Oxygen microenvironments in Escherichia coli biofilm nutrient transport channels: insights from complementary sensing approaches.

IF 2.6 4区 生物学 Q3 MICROBIOLOGY
Beatrice Bottura, Gail McConnell, Lindsey C Florek, Marina K Smiley, Ross Martin, Shannan Foylan, Ash Eana, Hannah T Dayton, Kelly N Eckartt, Alexa M Price-Whelan, Paul A Hoskisson, Gwyn W Gould, Lars E P Dietrich, Liam M Rooney
{"title":"Oxygen microenvironments in <i>Escherichia coli</i> biofilm nutrient transport channels: insights from complementary sensing approaches.","authors":"Beatrice Bottura, Gail McConnell, Lindsey C Florek, Marina K Smiley, Ross Martin, Shannan Foylan, Ash Eana, Hannah T Dayton, Kelly N Eckartt, Alexa M Price-Whelan, Paul A Hoskisson, Gwyn W Gould, Lars E P Dietrich, Liam M Rooney","doi":"10.1099/mic.0.001543","DOIUrl":null,"url":null,"abstract":"<p><p>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 <i>Escherichia coli</i> 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 <i>E. coli</i> 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.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"171 5","pages":""},"PeriodicalIF":2.6000,"publicationDate":"2025-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12056250/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiology-Sgm","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1099/mic.0.001543","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

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 Escherichia coli 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 E. coli 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.

大肠杆菌生物膜营养运输通道中的氧微环境:来自互补传感方法的见解。
生物膜中化学梯度和不同微环境的出现对微生物群落的分层、成熟和整体功能至关重要。这些梯度已经在整个生物膜中得到了很好的表征,但最近发现的大肠杆菌生物膜中营养转运通道的微环境仍未被探索。本研究采用三种不同的氧传感方法,对大肠杆菌大菌落生物膜形成的整个生物膜运输通道网络中的氧梯度和微环境进行了强有力的定量概述。氧纳米传感与激光共聚焦扫描显微镜相结合,证实了氧浓度沿生物膜运输通道的长度变化。电化学传感提供了运输通道中氧谱的精确量化,显示出与相邻细胞相似的缺氧谱。缺氧生物传感证实了这些方法,提供了整个生物质氧气利用的概述。运输通道维持氧梯度的发现与以前的文献相矛盾,以前的文献认为通道沿着生物膜的顶端表面完全向环境开放。我们通过生物膜薄片的正交可视化显示活跃生长的细胞薄层,为通道微环境的维持提供了一个潜在的机制。对生物膜运输通道中氧环境的全面概述为未来的研究提供了基础,旨在利用这些新兴结构进行新的生物修复方法。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Microbiology-Sgm
Microbiology-Sgm 生物-微生物学
CiteScore
4.60
自引率
7.10%
发文量
132
审稿时长
3.0 months
期刊介绍: We publish high-quality original research on bacteria, fungi, protists, archaea, algae, parasites and other microscopic life forms. Topics include but are not limited to: Antimicrobials and antimicrobial resistance Bacteriology and parasitology Biochemistry and biophysics Biofilms and biological systems Biotechnology and bioremediation Cell biology and signalling Chemical biology Cross-disciplinary work Ecology and environmental microbiology Food microbiology Genetics Host–microbe interactions Microbial methods and techniques Microscopy and imaging Omics, including genomics, proteomics and metabolomics Physiology and metabolism Systems biology and synthetic biology The microbiome.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信