Effect of ferrihydrite biomineralization on methanogenesis in an anaerobic incubation from paddy soil

Abstract

Microbial reduction of Fe(III) can be one of the major factors controlling methane production from anaerobic sedimentary environments, such as paddy soils and wetlands. Although secondary iron mineralization following Fe(III) reduction is a process that occurs naturally over time, it has not yet been considered in methanogenic systems. This study performed a long-term anaerobic incubation of a paddy soil and ferrihydrite-supplemented soil cultures to investigate methanogenesis during ferrihydrite biomineralization. The results revealed that the long-term effect of ferrihydrite on methanogenesis may be enhancement rather than suppression documented in previous studies. During initial microbial ferrihydrite reduction, methanogenesis was suppressed; however, the secondary minerals of magnetite formation was simultaneous with facilitated methanogenesis in terms of average methane production rate and acetate utilization rate. In the phase of magnetite formation, microbial community analysis revealed a strong stimulation of the bacterial Geobacter, Bacillus, and Sedimentibacter and the archaeal Methanosarcina in the ferrihydrite-supplemented cultures. Direct electric syntrophy between Geobacter and Methanosarcina via conductive magnetite is the plausible mechanism for methanogenesis acceleration along with magnetite formation. Our data suggested that a change in iron mineralogy might affect the conversion of anaerobic organic matter to methane and might provide a fresh perspective on the mitigation of methane emissions from paddy soils by ferric iron fertilization.

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

“…Although syntrophy is not necessary in the cocultures of G. sulfurreducens and M. barkeri to metabolize acetate to CH 4 , magnetite-accelerated methanogenesis from acetate has been observed under mesophilic and thermophilic conditions (16,17,20,40). Based on the advantage of Geobacter species utilizing acetate over acetoclastic methanogens (15), it was proposed that Geobacter oxidized acetate to CO 2 and that electrons were transferred via magnetite-mediated DIET to methanogens to reduce CO 2 to CH 4 (16,20,40).…”

“…Based on the advantage of Geobacter species utilizing acetate over acetoclastic methanogens (15), it was proposed that Geobacter oxidized acetate to CO 2 and that electrons were transferred via magnetite-mediated DIET to methanogens to reduce CO 2 to CH 4 (16,20,40). The growth of Geobacter in the presence of magnetite was dependent on methanogenesis, which demonstrated the syntrophic association between Geobacter and methanogens (16,40).…”

“…To address this question, we previously conducted long-term anaerobic incubation of paddy soil and ferrihydrite-supplemented soil cultures to investigate how secondary mineral products of ferrihydrite reduction affect methanogenesis; the results showed that microbial magnetite formation was correlated with facilitated methanogenesis, in terms of the average methane production rate and the acetate degradation rate (20). However, the association between the promotion of methanogenesis and magnetite formation is very speculative, due to the complexity of the soil system.…”

Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture

“…Interestingly, it appears that conductive materials, including graphite particles (Kato et al ., ; Zhao et al ., ), granular activated carbon (Liu et al ., ; Rotaru et al ., ; Xu et al ., ; Dang et al ., ; Lee et al ., ), biochar (Chen et al ., ; Zhao et al ., ), graphene (Tian et al ., ), carbon nanotubes (CNT) (Li et al ., ; Zhang and Lu, ), carbon felt (Xu et al ., ) and carbon cloth (Chen et al ., ; Zhao et al ., ; Lei et al ., ), but also iron oxides as magnetite (Kato et al ., ; Cruz Viggi et al ., ; Baek et al ., ; Zhuang et al ., ; Yamada et al ., ; Tang et al ., ; Yang et al ., ; Yin et al ., ; Zhang and Lu, ; Jing et al ., ) may increase the rate of electron transfer and may affect metabolic pathways in anaerobic microbial processes by promoting DIET, between bacteria and methanogens. In general, these materials are highly stable, have large surface area, good adsorption capacity and high electric conductivity (Figueiredo et al ., ; Van der Zee and Cervantes, ; Pereira et al ., ).…”

Magnetite accelerates syntrophic acetate oxidation in methanogenic systems with high ammonia concentrations

“…Conductive iron minerals (Kato et al ., ; Viggi et al ., ; Li et al ., ; Yamada et al ., ; Zhuang et al ., ) and conductive carbon materials such as activated carbon (Liu et al ., ), biochar (Chen et al ., 2014a) and carbon cloth (Chen et al ., 2014b) have been demonstrated to accelerate methanogenesis, in which these conductive materials mediate direct interspecies electron transfer (DIET) in syntrophic consortia. Kato et al .…”