NanoSIMS imaging of extracellular electron transport processes during microbial iron(III) reduction

Abstract

Microbial iron(III) reduction can have a profound effect on the fate of contaminants in natural and engineered environments. Different mechanisms of extracellular electron transport are used by Geobacter and Shewanella spp. to reduce insoluble Fe(III) minerals. Here we prepared a thin film of iron(III)-(oxyhydr)oxide doped with arsenic, and allowed the mineral coating to be colonised by Geobacter sulfurreducens or Shewanella ANA3 labelled with 13C from organic electron donors. This preserved the spatial relationship between metabolically active Fe(III)-reducing bacteria and the iron(III)-(oxyhydr)oxide that they were respiring. NanoSIMS imaging showed cells of G. sulfurreducens were co-located with the iron(III)-(oxyhydr)oxide surface and were significantly more 13C-enriched compared to cells located away from the mineral, consistent with Geobacter species requiring direct contact with an extracellular electron acceptor to support growth. There was no such intimate relationship between 13C-enriched S. ANA3 and the iron(III)-(oxyhydr)oxide surface, consistent with Shewanella species being able to reduce Fe(III) indirectly using a secreted endogenous mediator. Some differences were observed in the amount of As relative to Fe in the local environment of G. sulfurreducens compared to the bulk mineral, highlighting the usefulness of this type of analysis for probing interactions between microbial cells and Fe-trace metal distributions in biogeochemical experiments.

Chromium Reduction via a Semi-Conducting Hematite Electrode: Implications for Microbial Cycling of Metals in Natural Soils

“…Fe(II) forms favorable redox couples with other priority contaminants such as U or As, and this mechanism could play a role in the remediation or natural cycling of those contaminants. 3,[57][58][59][60] Fe(II) catalyzed recrystallization has been demonstrated for goethite, another semi-conducting Fe mineral, thus the results here also imply that this conduction mechanism may be more broadly applicable wherever Fe cycling occurs. Further investigation is needed, however, to demonstrate the range of biogeochemical systems where this mechanism is relevant, further understand the influence of these processes on hematite surface chemistry and illustrate the importance for this mechanism in natural soils and groundwater.…”

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

“…2), partial reduction of magnetite occurred; reflecting the availability for this less reactive iron oxide to serve as electron acceptor as well. A recent study used SEM to demonstrate that Geobacter can partly reduce an iron oxide mineral while colonizing its surface, with the partial reduction attributed to Geobacter being able to form direct cell-mineral contact [75]. Similarly acetoclastic methanogenesis was enhanced in Methanosarcina mazei when provided with magnetite nanoparticles while magnetite nanoparticles colonized the methanogen cell [76].…”

Bacterial diversity in Icelandic cold spring sources and in relation to the groundwater amphipod Crangonyx islandicus

“…The Shewanella , a chemolithoheterotrophic bacteria, can utilize sulphate and reduce iron and manganese, even without being in direct contact with the metal [75]. Most species can grow at 4°C [76], which is the same as the temperature of the spring waters where the amphipods are found in.…”