Thermodynamic controls on rates of iron oxide reduction by extracellular electron shuttles

Anaerobic microbial respiration in suboxic and anoxic environments often involves particulate ferric iron (oxyhydr-)oxides as terminal electron acceptors. To ensure efficient respiration, a widespread strategy among iron-reducing microorganisms is the use of extracellular electron shuttles (EES) that transfer two electrons from the microbial cell to the iron oxide surface. Yet, a fundamental understanding of how EES-oxide redox thermodynamics affect rates of iron oxide reduction remains elusive. Attempts to rationalize these rates for different EES, solution pH, and iron oxides on the basis of the underlying reaction free energy of the two-electron transfer were unsuccessful. Here, we demonstrate that broadly varying reduction rates determined in this work for different iron oxides and EES at varying solution chemistry as well as previously published data can be reconciled when these rates are instead related to the free energy of the less exergonic (or even endergonic) first of the two electron transfers from the fully, two-electron reduced EES to ferric iron oxide. We show how free energy relationships aid in identifying controls on microbial iron oxide reduction by EES, thereby advancing a more fundamental understanding of anaerobic respiration using iron oxides.