Understanding the role of phototrophic extracellular electron uptake in terrestrial carbon cycling at the systems level

Abstract:

Phototrophic extracellular electron uptake (pEEU) is a biological phenomenon by which photoautotrophs harness the energy of light and electrons from solid-phase conductive minerals (SPCMs) or their proxies (e. g., poised electrodes) to fix carbon dioxide (CO₂). Because wetland soils contain abundant SPCMs such as iron, pEEU likely has a crucial role in wetland carbon sequestration. To understand the role of pEEU in carbon sequestration in terrestrial inland wetland soils, we studied the soil from the Ellis Island wetland area located in Alton, Missouri. Initial characterization of the soil using SEM-EDS and FTIR revealed the presence of SPCMs such as hematite (Fe₂O₃) and goethite [FeO(OH)] that are essential minerals for anoxygenic phototrophs to fix CO₂ via pEEU in nature. We enriched the electroactive photoautotrophs using native soil as an inoculum in a bioelectrochemical (BEC) reactor using a carbon-felt electrode poised at a potential of +100 mV vs. standard hydrogen electrode (SHE). Incubation in a freshwater medium (FWM) under continuous infrared (IR) light shows biofilm development on the electrode surface. Cyclic voltammetry analysis showed that the electrochemical redox potential of biofilm-bound electrode is -330 mV. We then transferred the biofilm-bound electrode to a new BEC reactor with fresh FWM and poised at -330 mV for 80 h. The pEEU of biofilm-bound electrode was measured to be ~-5 mA cm^-2. These results suggest that pEEU-capable phototrophs are abundant in Ellis Island soils. Phylogenetic analysis using the pufM gene, encoding the type-II photosynthetic apparatus, suggests that the isolated microbes are closely related to the plant-associated Rhodopseudomonas palustris strain YSC3. Our preliminary data suggest that Ellis Island soils harbors pEEU-capable phototrophs that can potentially use SPCMs as electron donors (with electrodes serving as their proxies) for photoautotrophic growth. Our continued research on Ellis Island soils will add new systems-level insights into the role of pEEU in inland wetland ecosystems. Overall, our results will help refine the involvement of anoxygenic phototrophs in wetland soil carbon accumulation.