IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44379-5.html
   My bibliography  Save this article

Optogenetic spatial patterning of cooperation in yeast populations

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44379-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44379-5?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. 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. 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.
    3. 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.
    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. 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.
    6. 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.
    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. David Bruce Borenstein & Yigal Meir & Joshua W Shaevitz & Ned S Wingreen, 2013. "Non-Local Interaction via Diffusible Resource Prevents Coexistence of Cooperators and Cheaters in a Lattice Model," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-10, May.
    2. Yuzhen Zhang & Yukmi Cai & Bing Zhang & Yi-Heng P. Job Zhang, 2024. "Spatially structured exchange of metabolites enhances bacterial survival and resilience in biofilms," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Jorge Peña & Yannick Rochat, 2012. "Bipartite Graphs as Models of Population Structures in Evolutionary Multiplayer Games," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-13, September.
    4. Xiaojie Chen & Attila Szolnoki, 2018. "Punishment and inspection for governing the commons in a feedback-evolving game," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-15, July.
    5. Ankit Gupta & Mustafa Khammash, 2022. "Frequency spectra and the color of cellular noise," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Gita Naseri, 2023. "A roadmap to establish a comprehensive platform for sustainable manufacturing of natural products in yeast," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. John C. Boik, 2016. "Optimality of Social Choice Systems: Complexity, Wisdom, and Wellbeing Centrality," Working Paper 0005, Principled Societies Project, revised Mar 2017.
    8. Felix J H Hol & Peter Galajda & Krisztina Nagy & Rutger G Woolthuis & Cees Dekker & Juan E Keymer, 2013. "Spatial Structure Facilitates Cooperation in a Social Dilemma: Empirical Evidence from a Bacterial Community," PLOS ONE, Public Library of Science, vol. 8(10), pages 1-10, October.
    9. Kerry E Boyle & Hilary Monaco & Dave van Ditmarsch & Maxime Deforet & Joao B Xavier, 2015. "Integration of Metabolic and Quorum Sensing Signals Governing the Decision to Cooperate in a Bacterial Social Trait," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-26, June.
    10. Claudius Gros, 2022. "Generic catastrophic poverty when selfish investors exploit a degradable common resource," Papers 2208.08171, arXiv.org, revised Jan 2023.
    11. Wu, Yu’e & Zhang, Zhipeng & Wang, Xinyu & Chang, Shuhua, 2019. "Impact of probabilistic incentives on the evolution of cooperation in complex topologies," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 513(C), pages 307-314.
    12. Maxime Batsch & Isaline Guex & Helena Todorov & Clara M. Heiman & Jordan Vacheron & Julia A. Vorholt & Christoph Keel & Jan Roelof van der Meer, 2024. "Fragmented micro-growth habitats present opportunities for alternative competitive outcomes," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    13. François Bertaux & Sebastián Sosa-Carrillo & Viktoriia Gross & Achille Fraisse & Chetan Aditya & Mariela Furstenheim & Gregory Batt, 2022. "Enhancing bioreactor arrays for automated measurements and reactive control with ReacSight," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    14. Richard J. Lindsay & Philippa J. Holder & Mark Hewlett & Ivana Gudelj, 2024. "Experimental evolution of yeast shows that public-goods upregulation can evolve despite challenges from exploitative non-producers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Peña, Jorge & Nöldeke, Georg & Lehmann, Laurent, 2014. "Relatedness and synergies of kind and scale in the evolution of helping," Working papers 2014/09, Faculty of Business and Economics - University of Basel.
    16. Brian McLoone & Wai-Tong Louis Fan & Adam Pham & Rory Smead & Laurence Loewe, 2018. "Stochasticity, Selection, and the Evolution of Cooperation in a Two-Level Moran Model of the Snowdrift Game," Complexity, Hindawi, vol. 2018, pages 1-14, February.
    17. Helena R. Ma & Helen Z. Xu & Kyeri Kim & Deverick J. Anderson & Lingchong You, 2024. "Private benefit of β-lactamase dictates selection dynamics of combination antibiotic treatment," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. Robin Watson & Thomas J. H. Morgan & Rachel L. Kendal & Julie Van de Vyver & Jeremy Kendal, 2021. "Social Learning Strategies and Cooperative Behaviour: Evidence of Payoff Bias, but Not Prestige or Conformity, in a Social Dilemma Game," Games, MDPI, vol. 12(4), pages 1-26, November.
    19. Alicia Sanchez-Gorostiaga & Djordje Bajić & Melisa L Osborne & Juan F Poyatos & Alvaro Sanchez, 2019. "High-order interactions distort the functional landscape of microbial consortia," PLOS Biology, Public Library of Science, vol. 17(12), pages 1-34, December.
    20. Olga A Nev & Richard J Lindsay & Alys Jepson & Lisa Butt & Robert E Beardmore & Ivana Gudelj, 2021. "Predicting microbial growth dynamics in response to nutrient availability," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-20, March.

    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:15:y:2024:i:1:d:10.1038_s41467-023-44379-5. 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.