Effects of soluble electron shuttles on microbial iron reduction and methanogenesis.

Abstract

In many aquatic and terrestrial ecosystems, iron (Fe) reduction by microorganisms is a key part of biogeochemical cycling and energy flux. The presence of redox-active electron shuttles in the environment potentially enables a phylogenetically diverse group of microbes to use insoluble iron as a terminal electron acceptor. We investigated the impact that different electron shuttles had on respiration, microbial physiology, and microbial ecology. We tested eight different electron shuttles, seven quinones and riboflavin, with redox potentials between 0.217 and -0.340 V. Fe(III) reduction coupled with acetate oxidation was observed with all shuttles. Once Fe(III) reduction began to plateau, a rapid increase in acetate consumption was observed and coincided with the onset of methane production, except in the incubations with the shuttle 9,10-anthraquinone-2-carboxylic acid (AQC). The rates of iron reduction, acetate consumption, methanogenesis, and the microbial communities varied significantly across the different shuttles independent of redox potential. In general, shuttles appeared to reduce the overall diversity of the community compared to no shuttle controls, but certain shuttles were exceptions to this trend. Geobacteraceae were the predominant taxonomic family in all enrichments except in the presence of AQC or 1,2-dihydroxyanthraquinone (AQZ), but each shuttle enriched a unique community significantly different from the no shuttle control conditions. This suggests that the presence of different redox-active electron shuttles can have a large influence on the microbial ecology and total carbon flux in the environment.IMPORTANCEIron is the fourth most abundant element in the Earth's crust, and the reduction of iron by microbes is an important component of global biogeochemical cycles. A phylogenetically diverse group of microbes is capable of conserving energy with oxidized iron as a terminal electron acceptor, but the environmental conditions favoring certain taxonomic clades in iron-reducing environments are unclear. One complicating factor often overlooked in small-scale enrichments is the influence of soluble, redox-active electron shuttles on the rate and microbial ecology of iron reduction. We tested the effects of eight different electron shuttles on microbial physiology and ecology in iron-reducing enrichments derived from a local wetland. Each electron shuttle varied the microbial activity and enriched for a microbial community distinct from the no shuttle control condition. Therefore, in complex subsurface environments with many redox-active compounds present, we propose electron shuttles as a reason for the coexistence of multiple clades of iron-reducing bacteria.