Dissimilatory metal-reducing bacteria (DMRB) gain energy by coupling the oxidation of reduced organic compounds or H2 to the reduction of iron and other metal oxides. These oxides are poorly soluble at the temperature and pH ranges typical of most critical zone environments, and consequently many DMRB use soluble electron-shuttling compounds to aid the transfer of electrons to these extracellular electron acceptors. Pure culture studies suggest these electron shuttles enhance the overall rate of iron reduction, yet little is known about how the presence of these compounds affects complex native communities of microorganisms under iron-reducing conditions. We examined the effect quinone-based electron shuttles with different redox potentials have on the rate of iron reduction, the onset of methanogenesis, and the trajectory of microbial community development in wetland sediment microcosms amended with goethite (α-FeOOH) and either acetate or H2. Unlike pure culture experiments, microcosms given 9,10-anthraquinone-2-carboxylic acid (AQC) or 5-hydroxy-1,4-naphthoquinone (lawsone, NQL) showed no increase in the rate of iron reduction relative to control experiments with no shuttle (NS) added. The rate and extent of iron reduction increased significantly however in those given 9,10-anthraquinone-2,6-disulfonate (AQDS). Methanogenesis did not begin in AQDS, NQL, or NS microcosms until ferrous iron production ceased and was inhibited entirely in AQC-amended microcosms. These AQC-amended microcosms also showed a significant divergence from the others in microbial community development. 16S rRNA sequences classified as Geobacteraceae dominated NS control microcosms (61% average abundance) as well as those amended with AQDS (42-65%) and NQL (62%), though distinct operational taxonomic units (OTUs) were abundant depending on the shuttle used. AQC microcosms were instead dominated by Pelobacteraceae (68% in acetate-amended) or Shewanellaceae (72% in H2-amended), while Geobacteraceae accounted for only 8% and 1% of the total, respectively. These results suggest both redox potential and electron donor determine in part the extent and mechanism of iron reduction as well as the identity of the DMRB carrying out this process. Moreover, the complete inhibition of methanogenesis by AQC highlights the possibility for electron shuttles to influence microbial processes in addition to those involving respiration with insoluble terminal electron acceptors.

Effect of soluble electron shuttles on Iron(III) reduction, methane production, and microbial community dynamics in wetland sediment microcosms

253rd National Meeting (2017)

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