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 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.

A natural impact-resistant bicontinuous composite nanoparticle coating.

Nature utilizes the available resources to construct lightweight, strong and tough materials under constrained environmental conditions. The impact surface of the fast-striking dactyl club from the mantis shrimp is an example of one such composite material; the shrimp has evolved the capability to localize damage and avoid catastrophic failure from high-speed collisions during its feeding activities. Here we report that the dactyl club of mantis shrimps contains an impact-resistant coating composed of densely packed (about 88 per cent by volume) ~65-nm bicontinuous nanoparticles of hydroxyapatite integrated within an organic matrix. These mesocrystalline hydroxyapatite nanoparticles are assembled from small, highly aligned nanocrystals. Under impacts of high strain rates (around 104 s-1), particles rotate and translate, whereas the nanocrystalline networks fracture at low-angle grain boundaries, form dislocations and undergo amorphization. The interpenetrating organic network provides additional toughening, as well as substantial damping, with a loss coefficient of around 0.02. An unusual combination of stiffness and damping is therefore achieved, outperforming many engineered materials.

Anaerobic Respiration on Self-Doped Conjugated Polyelectrolytes: Impact of Chemical Structure.

We probe anaerobic respiration of bacteria in the presence of conjugated polyelectrolytes (CPEs). Three different CPEs were used to probe how structural variations impact biocurrent generation from Shewanella oneidensis MR-1. For the self-doped anionic CPE only, absorption spectroscopy shows that the addition of S. oneidensis MR-1 leads to the disappearance of the polaron (radical cation) band at >900 nm and an increase in the band at 735 nm due to the neutral species, consistent with electron transfer from microbe to polymer. Microbial three-electrode electrochemical cells (M3Cs) show an increase in the current generated by S. oneidensis MR-1 with addition of the self-doped CPE relative to other CPEs and controls. These experiments combined with in situ cyclic voltammetry suggest that the doped CPE facilitates electron transport to electrodes and reveal structure-function relationships relevant to developing materials for biotic/abiotic interfaces.

Biofilm as a redox conductor: a systematic study of the moisture and temperature dependence of its electrical properties.

Some microbial biofilms are electrically conductive. However, the mechanism of electron transport remains unclear. Here, we show that µm-scale long-distance electron transport through electrode-grown Geobacter sulfurreducens biofilms occurs via redox conduction, as determined by electrical measurements performed under varied hydration states and temperatures.

The conjugated oligoelectrolyte DSSN+ enables exceptional coulombic efficiency via direct electron transfer for anode-respiring Shewanella oneidensis MR-1-a mechanistic study.

Shewanella oneidensis MR-1 was cultivated on lactate with poised graphite electrode acceptors (E = +0.2 V vs. Ag/AgCl) in order to explore the basis for sustained increases in anodic current output following the addition of the lipid-intercalating conjugated oligoelectrolyte (COE), 4,4'-bis(4'-(N,N-bis(6''-(N,N,N-trimethylammonium)hexyl)amino)-styryl)stilbene tetraiodide (DSSN+). Microbial cultures, which were spiked with DSSN+, exhibit a ∼2.2-fold increase in charge collected, a ∼3.1-fold increase in electrode colonization by S. oneidensis, and a ∼1.7-fold increase in coulombic efficiency from 51 ± 10% to an exceptional 84 ± 7% without obvious toxicity effects. Direct microbial biofilm voltammetry reveals that DSSN+ rapidly and sustainably increases cytochrome-based direct electron transfer and subsequently increases flavin-based mediated electron transfer. Control experiments indicate that DSSN+ does not contribute to the current in the absence of bacteria.

Improving charge collection in Escherichia coli-carbon electrode devices with conjugated oligoelectrolytes.

It is important to tailor biotic-abiotic interfaces in order to maximize the utility of bioelectronic devices such as microbial fuel cells (MFCs), electrochemical sensors and bioelectrosynthetic systems. The efficiency of electron-equivalent extraction (or injection) across such biotic-abiotic interfaces is dependent on the choice of the microbe and the conductive electrode material. In this contribution, we show that spontaneous intercalation of a conjugated oligoelectrolyte, namely 4,4'-bis(4'-(N,N-bis(6''-(N,N,N-trimethylammonium)hexyl)amino)-styryl)stilbene tetraiodide (DSSN+), into the membranes of Escherichia coli leads to an increase in current generation in MFCs containing carbon-based electrodes. A combination of scanning electron microscopy (SEM) and confocal microscopy was employed to confirm the incorporation of DSSN+ into the cell membrane and biofilm formation atop carbon felt electrodes. Current collection was enhanced by more than 300% with addition of this conjugated oligoelectrolyte. The effect of DSSN+ concentration on electrical output was also investigated. Higher concentrations, up to 25 µM, lead to an overall increase in the number of charge equivalents transferred to the charge-collecting electrode, providing evidence in support of the central role of the synthetic system in improving device performance.

Conjugated oligoelectrolytes increase power generation in E. coli microbial fuel cells.

A series of conjugated oligoelectrolytes with structural variations is used to stain E. coli. By taking advantage of a high-throughput screening platform that incorporates gold anodes, it is found that MFCs with COE-modified E. coli generate significantly higher power densities, relative to unmodified E. coli. These findings highlight the potential of using water-soluble molecules inspired by the work on organic semiconductors to improve electrode/microbe interfaces.