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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
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    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. 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.
    3. 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.
    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.
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