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Abstract Microbial respiration via extracellular electron transfer (EET) drives several globally-important environmental processes and has applications in bioenergy, bioremediation, and bioelectronics.Geobacter sulfurreducensproduce micrometer-long cytochrome nanowires for long-range (>10 µm) EET, but also require transmembrane porin-cytochrome complexes (PCCs), which can only perform EET on the cell surface. It was unknown why cells performing long-range EET need both PCCs and nanowires. Using Om(abc)B and OmcS as a model PCC and nanowire, respectively, for EET to Fe(III), we show that PCCs and nanowires form sequential, independent EET pathways where PCCs first kickstart EET and provide energy crucial for nanowire synthesis, and then nanowires perform long-range EET. Our model explains why both PCCs and nanowires are necessary. To understand the underlying EET mechanism, we purified native Om(ab)B and OmcB and found high excitonic coupling among hemes. Their midpoint reduction potentials (-182, -167 mV, respectively) are tuned for efficient electron transport. Additionally, OmcB transfers electrons to Fe(III) ~5 times more efficiently than OmcS. Our work suggests that the metabolic trade-off between PCCs and nanowires results from efficient proteome allocation. Notably, PCCs are widespread in environmentally-important bacteria and co-evolved with OmcS nanowires. This previously-undescribed nanowire synthesis strategy could accelerate EET in diverse microbes and environments.
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Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires
Abstract 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 ofGeobacter sulfurreducensuse 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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- PAR ID:
- 10372863
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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