Iron Corrosion via Direct Metal-Microbe Electron Transfer

Abstract

The concept that anaerobic microorganisms can directly accept electrons from Fe(0) has been controversial because direct metal-microbe electron transfer has previously only been indirectly inferred. Fe(0) oxidation was studied with Geobacter sulfurreducens strain ACL, an autotrophic strain that was previously shown to grow with electrons derived from a graphite cathode as the sole electron donor. Strain ACL grew with Fe(0) as the sole electron donor and fumarate as the electron acceptor. However, it appeared that at least a portion of the electron transfer was via H2 produced nonenzymatically from the oxidation of Fe(0) to Fe(II). H2, which accumulated in abiotic controls, was consumed during the growth of strain ACL, the cells were predominately planktonic, and genes for the uptake hydrogenase were highly expressed. Strain ACLHF was constructed to prevent growth on H2 or formate by deleting the genes for the uptake of hydrogenase and formate dehydrogenases from strain ACL. Strain ACLHF also grew with Fe(0) as the sole electron donor, but H2 accumulated in the culture, and cells heavily colonized Fe(0) surfaces with no visible planktonic growth. Transcriptomics suggested that the outer surface c-type cytochromes OmcS and OmcZ were important during growth of strain ACLHF on Fe(0). Strain ACLHF did not grow on Fe(0) if the gene for either of these cytochromes was deleted. The specific attachment of strain ACLHF to Fe(0), coupled with requirements for known extracellular electrical contacts, suggest that direct metal-microbe electron transfer is the most likely option for Fe(0) serving as an electron donor. IMPORTANCE The anaerobic corrosion of iron structures is expensive to repair and can be a safety and environmental concern. It has been known for over 100 years that the presence of anaerobic respiratory microorganisms can accelerate iron corrosion. Multiple studies have suggested that there are sulfate reducers, methanogens, and acetogens that can directly accept electrons from Fe(0) to support sulfate or carbon dioxide reduction. However, all of the strains studied can also use H2 as an electron donor for growth, which is known to be abiotically produced from Fe(0). Furthermore, no proteins definitely shown to function as extracellular electrical contacts with Fe(0) were identified. The studies described here demonstrate that direct electron transfer from Fe(0) can support anaerobic respiration. They also map out a simple genetic approach to the study of iron corrosion mechanisms in other microorganisms. A better understanding of how microorganisms promote iron corrosion is expected to lead to the development of strategies that can help reduce adverse impacts from this process.

Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis

“…This conclusion was confirmed by metallic iron corrosion experiments, which can help in the understandings of microbial EEU mechanisms: if a direct electron uptake pathway is present, microbes are able to use Fe 0 as sole electron donor. Very recently, Tang et al (2019) has demonstrated direct metal electron uptake via c-OMCs in the autotrophic strain Geobacter sulfurreducens ACL. Evidences of similar EEU mechanism have been reported for two iron-corroding SRB, Desulfopila corrodens strain IS4 (Beese-Vasbender et al, 2015) and Desulfovibrio ferrophilus IS5 .…”

Enrichment of novelVerrucomicrobia, BacteroidetesandKrumholzibacteriain an oxygen-limited, methane- and iron-fed bioreactor inoculated with Bothnian Sea sediments

“…It is intriguing that krumholzibacteria_1 had both iron oxidation and reduction genes. The capacity for iron oxidation and reduction in the same organism has been previously described in Geobacter sulfurreducens (68,69). Further studies are necessary to elucidate these potential roles of krumholzibacteria_1 in iron cycling.…”

Geobacter protein nanowires

“…G. uraniireducens, which has an OmcS homolog but lacks e-pili, has phenotypes inconsistent with filament-based long-range electron transport (Butler et al, 2010;Rotaru et al, 2015;Tan et al, 2016b). OmcS is important for some forms of G. sulfurreducens extracellular electron exchange (Mehta et al, 2005;Summers et al, 2010b;Tang et al, 2019). An important question is whether OmcS exists as filaments extending from the cells in vivo or whether OmcS attached to cells or e-pili is the functionally important localization of OmcS.…”

“…However, in these instances OmcS localized along the surface of the cell may facilitate electron transport to e-pili (Mehta et al, 2005;Lovley, 2006) or OmcS localized along e-pili may promote electron transport between e-pili and Fe(III) oxides (Lovley, 2011). Deletion of the OmcS gene inhibited electron uptake from zero valent iron, but the cells were in close association with the metal surface, and thus would not require long filaments of OmcS extending from the cell in order to establish electrical contact via OmcS (Tang et al, 2019). An OmcS-deficient mutant did not effectively grow as the electron-accepting partner in co-cultures with G. metallireducens as the electron-donating microorganism (Summers et al, 2010a), but the requirement that G. metallireducens express e-pili for co-culture growth (Ueki et al, 2018) suggests that 712 conduits other than OmcS are important for the long-range electron transport between the 713 two species.…”