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Spatial structure, chemotaxis and quorum sensing shape bacterial biomass accumulation in complex porous media

Author

Listed:
  • David Scheidweiler

    (University of Lausanne)

  • Ankur Deep Bordoloi

    (University of Lausanne)

  • Wenqiao Jiao

    (University of Lausanne)

  • Vladimir Sentchilo

    (University of Lausanne)

  • Monica Bollani

    (IFN-CNR, L-NESS)

  • Audam Chhun

    (University of Lausanne)

  • Philipp Engel

    (University of Lausanne)

  • Pietro de Anna

    (University of Lausanne)

Abstract

Biological tissues, sediments, or engineered systems are spatially structured media with a tortuous and porous structure that host the flow of fluids. Such complex environments can influence the spatial and temporal colonization patterns of bacteria by controlling the transport of individual bacterial cells, the availability of resources, and the distribution of chemical signals for communication. Yet, due to the multi-scale structure of these complex systems, it is hard to assess how different biotic and abiotic properties work together to control the accumulation of bacterial biomass. Here, we explore how flow-mediated interactions allow the gut commensal Escherichia coli to colonize a porous structure that is composed of heterogenous dead-end pores (DEPs) and connecting percolating channels, i.e. transmitting pores (TPs), mimicking the structured surface of mammalian guts. We find that in presence of flow, gradients of the quorum sensing (QS) signaling molecule autoinducer-2 (AI-2) promote E. coli chemotactic accumulation in the DEPs. In this crowded environment, the combination of growth and cell-to-cell collision favors the development of suspended bacterial aggregates. This results in hot-spots of resource consumption, which, upon resource limitation, triggers the mechanical evasion of biomass from nutrients and oxygen depleted DEPs. Our findings demonstrate that microscale medium structure and complex flow coupled with bacterial quorum sensing and chemotaxis control the heterogenous accumulation of bacterial biomass in a spatially structured environment, such as villi and crypts in the gut or in tortuous pores within soil and filters.

Suggested Citation

  • David Scheidweiler & Ankur Deep Bordoloi & Wenqiao Jiao & Vladimir Sentchilo & Monica Bollani & Audam Chhun & Philipp Engel & Pietro de Anna, 2024. "Spatial structure, chemotaxis and quorum sensing shape bacterial biomass accumulation in complex porous media," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44267-y
    DOI: 10.1038/s41467-023-44267-y
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    References listed on IDEAS

    as
    1. Sara Hooshangi & William E Bentley, 2011. "LsrR Quorum Sensing “Switch” Is Revealed by a Bottom-Up Approach," PLOS Computational Biology, Public Library of Science, vol. 7(9), pages 1-11, September.
    2. Leanid Laganenka & Remy Colin & Victor Sourjik, 2016. "Correction: Corrigendum: Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli," Nature Communications, Nature, vol. 7(1), pages 1-1, December.
    3. Leanid Laganenka & Remy Colin & Victor Sourjik, 2016. "Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    4. Ankur Deep Bordoloi & David Scheidweiler & Marco Dentz & Mohammed Bouabdellaoui & Marco Abbarchi & Pietro de Anna, 2022. "Structure induced laminar vortices control anomalous dispersion in porous media," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Gerardo Cárcamo-Oyarce & Putthapoom Lumjiaktase & Rolf Kümmerli & Leo Eberl, 2015. "Quorum sensing triggers the stochastic escape of individual cells from Pseudomonas putida biofilms," Nature Communications, Nature, vol. 6(1), pages 1-9, May.
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