Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways
Lipophilic electron shuttles (ESs), such as phenazine and phenoxazine, can penetrate the outer membrane and enter the periplasmic space, mediating extracellular electron transfer reactions. This study investigates how lipophilic ESs (resazurin, a phenoxazine) regulate carbon metabolic pathways in bi...
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| Format: | Article |
| Language: | English |
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Wiley-VCH
2025-07-01
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| Series: | ChemElectroChem |
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| Online Access: | https://doi.org/10.1002/celc.202500092 |
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| author | Siyu Tan Xiao Zhu Xinxin Wang Huangsheng Su Zongqiang Zhu Xiaobo Luo John R. Reinfelder Yundang Wu Fangbai Li |
| author_facet | Siyu Tan Xiao Zhu Xinxin Wang Huangsheng Su Zongqiang Zhu Xiaobo Luo John R. Reinfelder Yundang Wu Fangbai Li |
| author_sort | Siyu Tan |
| collection | DOAJ |
| description | Lipophilic electron shuttles (ESs), such as phenazine and phenoxazine, can penetrate the outer membrane and enter the periplasmic space, mediating extracellular electron transfer reactions. This study investigates how lipophilic ESs (resazurin, a phenoxazine) regulate carbon metabolic pathways in bioelectrochemical systems using Shewanella oneidensis MR‐1 as a model organism. Through the analysis of acetate yield, CO2 production, coulombic efficiency, and other parameters, it is found that resazurin increases coulombic efficiency (26% vs 17% for anthraquinone‐2,6‐disulfonic acid [AQDS]) and reduces acetate yield (82% vs 90% for AQDS) while slightly increasing CO2 production (13.1% vs 11.8% for AQDS), indicating a shift in carbon metabolism. Transcriptome analysis reveals significant upregulation of genes involved in the NADH‐dependent metabolic pathway (e.g., nuoHIJKLMN) and ATP synthesis (atpABDEFGH) under resazurin conditions. Mutant strains lacking key genes in oxidative phosphorylation (Δatp) or substrate‐level phosphorylation (Δack&pta) further confirm the regulatory role of lipophilic shuttles. The study proposes that lipophilic ESs penetrate the periplasm, altering the redox state of inner‐membrane quinones and activating the NADH‐dependent metabolic pathway via the Arc system. This mechanism enhances TCA cycle activity and overall lactate metabolic efficiency. The findings provide insights into microbial carbon metabolic regulation and offer strategies for optimizing bioelectrochemical systems for bioremediation. |
| format | Article |
| id | doaj-art-3d6426ffbfaa49748d787bbe64ea4812 |
| institution | Kabale University |
| issn | 2196-0216 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Wiley-VCH |
| record_format | Article |
| series | ChemElectroChem |
| spelling | doaj-art-3d6426ffbfaa49748d787bbe64ea48122025-08-20T03:50:21ZengWiley-VCHChemElectroChem2196-02162025-07-011214n/an/a10.1002/celc.202500092Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic PathwaysSiyu Tan0Xiao Zhu1Xinxin Wang2Huangsheng Su3Zongqiang Zhu4Xiaobo Luo5John R. Reinfelder6Yundang Wu7Fangbai Li8Guangxi Key Laboratory of Environmental Pollution Control Theory and Technology College of Environmental Science and Engineering Guilin University of Technology Guilin 541006 ChinaNational‐Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China Guangdong Key Laboratory of Integrated Agro‐environmental Pollution Control and Management Institute of Eco‐environmental and Soil Sciences, Guangdong Academy of Sciences Guangzhou 510650 ChinaNational‐Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China Guangdong Key Laboratory of Integrated Agro‐environmental Pollution Control and Management Institute of Eco‐environmental and Soil Sciences, Guangdong Academy of Sciences Guangzhou 510650 ChinaCollege of Materials and Energy South China Agricultural University Guangzhou 510642 ChinaGuangxi Key Laboratory of Environmental Pollution Control Theory and Technology College of Environmental Science and Engineering Guilin University of Technology Guilin 541006 ChinaInnovation Center of Nuclear Environmental Safety Technology Southwest University of Science and Technology Mianyang 621010 ChinaDepartment of Environmental Sciences Rutgers University New Brunswick NJ 08901 USANational‐Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China Guangdong Key Laboratory of Integrated Agro‐environmental Pollution Control and Management Institute of Eco‐environmental and Soil Sciences, Guangdong Academy of Sciences Guangzhou 510650 ChinaNational‐Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China Guangdong Key Laboratory of Integrated Agro‐environmental Pollution Control and Management Institute of Eco‐environmental and Soil Sciences, Guangdong Academy of Sciences Guangzhou 510650 ChinaLipophilic electron shuttles (ESs), such as phenazine and phenoxazine, can penetrate the outer membrane and enter the periplasmic space, mediating extracellular electron transfer reactions. This study investigates how lipophilic ESs (resazurin, a phenoxazine) regulate carbon metabolic pathways in bioelectrochemical systems using Shewanella oneidensis MR‐1 as a model organism. Through the analysis of acetate yield, CO2 production, coulombic efficiency, and other parameters, it is found that resazurin increases coulombic efficiency (26% vs 17% for anthraquinone‐2,6‐disulfonic acid [AQDS]) and reduces acetate yield (82% vs 90% for AQDS) while slightly increasing CO2 production (13.1% vs 11.8% for AQDS), indicating a shift in carbon metabolism. Transcriptome analysis reveals significant upregulation of genes involved in the NADH‐dependent metabolic pathway (e.g., nuoHIJKLMN) and ATP synthesis (atpABDEFGH) under resazurin conditions. Mutant strains lacking key genes in oxidative phosphorylation (Δatp) or substrate‐level phosphorylation (Δack&pta) further confirm the regulatory role of lipophilic shuttles. The study proposes that lipophilic ESs penetrate the periplasm, altering the redox state of inner‐membrane quinones and activating the NADH‐dependent metabolic pathway via the Arc system. This mechanism enhances TCA cycle activity and overall lactate metabolic efficiency. The findings provide insights into microbial carbon metabolic regulation and offer strategies for optimizing bioelectrochemical systems for bioremediation.https://doi.org/10.1002/celc.202500092carbon metabolismcoulombic efficiencylipophilic electron shuttleShewanella oneidensis MR‐1TCA cycle |
| spellingShingle | Siyu Tan Xiao Zhu Xinxin Wang Huangsheng Su Zongqiang Zhu Xiaobo Luo John R. Reinfelder Yundang Wu Fangbai Li Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways ChemElectroChem carbon metabolism coulombic efficiency lipophilic electron shuttle Shewanella oneidensis MR‐1 TCA cycle |
| title | Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways |
| title_full | Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways |
| title_fullStr | Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways |
| title_full_unstemmed | Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways |
| title_short | Lipophilic Resazurin in Bioelectrochemical Systems: Role in Regulating Carbon Metabolic Pathways |
| title_sort | lipophilic resazurin in bioelectrochemical systems role in regulating carbon metabolic pathways |
| topic | carbon metabolism coulombic efficiency lipophilic electron shuttle Shewanella oneidensis MR‐1 TCA cycle |
| url | https://doi.org/10.1002/celc.202500092 |
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