Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments

Abstract

Syntrophic interaction occurs during anaerobic fermentation of organic substances forming methane as the final product. H2 and formate are known to serve as the electron carriers in this process. Recently, it has been shown that direct interspecies electron transfer (DIET) occurs for syntrophic CH4 production from ethanol and acetate. Here, we constructed paddy soil enrichments to determine the involvement of DIET in syntrophic butyrate oxidation and CH4 production. The results showed that CH4 production was significantly accelerated in the presence of nanoFe3 O4 in all continuous transfers. This acceleration increased with the increase of nanoFe3 O4 concentration but was dismissed when Fe3 O4 was coated with silica that insulated the mineral from electrical conduction. NanoFe3 O4 particles were found closely attached to the cell surfaces of different morphology, thus bridging cell connections. Molecular approaches, including DNA-based stable isotope probing, revealed that the bacterial Syntrophomonadaceae and Geobacteraceae, and the archaeal Methanosarcinaceae, Methanocellales and Methanobacteriales, were involved in the syntrophic butyrate oxidation and CH4 production. Among them, the growth of Geobacteraceae strictly relied on the presence of nanoFe3 O4 and its electrical conductivity in particular. Other organisms, except Methanobacteriales, were present in enrichments regardless of nanoFe3 O4 amendment. Collectively, our study demonstrated that the nanoFe3 O4 -facilitated DIET occurred in syntrophic CH4 production from butyrate, and Geobacter species played the key role in this process in the paddy soil enrichments.

Enhancement of Fecal Sludge Conversion Into Biogas Using Iron Powder During Anaerobic Digestion Process

“…Otherwise, it is also found that in the digester D containing 3 g of iron powder biogas production considerably diminished compared to the digester B and C (Figure 3b). The same observation was noted by [30] then [24] in their study on the effect of zero valent iron nanoparticles (Fe 0 ) and magnetite (Fe 3 O 4 ) during anaerobic digestion of sewage sludge. It appeared that the concentration of iron powder which allows optimum biogas is comprised between 1.25 g and 2.5 g of Fe kg -1 fecal sludge.…”

Bioaugmentation of anaerobic sludge digestion with iron-reducing bacteria: process and microbial responses to variations in hydraulic retention time

“…Although not directly involved in the methanogenic pathway, IRBs can directly affect the overall AD performance because Fe (III) reduction and methanogenesis are in competition for the common substrates, acetate and hydrogen (Ahring 2003). In contrast, several recent studies have reported potential positive effects of IRB activity on biomethanation (Li et al 2014;Zhang et al 2010). Particularly, Kato et al (2012) reported that methanogenesis rates from acetate and ethanol were markedly increased by adding magnetite (crystalline conductive ferric oxide) in the enriched microbial cultures from rice paddy soil.…”

Secondary Mineralization of Ferrihydrite Affects Microbial Methanogenesis in Geobacter-Methanosarcina Cocultures

“…The competition between DIRB and methanogenic archaea for common electron donors such as acetate and H 2 has been postulated as the primary mechanism by which ferrihydrite inhibits methanogenesis (12)(13)(14)(15). However, (semi)conductive iron oxides, such as hematite or magnetite, can accelerate methanogenesis from acetate, ethanol (16,17), propionate (17,18), and butyrate (19). It has been proposed that the mechanism for the stimulation of methanogenesis involves direct interspecies electron transfer (DIET) between syntrophic oxidizers and methanogens via the conductive iron oxide minerals (16,18,19).…”

“…However, (semi)conductive iron oxides, such as hematite or magnetite, can accelerate methanogenesis from acetate, ethanol (16,17), propionate (17,18), and butyrate (19). It has been proposed that the mechanism for the stimulation of methanogenesis involves direct interspecies electron transfer (DIET) between syntrophic oxidizers and methanogens via the conductive iron oxide minerals (16,18,19). These findings imply that the methanogenic pathway may be corre-lated with the mineralogical properties of iron oxide, particularly its crystallinity and conductivity.…”