Electrochemical Investigation of a Microbial Solar Cell Reveals a Nonphotosynthetic Biocathode Catalyst

Microbial solar cells (MSCs) are microbial fuel cells (MFCs) that generate their own oxidant and/or fuel through photosynthetic reactions. Here, we present electrochemical analyses and biofilm 16S rRNA gene profiling of biocathodes of sediment/seawaterbased MSCs inoculated from the biocathode of a previously described sediment/seawater-based MSC. Electrochemical analyses indicate that for these second-generation MSC biocathodes, catalytic activity diminishes over time if illumination is provided during growth, whereas it remains relatively stable if growth occurs in the dark. For both illuminated and dark MSC biocathodes, cyclic voltammetry reveals a catalytic-current–potential dependency consistent with heterogeneous electron transfer mediated by an insoluble microbial redox cofactor, which was conserved following enrichment of the dark MSC biocathode using a three-electrode configuration. 16S rRNA gene profiling showed Gammaproteobacteria, most closely related to Marinobacter spp., predominated in the enriched biocathode. The enriched biocathode biofilm is easily cultured on graphite cathodes, forms a multimicrobe-thick biofilm (up to 8.2 μm), and does not lose catalytic activity after exchanges of the reactor medium. Moreover, the consortium can be grown on cathodes with only inorganic carbon provided as the carbon source, which may be exploited for proposed bioelectrochemical systems for electrosynthesis of organic carbon from carbon dioxide. These results support a scheme where two distinct communities of organisms develop within MSC biocathodes: one that is photosynthetically active and one that catalyzes reduction of O2 by the cathode, where the former partially inhibits the latter. The relationship between the two communities must be further explored to fully realize the potential for MSC applications

Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms

Redox cycling of extracellular electron shuttles can enable the metabolic activity of subpopulations within multicellular bacterial biofilms that lack direct access to electron acceptors or donors. How these shuttles catalyze extracellular electron transfer (EET) within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazines mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by eDNA binding. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and can participate directly in redox reactions through DNA. In vivo, biofilm eDNA can also support rapid electron transfer between redox active intercalators. Together, these results establish that PYO:eDNA interactions support an efficient redox cycle with rapid EET that is faster than the rate of PYO loss from the biofilm

Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms

Redox cycling of extracellular electron shuttles can enable the metabolic activity of subpopulations within multicellular bacterial biofilms that lack direct access to electron acceptors or donors. How these shuttles catalyze extracellular electron transfer (EET) within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazines mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by eDNA binding. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and can participate directly in redox reactions through DNA. In vivo, biofilm eDNA can also support rapid electron transfer between redox active intercalators. Together, these results establish that PYO:eDNA interactions support an efficient redox cycle with rapid EET that is faster than the rate of PYO loss from the biofilm

Harvesting Energy from the Marine Sediment−Water Interface

Pairs of platinum mesh or graphite fiber-based electrodes, one embedded in marine sediment (anode), the other in proximal seawater (cathode), have been used to harvest low-level power from natural, microbe established, voltage gradients at marine sediment−seawater interfaces in laboratory aquaria. The sustained power harvested thus far has been on the order of 0.01 W/m2 of electrode geometric area but is dependent on electrode design, sediment composition, and temperature. It is proposed that the sediment/anode−seawater/cathode configuration constitutes a microbial fuel cell in which power results from the net oxidation of sediment organic matter by dissolved seawater oxygen. Considering typical sediment organic carbon contents, typical fluxes of additional reduced carbon by sedimentation to sea floors < 1000 m deep, and the proven viability of dissolved seawater oxygen as an oxidant for power generation by seawater batteries, it is calculated that optimized power supplies based on the phenomenon demonstrated here could power oceanographic instruments deployed for routine long-term monitoring operations in the coastal ocean

Electrode-Reducing Microoganisms that Harvest energy from Marine Sediments

Energy in the form of electricity can be harvested from marine sediments by placing a graphite electrode (the anode) in the anoxic zone and connecting it to a graphite cathode in the overlying aerobic water. We report a specific enrichment of microorganisms of the family Geobacteraceae on energy-harvesting anodes, and we show that these microorganisms can conserve energy to support their growth by oxidizing organic compounds with an electrode serving as the sole electron acceptor. This finding not only provides a method for extracting energy from organic matter, but also suggests a strategy for promoting the bioremediation of organic contaminants in subsurface environments

Microbial Electrochemical Energy Storage and Recovery in a Combined Electrotrophic and Electrogenic Biofilm

Here we report enrichment from a marine-derived inoculum of a nonphotosynthetic electroactive biofilm that is capable of both consuming electricity (electrotrophy) and producing electricity (electrogenesis) from a single electrode. With the alternation of the electrode potential between −0.4 and 0.0 VSHE every 10 min, alternating anodic and cathodic currents increased in lock step (maximum current density of ±1.4 ± 0.4 A/m2 in both modes, Coulombic efficiency of ∼98% per charge−discharge cycle), which is consistent with alternating between generation and consumption of energy storage compounds by the biofilm. Cyclic voltammetry exhibited a single sigmoid-shaped feature spanning anodic and cathodic limiting currents centered at −0.15 VSHE, a phenomenon not observed to date for an electroactive biofilm, and square wave voltammetry exhibited reversible peaks at −0.15 and −0.05 VSHE, suggesting the same redox cofactor(s) facilitates electron transport at the biofilm−electrode interface in both modes. Hydrogen and carbon monoxide, known energy and/or carbon sources for cellular metabolism, but no volatile fatty acids, were detected in reactors. Cells and cell clusters were spread across the electrode surface, as seen by confocal microscopy. These results suggest that a single microbial electrochemical biofilm can alternate between storing energy and generating power, furthering the potential applicability of bioelectrochemical systems