The bi-directional extracellular electron transfer process aids iron cycling by Geoalkalibacter halelectricus in a highly saline-alkaline condition

Abstract

Bi-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 haloalkaliphilic Geoalkalibacter halelectricus via bi-directional EET under haloalkaline conditions. It efficiently reduces Fe3+-oxide (Fe2O3) to Fe0 at a 2.29{+/-}0.07 mM/day rate linked to acetate oxidation via outward EET and oxidizes Fe0 to 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 A/cm2 current by linking acetate oxidation to anode reduction via outward EET and reduced fumarate by drawing electrons from the cathode (-2.5{+/-}0.3 A/cm2) via inward EET. The cyclic voltammograms of G. 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 by G. halelecctricus in achieving bi-directional EET. By reporting on the first haloalkaliphilic bacterium capable of oxidizing and reducing insoluble Fe0 and 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 of G. halelectricus in iron cycling in barely studied haloalkaline environments. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=116 SRC="FIGDIR/small/536630v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@1c8080aorg.highwire.dtl.DTLVardef@187d9d9org.highwire.dtl.DTLVardef@1ef6066org.highwire.dtl.DTLVardef@a2081b_HPS_FORMAT_FIGEXP M_FIG C_FIG