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Culturing of a complex gut microbial community in mucin-hydrogel carriers reveals strain- and gene-associated spatial organization

Author

Listed:
  • Xiaofan Jin

    (Gladstone Institutes)

  • Feiqiao B. Yu

    (Chan-Zuckerberg Biohub)

  • Jia Yan

    (Chan-Zuckerberg Biohub)

  • Allison M. Weakley

    (Stanford University)

  • Veronika Dubinkina

    (Gladstone Institutes)

  • Xiandong Meng

    (Stanford University)

  • Katherine S. Pollard

    (Gladstone Institutes
    Chan-Zuckerberg Biohub
    University of California San Francisco)

Abstract

Microbial community function depends on both taxonomic composition and spatial organization. While composition of the human gut microbiome has been deeply characterized, less is known about the organization of microbes between regions such as lumen and mucosa and the microbial genes regulating this organization. Using a defined 117 strain community for which we generate high-quality genome assemblies, we model mucosa/lumen organization with in vitro cultures incorporating mucin hydrogel carriers as surfaces for bacterial attachment. Metagenomic tracking of carrier cultures reveals increased diversity and strain-specific spatial organization, with distinct strains enriched on carriers versus liquid supernatant, mirroring mucosa/lumen enrichment in vivo. A comprehensive search for microbial genes associated with this spatial organization identifies candidates with known adhesion-related functions, as well as novel links. These findings demonstrate that carrier cultures of defined communities effectively recapitulate fundamental aspects of gut spatial organization, enabling identification of key microbial strains and genes.

Suggested Citation

  • Xiaofan Jin & Feiqiao B. Yu & Jia Yan & Allison M. Weakley & Veronika Dubinkina & Xiandong Meng & Katherine S. Pollard, 2023. "Culturing of a complex gut microbial community in mucin-hydrogel carriers reveals strain- and gene-associated spatial organization," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39121-0
    DOI: 10.1038/s41467-023-39121-0
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    References listed on IDEAS

    as
    1. Siegfried Schloissnig & Manimozhiyan Arumugam & Shinichi Sunagawa & Makedonka Mitreva & Julien Tap & Ana Zhu & Alison Waller & Daniel R. Mende & Jens Roat Kultima & John Martin & Karthik Kota & Shamil, 2013. "Genomic variation landscape of the human gut microbiome," Nature, Nature, vol. 493(7430), pages 45-50, January.
    2. Hao Shi & Qiaojuan Shi & Benjamin Grodner & Joan Sesing Lenz & Warren R. Zipfel & Ilana Lauren Brito & Iwijn De Vlaminck, 2020. "Highly multiplexed spatial mapping of microbial communities," Nature, Nature, vol. 588(7839), pages 676-681, December.
    3. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
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