Putative Extracellular Electron Transfer in Methanogenic Archaea

Abstract

It has been suggested that a few methanogens are capable of extracellular electron transfers. For instance, Methanosarcina barkeri can directly capture electrons from the coexisting microbial cells of other species. Methanothrix harundinacea and Methanosarcina horonobensis retrieve electrons from Geobacter metallireducens via direct interspecies electron transfer (DIET). Recently, Methanobacterium, designated strain YSL, has been found to grow via DIET in the co-culture with Geobacter metallireducens. Methanosarcina acetivorans can perform anaerobic methane oxidation and respiratory growth relying on Fe(III) reduction through the extracellular electron transfer. Methanosarcina mazei is capable of electromethanogenesis under the conditions where electron-transfer mediators like H₂ or formate are limited. The membrane-bound multiheme c-type cytochromes (MHC) and electrically-conductive cellular appendages have been assumed to mediate the extracellular electron transfer in bacteria like Geobacter and Shewanella species. These molecules or structures are rare but have been recently identified in a few methanogens. Here, we review the current state of knowledge for the putative extracellular electron transfers in methanogens and highlight the opportunities and challenges for future research.

Keywords: archaellum; c-type cytochrome; direct electron transfer; direct interspecies electron transfer; extracellular electron transfer; methanogenic archaea.

Figure 1

Prediction model of direct electron uptake in Methanosarcina barkeri, cited (Holmes et al., 2018). The black arrows represent the possible transfers of electrons via F₄₂₀ and Fd. The red arrow represents the possible route for electron uptake from the outside. The unknown electron transfer proteins may gain 8 e^— from external sources and then channel these electrons via MP/MPH₂ to Fpo. Fpo can utilize F₄₂₀/F₄₂₀H₂ to deliver electrons to the process of CO₂ to CH₄.

Figure 2

Pathway proposed for Fe(III)-dependent respiratory pathway and CH₄ oxidation by Ms. acetivorans. (A) Fe(III)-dependent respiratory pathway on acetate, cited (Prakash et al., 2019a). (B) Fe(III)-dependent respiratory pathway on methanol with 2-bromoethanesulfonate (BES), cited (Holmes et al., 2019). (C) Fe(III)-dependent CH₄ oxidation, cited (Yan et al., 2018).

Figure 3

Enzyme-dependent external electron uptake in Methanococcus maripaludis, cited (Lienemann et al., 2018). Hydrogenase and formte dehydrogenase can be released from the living or dead cells of methanogens and then are absorbed on the cathode surface. These surface-associated enzymes can catalyze the formation of H₂ or formate, which was then rapidly consumed by M. maripaludis cells to produce CH₄ (Deutzmann et al., 2015).