Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms
ABSTRACT Conductive nanowires are thought to contribute to long-range electron transfer (LET) in Geobacter sulfurreducens anode biofilms. Three types of nanowires have been identified: pili, OmcS, and OmcZ. Previous studies highlighted their conductive function in anode biofilms, yet a structural fu...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.03822-21 |
| _version_ | 1819280580980768768 |
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| author | Yin Ye Xing Liu Kenneth H. Nealson Christopher Rensing Shuping Qin Shungui Zhou |
| author_facet | Yin Ye Xing Liu Kenneth H. Nealson Christopher Rensing Shuping Qin Shungui Zhou |
| author_sort | Yin Ye |
| collection | DOAJ |
| description | ABSTRACT Conductive nanowires are thought to contribute to long-range electron transfer (LET) in Geobacter sulfurreducens anode biofilms. Three types of nanowires have been identified: pili, OmcS, and OmcZ. Previous studies highlighted their conductive function in anode biofilms, yet a structural function also has to be considered. We present here a comprehensive analysis of the function of nanowires in LET by inhibiting the expression of each nanowire. Meanwhile, flagella with poor conductivity were expressed to recover the structural function but not the conductive function of nanowires in the corresponding nanowire mutant strain. The results demonstrated that pili played a structural but not a conductive function in supporting biofilm formation. In contrast, the OmcS nanowire played a conductive but not a structural function in facilitating electron transfer in the biofilm. The OmcZ nanowire played both a structural and a conductive function to contribute to current generation. Expression of the poorly conductive flagellum was shown to enhance biofilm formation, subsequently increasing current generation. These data support a model in which multiheme cytochromes facilitate long-distance electron transfer in G. sulfurreducens biofilms. Our findings also suggest that the formation of a thicker biofilm, which contributed to a higher current generation by G. sulfurreducens, was confined by the biofilm formation deficiency, and this has applications in microbial electrochemical systems. IMPORTANCE The low power generation of microbial fuel cells limits their utility. Many factors can affect power generation, including inefficient electron transfer in the anode biofilm. Thus, understanding the mechanism(s) of electron transfer provides a pathway for increasing the power density of microbial fuel cells. Geobacter sulfurreducens was shown to form a thick biofilm on the anode. Cells far away from the anode reduce the anode through long-range electron transfer. Based on their conductive properties, three types of nanowires have been hypothesized to directly facilitate long-range electron transfer: pili, OmcS, and OmcZ nanowires. However, their structural contributions to electron transfer in anode biofilm have not been elucidated. Based on studies of mutants lacking one or more of these facilitators, our results support a cytochrome-mediated electron transfer process in Geobacter biofilms and highlight the structural contribution of nanowires in anode biofilm formation, which contributes to biofilm formation and current generation, thereby providing a strategy to increase current generation. |
| first_indexed | 2024-12-24T00:46:04Z |
| format | Article |
| id | doaj.art-e9062a8c802f4804af77a12a23aafdea |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-24T00:46:04Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
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| series | mBio |
| spelling | doaj.art-e9062a8c802f4804af77a12a23aafdea2022-12-21T17:23:49ZengAmerican Society for MicrobiologymBio2150-75112022-02-0113110.1128/mbio.03822-21Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive BiofilmsYin Ye0Xing Liu1Kenneth H. Nealson2Christopher Rensing3Shuping Qin4Shungui Zhou5Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, ChinaDepartment of Earth Science, University of Southern California, Los Angeles, California, USA, United StatesFujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, ChinaABSTRACT Conductive nanowires are thought to contribute to long-range electron transfer (LET) in Geobacter sulfurreducens anode biofilms. Three types of nanowires have been identified: pili, OmcS, and OmcZ. Previous studies highlighted their conductive function in anode biofilms, yet a structural function also has to be considered. We present here a comprehensive analysis of the function of nanowires in LET by inhibiting the expression of each nanowire. Meanwhile, flagella with poor conductivity were expressed to recover the structural function but not the conductive function of nanowires in the corresponding nanowire mutant strain. The results demonstrated that pili played a structural but not a conductive function in supporting biofilm formation. In contrast, the OmcS nanowire played a conductive but not a structural function in facilitating electron transfer in the biofilm. The OmcZ nanowire played both a structural and a conductive function to contribute to current generation. Expression of the poorly conductive flagellum was shown to enhance biofilm formation, subsequently increasing current generation. These data support a model in which multiheme cytochromes facilitate long-distance electron transfer in G. sulfurreducens biofilms. Our findings also suggest that the formation of a thicker biofilm, which contributed to a higher current generation by G. sulfurreducens, was confined by the biofilm formation deficiency, and this has applications in microbial electrochemical systems. IMPORTANCE The low power generation of microbial fuel cells limits their utility. Many factors can affect power generation, including inefficient electron transfer in the anode biofilm. Thus, understanding the mechanism(s) of electron transfer provides a pathway for increasing the power density of microbial fuel cells. Geobacter sulfurreducens was shown to form a thick biofilm on the anode. Cells far away from the anode reduce the anode through long-range electron transfer. Based on their conductive properties, three types of nanowires have been hypothesized to directly facilitate long-range electron transfer: pili, OmcS, and OmcZ nanowires. However, their structural contributions to electron transfer in anode biofilm have not been elucidated. Based on studies of mutants lacking one or more of these facilitators, our results support a cytochrome-mediated electron transfer process in Geobacter biofilms and highlight the structural contribution of nanowires in anode biofilm formation, which contributes to biofilm formation and current generation, thereby providing a strategy to increase current generation.https://journals.asm.org/doi/10.1128/mbio.03822-21Geobactercytochromeselectroactive biofilmnanowirepili |
| spellingShingle | Yin Ye Xing Liu Kenneth H. Nealson Christopher Rensing Shuping Qin Shungui Zhou Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms mBio Geobacter cytochromes electroactive biofilm nanowire pili |
| title | Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms |
| title_full | Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms |
| title_fullStr | Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms |
| title_full_unstemmed | Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms |
| title_short | Dissecting the Structural and Conductive Functions of Nanowires in Geobacter sulfurreducens Electroactive Biofilms |
| title_sort | dissecting the structural and conductive functions of nanowires in geobacter sulfurreducens electroactive biofilms |
| topic | Geobacter cytochromes electroactive biofilm nanowire pili |
| url | https://journals.asm.org/doi/10.1128/mbio.03822-21 |
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