skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 8:00 PM ET on Friday, March 21 until 8:00 AM ET on Saturday, March 22 due to maintenance. We apologize for the inconvenience.


Title: 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.

 
more » « less
Award ID(s):
2038000 1749662
PAR ID:
10372863
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
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
More Like this
  1. 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.

     
    more » « less
  2. Abstract

    Extracellular electron transfer (EET) via microbial nanowires drives globally-important environmental processes and biotechnological applications for bioenergy, bioremediation, and bioelectronics. Due to highly-redundant and complex EET pathways, it is unclear how microbes wire electrons rapidly (>106 s−1) from the inner-membrane through outer-surface nanowires directly to an external environment despite a crowded periplasm and slow (<105 s−1) electron diffusion among periplasmic cytochromes. Here, we show thatGeobacter sulfurreducensperiplasmic cytochromes PpcABCDE inject electrons directly into OmcS nanowires by binding transiently with differing efficiencies, with the least-abundant cytochrome (PpcC) showing the highest efficiency. Remarkably, this defined nanowire-charging pathway is evolutionarily conserved in phylogenetically-diverse bacteria capable of EET. OmcS heme reduction potentials are within 200 mV of each other, with a midpoint 82 mV-higher than reported previously. This could explain efficient EET over micrometres at ultrafast (<200 fs) rates with negligible energy loss. Engineering this minimal nanowire-charging pathway may yield microbial chassis with improved performance.

     
    more » « less
  3. Every living cell needs to get rid of leftover electrons when metabolism extracts energy through the oxidation of nutrients. Common soil microbes such as Geobacter sulfurreducens live in harsh environments that do not afford the luxury of soluble, ingestible electron acceptors like oxygen. Instead of resorting to fermentation, which requires the export of reduced compounds (e.g. ethanol or lactate derived from pyruvate) from the cell, these organisms have evolved a means to anaerobically respire by using nanowires to export electrons to extracellular acceptors in a process called extracellular electron transfer (EET) [ 1]. Since 2005, these nanowires were thought to be pili filaments [ 2]. But recent studies have revealed that nanowires are composed of multiheme cytochromes OmcS [ 3, 4] and OmcZ [ 5] whereas pili remain inside the cell during EET and are required for the secretion of nanowires [ 6]. However, how electrons are passed to these nanowires remains a mystery ( Figure 1A). Periplasmic cytochromes (Ppc) called PpcA-E could be doing the job, but only two of them (PpcA and PpcD) can couple electron/proton transfer — a necessary condition for energy generation. In a recent study, Salgueiro and co-workers selectively replaced an aromatic with an aliphatic residue to couple electron/proton transfer in PpcB and PpcE (Biochem. J. 2021, 478 (14): 2871–2887). This significant in vitro success of their protein engineering strategy may enable the optimization of bioenergetic machinery for bioenergy, biofuels, and bioelectronics applications. 
    more » « less
  4. null (Ed.)
    Materials that convert wasted heat into electricity are needed to help solve global warming and other climate challenges. Thermoelectric nanowires are novel metamaterials for such applications. Non-adiabatic coupling computations are critical in understanding thermally activated charge transfer in thermoelectric materials. Here, non-adiabatic computations are used to evaluate electron relaxation rates in lead telluride nanowires. This work reports results on PbTe (lead telluride) atomistic models doped with sodium and iodine that contain 288 atoms in simulation cells with periodic boundary conditions. The calculations are performed on the basis of ground-state DFT under the VASP software. The transitions between states are modelled in terms of Redfield equation of motion parameterised by on-the-fly non-adiabatic couplings along thermalised molecular dynamic trajectory. The initial states are approximated by the promotion of an electron from occupied to unoccupied Kohn–Sham orbital. In each transition, the change of the energy and spatial charge distribution with respect to time were calculated, demonstrating formation of charge transfer. The trends of electron and hole relaxation rates comply with the energy gap law. 
    more » « less
  5. Abstract

    Zinc oxide (ZnO) nanowires are widely studied for use in ultraviolet optoelectronic devices, such as nanolasers and sensors. Nanowires (NWs) with an MgO shell exhibit enhanced band‐edge photoluminescence (PL), a result previously attributed to passivation of ZnO defects. However, we find that processing the ZnO NWs under low oxygen partial pressure leads to an MgO‐thickness‐dependent PL enhancement owing to the formation of optical cavity modes. Conversely, processing under higher oxygen partial pressure leads to NWs that support neither mode formation nor band‐edge PL enhancement. High‐resolution electron microscopy and density‐functional calculations implicate the ZnOm‐plane surface morphology as the key determinant of core‐shell structure and cavity‐mode optics. A ZnO surface with atomic steps along them‐plane in thec‐axis direction stimulates the growth of a smooth MgO shell that supports guided‐wave optical modes and enhanced UV PL. On the other hand, a smoother ZnO surface leads to nucleation of a rough cladding layer which supports neither enhanced UV PL nor optical cavity modes. Finite‐element analysis shows a clear correlation between allowed Fabry‐Perot and whispering gallery modes and enhanced UV‐PL. These results point the way to fabricating ZnO/MgO core‐shell nanowires for more efficient UV nanolasers, scintillators, and sensors.

     
    more » « less