Multichannel Bioelectronic Sensing: Binary Encoding of Environmental Contaminants
Authors: Zhang Xu , Charrier Marimikel , Ajo-Franklin Caroline M 
Published: December 2024

Environmental water contamination from natural and synthetic chemicals is a pressing global issue. Addressing this requires the development of portable, selective, and accurate sensors. Biosensors, particularly whole-cell bioelectronic sensors, are promising due to their ability to convert chemical signals into electrical signals via extracellular electron transfer (EET) pathways. However, these sensors typically employ a single electron transfer pathway as an electrochemical channel, limiting them to the detection of a single analyte (Atkinson et al. 2022).

To expand the information content, we have developed a multichannel sensor where different chemicals regulate distinct EET pathways within a single Escherichia coli cell. One channel utilizes the flavin synthesis pathway from Bacillus subtilis (Yang Yun et al. 2017) and is controlled by a cadmium-responsive promoter (Hui et al. 2021). Another channel, the Mtr pathway from Shewanella oneidensis (Ross Daniel E. et al. 2007), is controlled by an arsenite-responsive promoter (Chen et al. 2019) through activation of cytochrome CymA expression. We exploit the differing redox potentials of these two EET pathways (Kracke, Vassilev, and Krömer 2015) to develop a redox-potential-dependent algorithm that efficiently converts analog current curves into 2-bit binary outputs. This enables our bioelectronic sensor to detect and differentiate heavy metals at EPA limits. When deployed in complex environmental water samples with lower electroactivities, our sensor effectively and accurately encodes 2-bit binary signals across various analyte conditions. Thus, our multichannel bioelectronic sensor advances the field through simultaneous detection of different chemicals by a single cell, significantly expanding information transmission from EET and helping to safeguard human and environmental health.

References:

Atkinson, Joshua T., Lin Su, Xu Zhang, George N. Bennett, Jonathan J. Silberg, and Caroline M. Ajo-Franklin. 2022. “Real-Time Bioelectronic Sensing of Environmental Contaminants.” Nature 611(7936):548–53. doi: 10.1038/s41586-022-05356-y.

Chen, Sheng-Yan, Wenping Wei, Bin-Cheng Yin, Yanbin Tong, Jianjiang Lu, and Bang-Ce Ye. 2019. “Development of a Highly Sensitive Whole-Cell Biosensor for Arsenite Detection through Engineered Promoter Modifications.” ACS Synthetic Biology 8(10):2295–2302. doi: 10.1021/acssynbio.9b00093.

Hui, Chang-ye, Yan Guo, Jian Wu, Lisa Liu, Xue-qin Yang, Xiang Guo, Ying Xie, and Juan Yi. 2021. “Detection of Bioavailable Cadmium by Double-Color Fluorescence Based on a Dual-Sensing Bioreporter System.” Frontiers in Microbiology 12.

Kracke, Frauke, Igor Vassilev, and Jens O. Krömer. 2015. “Microbial Electron Transport and Energy Conservation – the Foundation for Optimizing Bioelectrochemical Systems.” Frontiers in Microbiology 6.

Ross Daniel E., Ruebush Shane S., Brantley Susan L., Hartshorne Robert S., Clarke Thomas A., Richardson David J., and Tien Ming. 2007. “Characterization of Protein-Protein Interactions Involved in Iron Reduction by Shewanella Oneidensis MR-1.” Applied and Environmental Microbiology 73(18):5797–5808. doi: 10.1128/AEM.00146-07.

Yang Yun, Wu Yichao, Hu Yidan, Wang Hua, Guo Lin, Fredrickson James K., and Cao Bin. 2017. “Harnessing the Periplasm of Bacterial Cells To Develop Biocatalysts for the Biosynthesis of Highly Pure Chemicals.” Applied and Environmental Microbiology 84(1):e01693-17. doi: 10.1128/AEM.01693-17.

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