Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer
The primary limitation to the practicability of electroactive microorganisms in bioelectrochemical systems lies in their low extracellular electron transfer (EET) efficiency. The proton motive force (PMF) represents the electrochemical gradient of protons generated by electron transport and proton p...
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KeAi Communications Co., Ltd.
2025-06-01
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| Series: | Synthetic and Systems Biotechnology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2405805X25000018 |
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| author | Wenqi Ding Tong Lin Yun Yang Wen-Wei Li Shaoan Cheng Hao Song |
| author_facet | Wenqi Ding Tong Lin Yun Yang Wen-Wei Li Shaoan Cheng Hao Song |
| author_sort | Wenqi Ding |
| collection | DOAJ |
| description | The primary limitation to the practicability of electroactive microorganisms in bioelectrochemical systems lies in their low extracellular electron transfer (EET) efficiency. The proton motive force (PMF) represents the electrochemical gradient of protons generated by electron transport and proton pumping across the cytoplasmic membrane, serving as a crucial energy transfer pathway in bacterial membranes. Nevertheless, the impact of PMF on the EET efficiency remains ambiguous, while the microbial rhodopsin offers a simple and efficient avenue for non-photosynthetic cells to harness PMF. Here, we studied the function of three microbial rhodopsins (Arch, Mac, and cR-1) in facilitating EET via their heterologous expression in S. oneidensis, a model electroactive microorganism. Among these, the recombinant strain expressing rhodopsin cR-1 exhibited the highest output power density of 0.87 W/m2, 3.49-fold increase over the wild-type S. oneidensis MR-1. Our further transcriptomics analyses of the energy and materials metabolism of strain cR-1 showed that the underlying mechanism of enhanced EET efficiency was resulted from heterologous expression of the light-driven proton pump. The results suggested that strain cR-1 effectively expels protons to generate additional PMF and provide extra ATP supply to the cells, which facilitated lactate uptake and utilization, thus enhancing electrons generation in cells. This augmented intracellular electron pool capacity ultimately resulted in enhancement of EET rate and power generation efficiency of the recombinant S. oneidensis. |
| format | Article |
| id | doaj-art-c764e2e1e3ea4a73a49e6610ede4a2c4 |
| institution | Kabale University |
| issn | 2405-805X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | KeAi Communications Co., Ltd. |
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| series | Synthetic and Systems Biotechnology |
| spelling | doaj-art-c764e2e1e3ea4a73a49e6610ede4a2c42025-01-19T06:26:16ZengKeAi Communications Co., Ltd.Synthetic and Systems Biotechnology2405-805X2025-06-01102410420Proton motive force generated by microbial rhodopsin promotes extracellular electron transferWenqi Ding0Tong Lin1Yun Yang2Wen-Wei Li3Shaoan Cheng4Hao Song5Frontiers Science Centre for Synthetic Biology (Ministry of Education), And Key Laboratory of Systems Bioengineering, School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, ChinaCollege of Life Science, Langfang Normal University, Langfang, Hebei, 065000, ChinaBeijing Advanced Innovation Centre for Biomedical Engineering, Key Laboratory for Biomechanics and Mechanobiology of Ministry of Education, School of Engineering Medicine, Beihang University, Beijing, 100083, ChinaChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science & Technology of China, Hefei, 230026, ChinaState Key Laboratory of Clean Energy, Department of Energy Engineering, Zhejiang University, Hangzhou, 310027, ChinaFrontiers Science Centre for Synthetic Biology (Ministry of Education), And Key Laboratory of Systems Bioengineering, School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, China; Haihe Laboratory of Sustainable Chemical Transformations, Tianjin, 300192, China; Corresponding author. Frontiers Science Centre for Synthetic Biology (Ministry of Education), And Key Laboratory of Systems Bioengineering, School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, China.The primary limitation to the practicability of electroactive microorganisms in bioelectrochemical systems lies in their low extracellular electron transfer (EET) efficiency. The proton motive force (PMF) represents the electrochemical gradient of protons generated by electron transport and proton pumping across the cytoplasmic membrane, serving as a crucial energy transfer pathway in bacterial membranes. Nevertheless, the impact of PMF on the EET efficiency remains ambiguous, while the microbial rhodopsin offers a simple and efficient avenue for non-photosynthetic cells to harness PMF. Here, we studied the function of three microbial rhodopsins (Arch, Mac, and cR-1) in facilitating EET via their heterologous expression in S. oneidensis, a model electroactive microorganism. Among these, the recombinant strain expressing rhodopsin cR-1 exhibited the highest output power density of 0.87 W/m2, 3.49-fold increase over the wild-type S. oneidensis MR-1. Our further transcriptomics analyses of the energy and materials metabolism of strain cR-1 showed that the underlying mechanism of enhanced EET efficiency was resulted from heterologous expression of the light-driven proton pump. The results suggested that strain cR-1 effectively expels protons to generate additional PMF and provide extra ATP supply to the cells, which facilitated lactate uptake and utilization, thus enhancing electrons generation in cells. This augmented intracellular electron pool capacity ultimately resulted in enhancement of EET rate and power generation efficiency of the recombinant S. oneidensis.http://www.sciencedirect.com/science/article/pii/S2405805X25000018Extracellular electron transferMicrobial rhodopsinProton motive forceShewanella oneidensis MR-1 |
| spellingShingle | Wenqi Ding Tong Lin Yun Yang Wen-Wei Li Shaoan Cheng Hao Song Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer Synthetic and Systems Biotechnology Extracellular electron transfer Microbial rhodopsin Proton motive force Shewanella oneidensis MR-1 |
| title | Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| title_full | Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| title_fullStr | Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| title_full_unstemmed | Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| title_short | Proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| title_sort | proton motive force generated by microbial rhodopsin promotes extracellular electron transfer |
| topic | Extracellular electron transfer Microbial rhodopsin Proton motive force Shewanella oneidensis MR-1 |
| url | http://www.sciencedirect.com/science/article/pii/S2405805X25000018 |
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