Electron transfer versatility of a Geobacter sp. links PAH degradation with multi-electron acceptor respiration,...

Anaerobic degradation of polycyclic aromatic hydrocarbons (PAHs) is often constrained by the availability and accessibility of terminal electron acceptors in anoxic, metal-rich environments. Here we characterize a Geobacter sp. (strain GeoA) that couples phenanthrene oxidation to respiration with nitrate, Mn(IV), Fe(III)-citrate, sulfate, Cr(VI), and crystalline magnetite. Phenanthrene removal (initial 280 μM) proceeded fastest with Mn(IV) and nitrate (about 96 % within 5-7 d), followed by Fe(III)-citrate (about 95 % in 20 d), sulfate (about 95 % in 24 d), and Cr(VI) (about 61 % in 56 d, concomitant with complete reduction of 2.1 mM Cr(VI)). While previous studies mainly focused on amorphous or poorly crystalline Fe(III) minerals, the role of highly crystalline magnetite as an active electron sink has remained unclear. In this study, GeoA reduced ∼35 % of supplied magnetite (20 mM Fe(III) basis) and exhibited an acetate:Fe(III) stoichiometry (∼1:8) consistent with dissimilatory reduction. XPS and AQDS enhancement assays, together with upregulation of pilA and the flavin exporter yeeO, indicate that both direct and shuttle-facilitated extracellular electron transfer contribute to crystalline iron oxide reduction. Metabolite profiling with ¹³C-bicarbonate labelling, together with genomic evidence, supports a carboxylation-initiated route for anaerobic phenanthrene activation. An analysis of Earth Microbiome Project datasets shows Geobacter predominance among dissimilatory iron-reducing genera in soils and sediments, consistent with ecological adaptation to solid-phase electron acceptors. These findings expand the known respiratory flexibility and bio-remediation potential of PAH-degrading bacteria and provide the first mechanistic evidence of PAH oxidation coupled to magnetite reduction by a single pure strain, highlighting crystalline magnetite as a relevant electron sink in PAH-metal co-contaminated anoxic environments.