The bi-directional extracellular electron transfer process aids iron cycling byGeoalkalibacter halelectricusin a highly saline-alkaline condition

Abstract

AbstractBi-directional extracellular electron transfer (EET) is crucial to upholding microbial metabolism with insoluble electron acceptors or donors in anoxic environments. Investigating bi-directional EET-capable microorganisms is desired to understand the cell-cell and microbe-mineral interactions and their role in mineral cycling besides leveraging their energy generation and conversion, biosensing, and bio-battery applications. Here, we report on iron cycling by haloalkaliphilicGeoalkalibacter halelectricusvia bi-directional EET under haloalkaline conditions. It efficiently reduces Fe3+-oxide (Fe2O3) to Fe0at a 2.29±0.07 mM/day rate linked to acetate oxidation via outward EET and oxidizes Fe0to Fe3+with a 0.038±0.002 mM/day rate via inward EET to reduce fumarate. Bioelectrochemical cultivation confirmed its outward and inward EET capabilities. It produced 895±23 μA/cm2current by linking acetate oxidation to anode reduction via outward EET and reduced fumarate by drawing electrons from the cathode (−2.5±0.3 μA/cm2) via inward EET. The cyclic voltammograms ofG. halelectricus biofilms revealed redox moieties with different formal potentials, suggesting the involvement of different membrane components in bi-directional EET. The cyclic voltammetry and GC-MS analysis of the cell-free spent medium revealed the lack of soluble redox mediators, suggesting direct electron transfer byG. halelecctricus in achieving bi-directional EET. By reporting on the first haloalkaliphilic bacterium capable of oxidizing and reducing insoluble Fe0and Fe3+-oxide, respectively, this study advances the limited understanding of the metabolic capabilities of extremophiles to respire on insoluble electron acceptors or donors via bi-directional EET and invokes the possible role ofG. halelectricus in iron cycling in barely studied haloalkaline environments.Graphical abstract