Inhibitory Effects of Ferrihydrite on a Thermophilic Methanogenic Community

Yamada, Chihaya; Kato, Souichiro; Ueno, Yoshiyuki; Ishii, Masaharu; Igarashi, Yasuo

doi:10.1264/jsme2.me14026

Cited by 21 publications

(19 citation statements)

References 30 publications

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“…The amounts of reducing equivalents consumed by Fe(III) reduction were 37.5% of that expected from the observed decrease in CH 4 production in the ferrihydrite‐supplemented cultures, indicating that ferrihydrite‐dependent inhibition of methanogenesis was not completely due to the direct competition between Fe(III)‐reducing bacteria and methanogens for acetate. The diversion of electron flow from methanogenesis to ferrihydrite reduction by methanogens might contribute to the direct inhibition of methanogenesis by ferrrihydrite, which has been demonstrated in microbial communities [ Yamada et al ., ] and pure culture of methanogens [ Bond and Lovley , ; van Bodegom et al ., ; Liu et al ., ; Zhang et al ., ; Yamada et al ., ].…”

Section: Resultsmentioning

confidence: 99%

“…The main inhibitory mechanisms was proposed as Fe(III)‐reducing microorganisms reduce the levels of primary electron donors (acetate or hydrogen) available for methane production [ Achtnich et al ., ; Jäckel and Schnell , ; Qu et al ., ] and thus increase the contribution of Fe(III) reduction to anaerobic degradation of organic matter at the expense of methanogenesis. Furthermore, the increase in redox potential of the environments by the presence of Fe(III) oxides [ Fetzer and Conrad , ; Hirano et al ., ] and the diversion of electron flow from CO 2 reduction (methanogenesis) to Fe(III) reduction by methanogens capable of Fe(III) reduction [ Bond and Lovley , ; van Bodegom et al ., ; Liu et al ., ; Zhang et al ., ; Yamada et al ., , ] have been postulated as the direct inhibition of methanogenesis by Fe(III) oxides. Thus, ferric iron fertilization of rice paddies has been suggested as a potential option for mitigating methane emissions [ Jäckel et al ., ].…”

Section: Introductionmentioning

confidence: 99%

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

Tang

et al. 2015

J. Geophys. Res. Biogeosci.

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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.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Tang

et al. 2015

J. Geophys. Res. Biogeosci.

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“…It has been reported that washed cell suspension of certain hyperthermophilic methanogens has the ability to reduce soluble Fe(III) citrate (Vargas et al, 1998), while their ability to reduce insoluble Fe(III) minerals and the inhibitory effects of Fe(III) on their methanogenesis have not been investigated. Our group has recently reported the inhibitory effects of ferrihydrite on microbial communities obtained from a thermophilic anaerobic digester (Yamada et al, 2014). Additionally, Zhang et al (2013) has recently found the reduction of structural Fe(III) in smectite minerals by Methanothermobacter thermautotrophicus (hereafter Mtb.…”

Section: Introductionmentioning

confidence: 99%

Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens

Yamada

Kato

Kimura

et al. 2014

FEMS Microbiol Ecol

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Three thermophilic methanogens (Methanothermobacter thermautotrophicus, Methanosaeta thermophila, and Methanosarcina thermophila) were investigated for their ability to reduce poorly crystalline Fe(III) oxides (ferrihydrite) and the inhibitory effects of ferrihydrite on their methanogenesis. This study demonstrated that Fe(II) generation from ferrihydrite occurs in the cultures of the three thermophilic methanogens only when H2 was supplied as the source of reducing equivalents, even in the cultures of Mst. thermophila that do not grow on and produce CH4 from H2/CO2. While supplementation of ferrihydrite resulted in complete inhibition or suppression of methanogenesis by the thermophilic methanogens, ferrihydrite reduction by the methanogens at least partially alleviates the inhibitory effects. Microscopic and crystallographic analyses on the ferrihydrite-reducing Msr. thermophila cultures exhibited generation of magnetite on its cell surfaces through partial reduction of ferrihydrite. These findings suggest that at least certain thermophilic methanogens have the ability to extracellularly transfer electrons to insoluble Fe(III) compounds, affecting their methanogenic activities, which would in turn have significant impacts on materials and energy cycles in thermophilic anoxic environments.

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“…For example, a unique Bacteroidetes organism ( Proteiniphilum acetatigenes strain TB107) remarkably promotes syntrophic propionate degradation by Syntrophobacter and Methanobacterium (Chen and Dong, ). Extracellular electron transfer (EET) (or electric syntrophy) mediated by flagella/pili/cytochrome and conductive materials can be possible facilitative mechanism for methanogenesis in anaerobic bioreactors (Shimoyama et al ., ; Kato and Watanabe, ; Kato et al ., , ; Yamada et al ., ; Kato, ). The specific syntrophic associations we identified in full‐scale UASBs degrading industrial wastewater indicate the importance of characterizing microbial communities in commercially operated full‐scale wastewater treatment processes.…”

Section: Resultsmentioning

confidence: 98%

Co‐occurrence network analysis reveals thermodynamics‐driven microbial interactions in methanogenic bioreactors

Narihiro

Nobu

Bocher³

et al. 2018

Environ Microbiol Rep

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Methanogenic bioreactors have been applied to treat purified terephthalic acid (PTA) wastewater containing complex aromatic compounds, such as terephthalic acid, para-toluic acid and benzoic acid. This study characterized the interaction of microbial populations in 42 samples obtained from 10 PTA-degrading methanogenic bioreactors. Approximately, 54 dominant populations (11 methanogens, 8 syntrophs and 35 functionally unknown clades) that represented 73.9% of total 16S rRNA gene iTag sequence reads were identified. Co-occurrence analysis based on the abundance of dominant OTUs showed two non-overlapping networks centred around aromatic compound- (group AR: Syntrophorhabdaceae, Syntrophus and Pelotomaculum) and fatty acid- (group FA: Smithella and Syntrophobacter) degrading syntrophs. Group AR syntrophs have no direct correlation with hydrogenotrophic methanogens, while those from group FA do. As degradation of aromatic compounds has a wider thermodynamic window than fatty acids, Group AR syntrophs may be less influenced by fluctuations in hydrogenotrophic methanogen abundance or may non-specifically interact with diverse methanogens. In both groups, network analysis reveals full-scale- and lab-scale-specific uncultivated taxa that may mediate interactions between syntrophs and methanogens, suggesting that those uncultivated taxa may support the degradation of aromatic compounds through uncharted ecophysiological traits. These observations suggest that organisms from multiple niches orchestrate their metabolic capacity in multiple interaction networks to effectively degrade PTA wastewater.

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Inhibitory Effects of Ferrihydrite on a Thermophilic Methanogenic Community

Cited by 21 publications

References 30 publications

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

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

Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens

Co‐occurrence network analysis reveals thermodynamics‐driven microbial interactions in methanogenic bioreactors

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