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Optogenetic spatial patterning of cooperation in yeast populations

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  • Matthias Bec

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Sylvain Pouzet

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Céline Cordier

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Simon Barral

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Vittore Scolari

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie
    Université PSL, Sorbonne Université, CNRS UMR3664, Laboratoire Dynamique du Noyau)

  • Benoit Sorre

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Alvaro Banderas

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

  • Pascal Hersen

    (Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico Chimie Curie)

Abstract

Microbial communities are shaped by complex metabolic interactions such as cooperation and competition for resources. Methods to control such interactions could lead to major advances in our ability to better engineer microbial consortia for synthetic biology applications. Here, we use optogenetics to control SUC2 invertase production in yeast, thereby shaping spatial assortment of cooperator and cheater cells. Yeast cells behave as cooperators (i.e., transform sucrose into hexose, a public good) upon blue light illumination or cheaters (i.e., consume hexose produced by cooperators to grow) in the dark. We show that cooperators benefit best from the hexoses they produce when their domain size is constrained between two cut-off length-scales. From an engineering point of view, the system behaves as a bandpass filter. The lower limit is the trace of cheaters’ competition for hexoses, while the upper limit is defined by cooperators’ competition for sucrose. Cooperation mostly occurs at the frontiers with cheater cells, which not only compete for hexoses but also cooperate passively by letting sucrose reach cooperators. We anticipate that this optogenetic method could be applied to shape metabolic interactions in a variety of microbial ecosystems.

Suggested Citation

  • Matthias Bec & Sylvain Pouzet & Céline Cordier & Simon Barral & Vittore Scolari & Benoit Sorre & Alvaro Banderas & Pascal Hersen, 2024. "Optogenetic spatial patterning of cooperation in yeast populations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44379-5
    DOI: 10.1038/s41467-023-44379-5
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    References listed on IDEAS

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    1. Xianglai Li & Zhao Zhou & Wenna Li & Yajun Yan & Xiaolin Shen & Jia Wang & Xinxiao Sun & Qipeng Yuan, 2022. "Design of stable and self-regulated microbial consortia for chemical synthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Dirk Benzinger & Mustafa Khammash, 2018. "Pulsatile inputs achieve tunable attenuation of gene expression variability and graded multi-gene regulation," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    3. Sonali Gupta & Tyler D. Ross & Marcella M. Gomez & Job L. Grant & Philip A. Romero & Ophelia S. Venturelli, 2020. "Investigating the dynamics of microbial consortia in spatially structured environments," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    4. Daniel Lelie & Akihiko Oka & Safiyh Taghavi & Junji Umeno & Ting-Jia Fan & Katherine E. Merrell & Sarah D. Watson & Lisa Ouellette & Bo Liu & Muyiwa Awoniyi & Yunjia Lai & Liang Chi & Kun Lu & Christo, 2021. "Rationally designed bacterial consortia to treat chronic immune-mediated colitis and restore intestinal homeostasis," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    5. Jeff Gore & Hyun Youk & Alexander van Oudenaarden, 2009. "Snowdrift game dynamics and facultative cheating in yeast," Nature, Nature, vol. 459(7244), pages 253-256, May.
    6. Jintao Liu & Arthur Prindle & Jacqueline Humphries & Marçal Gabalda-Sagarra & Munehiro Asally & Dong-yeon D. Lee & San Ly & Jordi Garcia-Ojalvo & Gürol M. Süel, 2015. "Metabolic co-dependence gives rise to collective oscillations within biofilms," Nature, Nature, vol. 523(7562), pages 550-554, July.
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