Extracellular electron transfer through microbial reduction of solid-phase humic substances

The decay of soil and sedimentary organic matter yields organic compounds with a high molecular weight, termed humic substances(1). Microorganisms can transfer electrons to dissolved humic substances(2), and reduced humic substances can rapidly reduce iron(III) oxides(3). Thus, dissolved humic substances can serve as electron shuttles that promote iron( III) oxide reduction in sediments(2,4). However, most humic substances in soils and sediments are in particulate, rather than dissolved, form(1); the ability of microorganisms to reduce solid-phase humics and their capacity to shuttle electrons is thus far unknown. Here we show through incubation experiments and electron spin resonance measurements that iron(III)-oxide-reducing bacteria can transfer electrons to solid-phase humic substances in sediments sampled from wetlands. Although the electron-accepting capacity of the solid-phase humics was modest, solid-phase humics significantly accelerated iron(III) oxide reduction, by shuttling electrons from bacteria to oxide surfaces. Microbial solid-phase humics reduction represents a new mechanism for extracellular electron transfer that can facilitate reduction of iron(III) oxide and other redox reactions in sediments and soils.