometric approach for analyzing serially diluted communities, with or without diauxie, which intuitively explains several additional emergent community properties, such as the apparent lack of species which grow fastest on a resource other than their most preferred resource. Overall, our work provides testable predictions for the assembly of natural as well as synthetic communities of diauxically shifting microbes.

Suggested Citation

  • Zihan Wang & Akshit Goyal & Veronika Dubinkina & Ashish B. George & Tong Wang & Yulia Fridman & Sergei Maslov, 2021. "Complementary resource preferences spontaneously emerge in diauxic microbial communities," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27023-y
    DOI: 10.1038/s41467-021-27023-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27023-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-27023-y?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. Jed A. Fuhrman, 2009. "Microbial community structure and its functional implications," Nature, Nature, vol. 459(7244), pages 193-199, May.
    2. Artur Rogowski & Jonathon A. Briggs & Jennifer C. Mortimer & Theodora Tryfona & Nicolas Terrapon & Elisabeth C. Lowe & Arnaud Baslé & Carl Morland & Alison M. Day & Hongjun Zheng & Theresa E. Rogers &, 2015. "Glycan complexity dictates microbial resource allocation in the large intestine," Nature Communications, Nature, vol. 6(1), pages 1-16, November.
    3. Benjamin D. Towbin & Yael Korem & Anat Bren & Shany Doron & Rotem Sorek & Uri Alon, 2017. "Optimality and sub-optimality in a bacterial growth law," Nature Communications, Nature, vol. 8(1), pages 1-8, April.
    4. Elena Perrin & Veronica Ghini & Michele Giovannini & Francesca Di Patti & Barbara Cardazzo & Lisa Carraro & Camilla Fagorzi & Paola Turano & Renato Fani & Marco Fondi, 2020. "Diauxie and co-utilization of carbon sources can coexist during bacterial growth in nutritionally complex environments," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. Jaeyun Sung & Seunghyeon Kim & Josephine Jill T. Cabatbat & Sungho Jang & Yong-Su Jin & Gyoo Yeol Jung & Nicholas Chia & Pan-Jun Kim, 2017. "Global metabolic interaction network of the human gut microbiota for context-specific community-scale analysis," Nature Communications, Nature, vol. 8(1), pages 1-12, August.
    6. Erez Dekel & Uri Alon, 2005. "Optimality and evolutionary tuning of the expression level of a protein," Nature, Nature, vol. 436(7050), pages 588-592, July.
    7. Alan R. Pacheco & Melisa L. Osborne & Daniel Segrè, 2021. "Non-additive microbial community responses to environmental complexity," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    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. Robert Planqué & Josephus Hulshof & Bas Teusink & Johannes C Hendriks & Frank J Bruggeman, 2018. "Maintaining maximal metabolic flux by gene expression control," PLOS Computational Biology, Public Library of Science, vol. 14(9), pages 1-20, September.
    2. Leon Dlugosch & Anja Poehlein & Bernd Wemheuer & Birgit Pfeiffer & Thomas H. Badewien & Rolf Daniel & Meinhard Simon, 2022. "Significance of gene variants for the functional biogeography of the near-surface Atlantic Ocean microbiome," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Matteo Mori & Chuankai Cheng & Brian R. Taylor & Hiroyuki Okano & Terence Hwa, 2023. "Functional decomposition of metabolism allows a system-level quantification of fluxes and protein allocation towards specific metabolic functions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Ramón Verduzco-Oliva & Janet Alejandra Gutierrez-Uribe, 2020. "Beyond Enzyme Production: Solid State Fermentation (SSF) as an Alternative Approach to Produce Antioxidant Polysaccharides," Sustainability, MDPI, vol. 12(2), pages 1-14, January.
    5. William R Harcombe & Nigel F Delaney & Nicholas Leiby & Niels Klitgord & Christopher J Marx, 2013. "The Ability of Flux Balance Analysis to Predict Evolution of Central Metabolism Scales with the Initial Distance to the Optimum," PLOS Computational Biology, Public Library of Science, vol. 9(6), pages 1-11, June.
    6. Itxaso Anso & Andreas Naegeli & Javier O. Cifuente & Ane Orrantia & Erica Andersson & Olatz Zenarruzabeitia & Alicia Moraleda-Montoya & Mikel García-Alija & Francisco Corzana & Rafael A. Orbe & Franci, 2023. "Turning universal O into rare Bombay type blood," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Vanessa R. Marcelino & Caitlin Welsh & Christian Diener & Emily L. Gulliver & Emily L. Rutten & Remy B. Young & Edward M. Giles & Sean M. Gibbons & Chris Greening & Samuel C. Forster, 2023. "Disease-specific loss of microbial cross-feeding interactions in the human gut," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Avraham E Mayo & Yaakov Setty & Seagull Shavit & Alon Zaslaver & Uri Alon, 2006. "Plasticity of the cis-Regulatory Input Function of a Gene," PLOS Biology, Public Library of Science, vol. 4(4), pages 1-1, March.
    9. Lei Zhang & Yu Cheng & Guang Gao & Jiahu Jiang, 2019. "Spatial-Temporal Variation of Bacterial Communities in Sediments in Lake Chaohu, a Large, Shallow Eutrophic Lake in China," IJERPH, MDPI, vol. 16(20), pages 1-18, October.
    10. David A Sivak & Matt Thomson, 2014. "Environmental Statistics and Optimal Regulation," PLOS Computational Biology, Public Library of Science, vol. 10(9), pages 1-12, September.
    11. Ruoyu Luo & Lin Ye & Chenyang Tao & Kankan Wang, 2013. "Simulation of E. coli Gene Regulation including Overlapping Cell Cycles, Growth, Division, Time Delays and Noise," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-10, April.
    12. Jennifer L. Modesto & Victoria H. Pearce & Guy E. Townsend, 2023. "Harnessing gut microbes for glycan detection and quantification," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Shengbo Wu & Jie Feng & Chunjiang Liu & Hao Wu & Zekai Qiu & Jianjun Ge & Shuyang Sun & Xia Hong & Yukun Li & Xiaona Wang & Aidong Yang & Fei Guo & Jianjun Qiao, 2022. "Machine learning aided construction of the quorum sensing communication network for human gut microbiota," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    14. Rok Grah & Tamar Friedlander, 2020. "The relation between crosstalk and gene regulation form revisited," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-24, February.
    15. de Oliveira, Viviane M. & Amado, André & Campos, Paulo R.A., 2018. "The interplay of tradeoffs within the framework of a resource-based modelling," Ecological Modelling, Elsevier, vol. 384(C), pages 249-260.
    16. Yangyi Zhou & Jiangping Wang, 2023. "The Composition and Assembly of Soil Microbial Communities Differ across Vegetation Cover Types of Urban Green Spaces," Sustainability, MDPI, vol. 15(17), pages 1-15, August.
    17. Elise Vaumourin & Patrick Gasqui & Jean-Philippe Buffet & Jean-Louis Chapuis & Benoît Pisanu & Elisabeth Ferquel & Muriel Vayssier-Taussat & Gwenaël Vourc’h, 2013. "A Probabilistic Model in Cross-Sectional Studies for Identifying Interactions between Two Persistent Vector-Borne Pathogens in Reservoir Populations," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-9, June.
    18. Heneghan, Ryan F. & Everett, Jason D. & Sykes, Patrick & Batten, Sonia D. & Edwards, Martin & Takahashi, Kunio & Suthers, Iain M. & Blanchard, Julia L. & Richardson, Anthony J., 2020. "A functional size-spectrum model of the global marine ecosystem that resolves zooplankton composition," Ecological Modelling, Elsevier, vol. 435(C).
    19. Klement Stojanovski & Helge Großhans & Benjamin D. Towbin, 2022. "Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Xiaoping Xin & Jiali Shentu & Tiequan Zhang & Xiaoe Yang & Virupax C. Baligar & Zhenli He, 2022. "Sources, Indicators, and Assessment of Soil Contamination by Potentially Toxic Metals," Sustainability, MDPI, vol. 14(23), pages 1-16, November.

    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:12:y:2021:i:1:d:10.1038_s41467-021-27023-y. 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.