Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium
ABSTRACT Understanding the extracellular electron transfer mechanisms of electroactive bacteria could help determine their potential in microbial fuel cells (MFCs) and their microbial syntrophy with redox-active minerals in natural environments. However, the mechanisms of extracellular electron tran...
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American Society for Microbiology
2025-01-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01226-24 |
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| author | Liyuan Hou Rebecca Cortez Michael Hagerman Zhiqiang Hu Erica L.-W. Majumder |
| author_facet | Liyuan Hou Rebecca Cortez Michael Hagerman Zhiqiang Hu Erica L.-W. Majumder |
| author_sort | Liyuan Hou |
| collection | DOAJ |
| description | ABSTRACT Understanding the extracellular electron transfer mechanisms of electroactive bacteria could help determine their potential in microbial fuel cells (MFCs) and their microbial syntrophy with redox-active minerals in natural environments. However, the mechanisms of extracellular electron transfer to electrodes by sulfate-reducing bacteria (SRB) remain underexplored. Here, we utilized double-chamber MFCs with carbon cloth electrodes to investigate the extracellular electron transfer mechanisms of Desulfovibrio vulgaris Hildenborough (DvH), a model SRB, under varying lactate and sulfate concentrations using different DvH mutants. Our MFC setup indicated that DvH can harvest electrons from lactate at the anode and transfer them to cathode, where DvH could further utilize these electrons. Patterns in current production compared with variations of electron donor/acceptor ratios in the anode and cathode suggested that attachment of DvH to the electrode and biofilm density were critical for effective electricity generation. Electron microscopy analysis of DvH biofilms indicated DvH utilized filaments that resemble pili to attach to electrodes and facilitate extracellular electron transfer from cell to cell and to the electrode. Proteomics profiling indicated that DvH adapted to electroactive respiration by presenting more pili- and flagellar-related proteins. The mutant with a deletion of the major pilus-producing gene yielded less voltage and far less attachment to both anodic and catholic electrodes, suggesting the importance of pili in extracellular electron transfer. The mutant with a deficiency in biofilm formation, however, did not eliminate current production indicating the existence of indirect extracellular electron transfer. Untargeted metabolomics profiling showed flavin-based metabolites, potential electron shuttles.IMPORTANCEWe explored the application of Desulfovibrio vulgaris Hildenborough in microbial fuel cells (MFCs) and investigated its potential extracellular electron transfer (EET) mechanism. We also conducted untargeted proteomics and metabolomics profiling, offering insights into how DvH adapts metabolically to different electron donors and acceptors. An understanding of the EET mechanism and metabolic flexibility of DvH holds promise for future uses including bioremediation or enhancing efficacy in MFCs for wastewater treatment applications. |
| format | Article |
| id | doaj-art-91323ff74d7440f68e3ca6d985efe868 |
| institution | Kabale University |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-91323ff74d7440f68e3ca6d985efe8682025-01-07T14:05:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.01226-24Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacteriumLiyuan Hou0Rebecca Cortez1Michael Hagerman2Zhiqiang Hu3Erica L.-W. Majumder4Department of Civil and Environmental Engineering, Utah State University, Logan, Utah, USADepartment of Mechanical Engineering, Union College, Schenectady, New York, USADepartment of Chemistry, Union College, Schenectady, New York, USADepartment of Civil and Environmental Engineering, University of Missouri, Columbia, Missouri, USADepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USAABSTRACT Understanding the extracellular electron transfer mechanisms of electroactive bacteria could help determine their potential in microbial fuel cells (MFCs) and their microbial syntrophy with redox-active minerals in natural environments. However, the mechanisms of extracellular electron transfer to electrodes by sulfate-reducing bacteria (SRB) remain underexplored. Here, we utilized double-chamber MFCs with carbon cloth electrodes to investigate the extracellular electron transfer mechanisms of Desulfovibrio vulgaris Hildenborough (DvH), a model SRB, under varying lactate and sulfate concentrations using different DvH mutants. Our MFC setup indicated that DvH can harvest electrons from lactate at the anode and transfer them to cathode, where DvH could further utilize these electrons. Patterns in current production compared with variations of electron donor/acceptor ratios in the anode and cathode suggested that attachment of DvH to the electrode and biofilm density were critical for effective electricity generation. Electron microscopy analysis of DvH biofilms indicated DvH utilized filaments that resemble pili to attach to electrodes and facilitate extracellular electron transfer from cell to cell and to the electrode. Proteomics profiling indicated that DvH adapted to electroactive respiration by presenting more pili- and flagellar-related proteins. The mutant with a deletion of the major pilus-producing gene yielded less voltage and far less attachment to both anodic and catholic electrodes, suggesting the importance of pili in extracellular electron transfer. The mutant with a deficiency in biofilm formation, however, did not eliminate current production indicating the existence of indirect extracellular electron transfer. Untargeted metabolomics profiling showed flavin-based metabolites, potential electron shuttles.IMPORTANCEWe explored the application of Desulfovibrio vulgaris Hildenborough in microbial fuel cells (MFCs) and investigated its potential extracellular electron transfer (EET) mechanism. We also conducted untargeted proteomics and metabolomics profiling, offering insights into how DvH adapts metabolically to different electron donors and acceptors. An understanding of the EET mechanism and metabolic flexibility of DvH holds promise for future uses including bioremediation or enhancing efficacy in MFCs for wastewater treatment applications.https://journals.asm.org/doi/10.1128/spectrum.01226-24electron transfer mechanismsDesulfovibrio vulgaris Hildenboroughelectrically conductive pilielectroactive respirationmicrobial fuel cells |
| spellingShingle | Liyuan Hou Rebecca Cortez Michael Hagerman Zhiqiang Hu Erica L.-W. Majumder Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium Microbiology Spectrum electron transfer mechanisms Desulfovibrio vulgaris Hildenborough electrically conductive pili electroactive respiration microbial fuel cells |
| title | Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| title_full | Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| title_fullStr | Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| title_full_unstemmed | Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| title_short | Co-occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| title_sort | co occurrence of direct and indirect extracellular electron transfer mechanisms during electroactive respiration in a dissimilatory sulfate reducing bacterium |
| topic | electron transfer mechanisms Desulfovibrio vulgaris Hildenborough electrically conductive pili electroactive respiration microbial fuel cells |
| url | https://journals.asm.org/doi/10.1128/spectrum.01226-24 |
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