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Volume 171, Issue 5

Oxygen microenvironments in biofilm nutrient transport channels: insights from complementary sensing approaches Open Access

Abstract

Chemical gradients and the emergence of distinct microenvironments in biofilms are vital to the stratification, maturation and overall function of microbial communities. These gradients have been well characterized throughout the biofilm mass, but the microenvironment of recently discovered nutrient transporting channels in biofilms remains unexplored. This study employs three different oxygen sensing approaches to provide a robust quantitative overview of the oxygen gradients and microenvironments throughout the biofilm transport channel networks formed by macrocolony biofilms. Oxygen nanosensing combined with confocal laser scanning microscopy established that the oxygen concentration changes along the length of biofilm transport channels. Electrochemical sensing provided precise quantification of the oxygen profile in the transport channels, showing similar anoxic profiles compared with the adjacent cells. Anoxic biosensing corroborated these approaches, providing an overview of the oxygen utilization throughout the biomass. The discovery that transport channels maintain oxygen gradients contradicts the previous literature that channels are completely open to the environment along the apical surface of the biofilm. We provide a potential mechanism for the sustenance of channel microenvironments via orthogonal visualizations of biofilm thin sections showing thin layers of actively growing cells. This complete overview of the oxygen environment in biofilm transport channels primes future studies aiming to exploit these emergent structures for new bioremediation approaches.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biofilm physiology , microbial communities and redox sensing
Funding
This study was supported by the:
  • Scottish Universities Life Science Alliance
    • Principle Award Recipient: LiamM. Rooney
  • Leverhulme Trust
    • Principle Award Recipient: GailMcConnell
  • National Institutes of Health and the National Institute of Allergy and Infectious Diseases (Award R01AI103369)
    • Principle Award Recipient: LarsE.P. Dietrich
  • Royal Academy of Engineering (GB) (Award RCSRF2021\11\15)
    • Principle Award Recipient: PaulA. Hoskisson
  • Royal Microscopical Society
    • Principle Award Recipient: LiamM. Rooney
  • Microbiology Society (Award GA004356)
    • Principle Award Recipient: LiamM. Rooney
  • Biotechnology and Biological Sciences Research Council (Award BB/V019643/1)
    • Principle Award Recipient: GailMcConnell
  • Biotechnology and Biological Sciences Research Council (Award BB/T011602/1)
    • Principle Award Recipient: GailMcConnell
  • Biotechnology and Biological Sciences Research Council (Award BB/P02565X/1)
    • Principle Award Recipient: GailMcConnell
  • Medical Research Council (Award MR/K015583/1)
    • Principle Award Recipient: GailMcConnell
  • University of Strathclyde
    • Principle Award Recipient: LiamM. Rooney
© 2025 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2025-05-06
2025-05-17
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Oxygen microenvironments in Escherichia coli biofilm nutrient transport channels: insights from complementary sensing approaches
Microbiology 171, 001543 (2025); https://doi.org/10.1099/mic.0.001543
/content/journal/micro/10.1099/mic.0.001543
/content/journal/micro/10.1099/mic.0.001543
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