Electron shuttles enhance anaerobic oxidation of methane coupled to iron(III) reduction

Anaerobic oxidation of methane (AOM) has recently been coupled with the reduction of insoluble electron acceptors such as iron minerals. However, effects of electron shuttles (ESs) on this process and the underlying coupling mechanisms remain not well understood. Here, we evaluated AOM-coupled ferrihydrite reduction by a mixed culture in the absence and presence of ESs. The results showed that ESs (AQS, flavin, HA and AQDS) significantly enhanced the rate (up to 7.4 times) of AOM-dependent ferrihydrite reduction compared with the control. The enhancements were linearly related with the electron transfer capacity of ESs. Illumina high-throughput sequencing and DNA-based stable isotope probing revealed that the AOM-coupled iron reduction depended on the syntrophic interaction of Methanobacterium and the partner bacteria. Methanobacterium as the dominant microorganism, did not assimilate methane into its biomasses. However, it played a crucial role in the partial oxidation of methane into an intermediate (i.e. propionate), which was then assimilated by the partner bacteria (e.g. Cellulomonas, Desulfovibrio, Actinotalea, etc.) for ferrihydrite reduction. This work suggests that ESs in natural environments can mitigate the methane emissions by facilitating the AOM process and biogeochemical cycles of iron.