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Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires

Light-induced microbial electron transfer has potential for efficient production of value-added chemicals, biofuels and biodegradable materials owing to diversified metabolic pathways. However, most microbes lack photoactive proteins and require synthetic photosensitizers that suffer from photocorro...

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Autores principales: Neu, Jens, Shipps, Catharine C., Guberman-Pfeffer, Matthew J., Shen, Cong, Srikanth, Vishok, Spies, Jacob A., Kirchhofer, Nathan D., Yalcin, Sibel Ebru, Brudvig, Gary W., Batista, Victor S., Malvankar, Nikhil S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9452534/
https://www.ncbi.nlm.nih.gov/pubmed/36071037
http://dx.doi.org/10.1038/s41467-022-32659-5
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author Neu, Jens
Shipps, Catharine C.
Guberman-Pfeffer, Matthew J.
Shen, Cong
Srikanth, Vishok
Spies, Jacob A.
Kirchhofer, Nathan D.
Yalcin, Sibel Ebru
Brudvig, Gary W.
Batista, Victor S.
Malvankar, Nikhil S.
author_facet Neu, Jens
Shipps, Catharine C.
Guberman-Pfeffer, Matthew J.
Shen, Cong
Srikanth, Vishok
Spies, Jacob A.
Kirchhofer, Nathan D.
Yalcin, Sibel Ebru
Brudvig, Gary W.
Batista, Victor S.
Malvankar, Nikhil S.
author_sort Neu, Jens
collection PubMed
description Light-induced microbial electron transfer has potential for efficient production of value-added chemicals, biofuels and biodegradable materials owing to diversified metabolic pathways. However, most microbes lack photoactive proteins and require synthetic photosensitizers that suffer from photocorrosion, photodegradation, cytotoxicity, and generation of photoexcited radicals that are harmful to cells, thus severely limiting the catalytic performance. Therefore, there is a pressing need for biocompatible photoconductive materials for efficient electronic interface between microbes and electrodes. Here we show that living biofilms of Geobacter sulfurreducens use nanowires of cytochrome OmcS as intrinsic photoconductors. Photoconductive atomic force microscopy shows up to 100-fold increase in photocurrent in purified individual nanowires. Photocurrents respond rapidly (<100 ms) to the excitation and persist reversibly for hours. Femtosecond transient absorption spectroscopy and quantum dynamics simulations reveal ultrafast (~200 fs) electron transfer between nanowire hemes upon photoexcitation, enhancing carrier density and mobility. Our work reveals a new class of natural photoconductors for whole-cell catalysis.
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spelling pubmed-94525342022-09-09 Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires Neu, Jens Shipps, Catharine C. Guberman-Pfeffer, Matthew J. Shen, Cong Srikanth, Vishok Spies, Jacob A. Kirchhofer, Nathan D. Yalcin, Sibel Ebru Brudvig, Gary W. Batista, Victor S. Malvankar, Nikhil S. Nat Commun Article Light-induced microbial electron transfer has potential for efficient production of value-added chemicals, biofuels and biodegradable materials owing to diversified metabolic pathways. However, most microbes lack photoactive proteins and require synthetic photosensitizers that suffer from photocorrosion, photodegradation, cytotoxicity, and generation of photoexcited radicals that are harmful to cells, thus severely limiting the catalytic performance. Therefore, there is a pressing need for biocompatible photoconductive materials for efficient electronic interface between microbes and electrodes. Here we show that living biofilms of Geobacter sulfurreducens use nanowires of cytochrome OmcS as intrinsic photoconductors. Photoconductive atomic force microscopy shows up to 100-fold increase in photocurrent in purified individual nanowires. Photocurrents respond rapidly (<100 ms) to the excitation and persist reversibly for hours. Femtosecond transient absorption spectroscopy and quantum dynamics simulations reveal ultrafast (~200 fs) electron transfer between nanowire hemes upon photoexcitation, enhancing carrier density and mobility. Our work reveals a new class of natural photoconductors for whole-cell catalysis. Nature Publishing Group UK 2022-09-07 /pmc/articles/PMC9452534/ /pubmed/36071037 http://dx.doi.org/10.1038/s41467-022-32659-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Neu, Jens
Shipps, Catharine C.
Guberman-Pfeffer, Matthew J.
Shen, Cong
Srikanth, Vishok
Spies, Jacob A.
Kirchhofer, Nathan D.
Yalcin, Sibel Ebru
Brudvig, Gary W.
Batista, Victor S.
Malvankar, Nikhil S.
Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title_full Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title_fullStr Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title_full_unstemmed Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title_short Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
title_sort microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome omcs nanowires
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9452534/
https://www.ncbi.nlm.nih.gov/pubmed/36071037
http://dx.doi.org/10.1038/s41467-022-32659-5
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