IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51940-3.html
   My bibliography  Save this article

Spatially structured exchange of metabolites enhances bacterial survival and resilience in biofilms

Author

Listed:
  • Yuzhen Zhang

    (Chinese Academy of Sciences)

  • Yukmi Cai

    (Chinese Academy of Sciences)

  • Bing Zhang

    (Yanshan University)

  • Yi-Heng P. Job Zhang

    (Chinese Academy of Sciences)

Abstract

Biofilm formation enhances bacterial survival and antibiotic tolerance, but the underlying mechanisms are incompletely understood. Here, we show that biofilm growth is accompanied by a reduction in bacterial energy metabolism and membrane potential, together with metabolic exchanges between the inner and outer regions in biofilms. More specifically, nutrient-starved cells in the interior supply amino acids to cells in the periphery, while peripheral cells experience a decrease in membrane potential and provide fatty acids to interior cells. Fatty acids facilitate the repair of starvation-induced membrane damage in inner cells and enhance their survival in the presence of antibiotics. Thus, metabolic exchanges between inner and outer cells contribute to survival of the nutrient-starved inner cells and contribute to antibiotic tolerance within the biofilm.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51940-3
    DOI: 10.1038/s41467-024-51940-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51940-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51940-3?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. Yichao Wu & Chengxia Fu & Caroline L. Peacock & Søren J. Sørensen & Marc A. Redmile-Gordon & Ke-Qing Xiao & Chunhui Gao & Jun Liu & Qiaoyun Huang & Zixue Li & Peiyi Song & Yongguan Zhu & Jizhong Zhou , 2023. "Cooperative microbial interactions drive spatial segregation in porous environments," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Felix Wong & Jonathan M. Stokes & Bernardo Cervantes & Sider Penkov & Jens Friedrichs & Lars D. Renner & James J. Collins, 2021. "Cytoplasmic condensation induced by membrane damage is associated with antibiotic lethality," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Christopher A. Werley & Stefano Boccardo & Alessandra Rigamonti & Emil M. Hansson & Adam E. Cohen, 2020. "Multiplexed Optical Sensors in Arrayed Islands of Cells for multimodal recordings of cellular physiology," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    4. 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.
    5. Viridiana Olin-Sandoval & Jason Shu Lim Yu & Leonor Miller-Fleming & Mohammad Tauqeer Alam & Stephan Kamrad & Clara Correia-Melo & Robert Haas & Joanna Segal & David Alejandro Peña Navarro & Lucia Her, 2019. "Lysine harvesting is an antioxidant strategy and triggers underground polyamine metabolism," Nature, Nature, vol. 572(7768), pages 249-253, August.
    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. John C. Boik, 2016. "Optimality of Social Choice Systems: Complexity, Wisdom, and Wellbeing Centrality," Working Paper 0005, Principled Societies Project, revised Mar 2017.
    2. Yan, Xuejun & Lee, Hyung-Sool & Li, Nan & Wang, Xin, 2020. "The micro-niche of exoelectrogens influences bioelectricity generation in bioelectrochemical systems," Renewable and Sustainable Energy Reviews, Elsevier, vol. 134(C).
    3. Giovanni Scarinci & Jan-Luca Ariens & Georgia Angelidou & Sebastian Schmidt & Timo Glatter & Nicole Paczia & Victor Sourjik, 2024. "Enhanced metabolic entanglement emerges during the evolution of an interkingdom microbial community," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Yifan Yang & Omer Karin & Avi Mayo & Xiaohu Song & Peipei Chen & Ana L. Santos & Ariel B. Lindner & Uri Alon, 2023. "Damage dynamics and the role of chance in the timing of E. coli cell death," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Vincent Charron-Lamoureux & Lounès Haroune & Maude Pomerleau & Léo Hall & Frédéric Orban & Julie Leroux & Adrien Rizzi & Jean-Sébastien Bourassa & Nicolas Fontaine & Élodie V. d’Astous & Philippe Daup, 2023. "Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Jung Hun Park & Gábor Holló & Yolanda Schaerli, 2024. "From resonance to chaos by modulating spatiotemporal patterns through a synthetic optogenetic oscillator," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. 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.
    8. Xiaoling Zhai & Joseph W Larkin & Kaito Kikuchi & Samuel E Redford & Ushasi Roy & Gürol M Süel & Andrew Mugler, 2019. "Statistics of correlated percolation in a bacterial community," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-19, December.
    9. Ritu Gupta & Swagata Adhikary & Nidhi Dalpatraj & Sunil Laxman, 2024. "An economic demand-based framework for prioritization strategies in response to transient amino acid limitations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    10. Fondi, Marco & Di Patti, Francesca, 2019. "A synthetic ecosystem for the multi-level modelling of heterotroph-phototroph metabolic interactions," Ecological Modelling, Elsevier, vol. 399(C), pages 13-22.

    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_s41467-024-51940-3. 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.