Methanogenesis facilitated by electric syntrophy via (semi)conductive iron‐oxide minerals

Abstract

Methanogenesis is an essential part of the global carbon cycle and a key bioprocess for sustainable energy. Methanogenesis from organic matter is accomplished by syntrophic interactions among different species of microbes, in which interspecies electron transfer (IET) via diffusive carriers (e.g. hydrogen and formate) is known to be the bottleneck step. We report herein that the supplementation of soil microbes with (semi)conductive iron-oxide minerals creates unique interspecies interactions and facilitates methanogenesis. Methanogenic microbes were enriched from rice paddy field soil with either acetate or ethanol as a substrate in the absence or presence of (semi)conductive iron oxides (haematite or magnetite). We found that the supplementation with either of these iron oxides resulted in the acceleration of methanogenesis in terms of lag time and production rate, while the supplementation with an insulative iron oxide (ferrihydrite) did not. Clone-library analyses of 16S rRNA gene fragments PCR-amplified from the enrichment cultures revealed that the iron-oxide supplementation stimulated the growth of Geobacter spp. Furthermore, the addition of a specific inhibitor for methanogenesis suppressed the growth of Geobacter spp. These results suggest that Geobacter grew under syntrophic association with methanogens, and IET could occur via electric currents through (semi)conductive iron-oxide minerals (termed 'electric syntrophy'). Given the ubiquity of conductive minerals in nature, such energetic interactions may occur widely in soil and sediments and can be used to develop efficient bioenergy processes.

Extracellular Quinones Affecting Methane Production and Methanogenic Community in Paddy Soil

“…Syntrophic interaction between Geobacter and Methanosarcina through DIET might be conducted with conductive pilis or minerals [19,32]. The poor presence of Methanobacterium and the rich presence of Methanosarcina in methanogenesis-facilitated cultures (0.5-and 5-mM AQDS-supplemented cultures) were in good agreement with the distribution of methanogenic community involved in DI-ET from Geobacter to Methanosarcina through (semi)conductive iron oxides [19].…”

“…The genus Geobacter has been surprisingly discovered to be capable of forming highly conductive network of pilis that facilitate long-range electron transfer [34,38,39], which is becoming an important feature of Geobacter species in anaerobic environments [17,26,27]. There is increasing evidence that Geobacter species are important syntrophic microorganisms capable of establishing syntrophic association with methanogens [19,29,45]. Recent study demonstrated the possibility of direct interspecies electron transfer (DIET) between Geobacter species and Methanosaeta concilii within upflow anaerobic sludge blanket reactor methanogenic aggregates, which were electrically conductive largely contributed by Geobacter species [32].…”

“…Recent study demonstrated the possibility of direct interspecies electron transfer (DIET) between Geobacter species and Methanosaeta concilii within upflow anaerobic sludge blanket reactor methanogenic aggregates, which were electrically conductive largely contributed by Geobacter species [32]. Using rice paddy soil as microbial inocula, Kato et al [19] reported the syntrophic association between Geobacter and Methanosarcina in the presence of hematite and magnetite; methanogenesis was facilitated via DIET through (semi) conductive iron oxides. In this study, Methanosarcina and Methanobacterium are detected as the most abundant methanogens in the soil cultures, similar to other rice paddy soils [9,29,52].…”

“…DIET from syntrophic bacteria to methanogens was considered to be more effective than the use of hydrogen or formate as an intermediary electron carrier for methanogenesis [25,46]. Methanosarcina species are capable of extracellular electron acceptors to reduce extracellular quinones, humic acids, and Fe(III) oxides [3,50], and have been reported to be syntrophic partners of Geobacter species for converting acetate to CH 4 via DIET [19]. In the 0.5-and 5-mM AQDS treatments, enriched Geobacter oxidized acetate to CO 2 and methanogenesis was the main electron accepting processes after AQDS depletion.…”

“…MspI was used as a restriction enzyme to screen mcrA clones with T-RFLP analyses; only major TRFs are shown. T-RFs of 164, 173, and, 213 bp are representative of Methanosarcina; a T-RF of 484 bp is representative of Methanobacterium; The T-RF peaks at 150, 466, and 569 bp could not be assigned since these T-RFs did not have sequences matched in the clone library interaction with Geobacter and conducted hydrogenotrophic methanogenesis (CO 2 reduction to CH 4 ) [19]. In the supplementary experiment, the addition of 5 mM BES should not affect the growth of Geobacter if it was not associated with methanogenesis.…”