The involvement of Shewanella spp. in biocorrosion is often attributed to their Fe(III)-reducing properties, but they could also affect corrosion by using metallic iron as an electron donor. Previously, we isolated Shewanella strain 4t3-1-2LB from an acetogenic community enriched with Fe(0) as the sole electron donor. Here, we investigated its use of Fe(0) as an electron donor with fumarate as an electron acceptor and explored its corrosion-enhancing mechanism. Without Fe(0), strain 4t3-1-2LB fermented fumarate to succinate and CO 2, as was shown by the reaction stoichiometry and pH. With Fe(0), strain 4t3-1-2LB completely reduced fumarate to succinate and increased the Fe(0) corrosion rate (7.0 ± 0.6)-fold in comparison to that of abiotic controls (based on the succinate-versus-abiotic hydrogen formation rate). Fumarate reduction by strain 4t3-1-2LB was, at least in part, supported by chemical hydrogen formation on Fe(0). Filter-sterilized spent medium increased the hydrogen generation rate only 1.5-fold, and thus extracellular hydrogenase enzymes appear to be insufficient to explain the enhanced corrosion rate. Electrochemical measurements suggested that strain 4t3-1-2LB did not excrete dissolved redox mediators. Exchanging the medium and scanning electron microscopy (SEM) imaging indicated that cells were attached to Fe(0). It is possible that strain 4t3-1-2LB used a direct mechanism to withdraw electrons from Fe(0) or favored chemical hydrogen formation on Fe(0) through maintaining low hydrogen concentrations. In coculture with an Acetobacterium strain, strain 4t3-1-2LB did not enhance acetogenesis from Fe(0). This work describes a strong corrosion enhancement by a Shewanella strain through its use of Fe(0) as an electron donor and provides insights into its corrosion-enhancing mechanism.
IMPORTANCE Shewanella spp. are frequently found on corroded metal structures. Their role in microbial influenced corrosion has been attributed mainly to their Fe(III)-reducing properties and, therefore, has been studied with the addition of an electron donor (lactate). Shewanella spp., however, can also use solid electron donors, such as cathodes and potentially Fe(0). In this work, we show that the electron acceptor fumarate supported the use of Fe(0) as the electron donor by Shewanella strain 4t3-1-2LB, which caused a (7.0 ± 0.6)-fold increase of the corrosion rate. The corrosion-enhancing mechanism likely involved cell surface-associated components in direct contact with the Fe(0) surface or maintenance of low hydrogen levels by attached cells, thereby favoring chemical hydrogen formation by Fe(0). This work sheds new light on the role of Shewanella spp. in biocorrosion, while the insights into the corrosion-enhancing mechanism contribute to the understanding of extracellular electron uptake processes.