NanoFe3O4 as Solid Electron Shuttles to Accelerate Acetotrophic Methanogenesis by Methanosarcina barkeri

Abstract

Magnetite nanoparticles (nanoFe3O4) have been reported to facilitate direct interspecies electron transfer (DIET) between syntrophic bacteria and methanogens thereby improving syntrophic methanogenesis. However, whether or how nanoFe3O4 affects acetotrophic methanogenesis remain unknown. Herein, we demonstrate the unique role of nanoFe3O4 in accelerating methane production from direct acetotrophic methanogenesis in Methanosarcina-enriched cultures, which was further confirmed by pure cultures of Methanosarcina barkeri. Compared with other nanomaterials of higher electrical conductivity such as carbon nanotubes and graphite, nanoFe3O4 with mixed valence Fe(II) and Fe(III) had the most significant stimulatory effect on methane production, suggesting its redox activity rather than electrical conductivity led to enhanced methanogenesis by M. barkeri. Cell morphology and spectroscopy analysis revealed that nanoFe3O4 penetrated into the cell membrane and cytoplasm of M. barkeri. These results provide the unprecedented possibility that nanoFe3O4 in the cell membrane of methanogens serve as electron shuttles to facilitate intracellular electron transfer and thus enhance methane production. This work has important implications not only for understanding the mechanisms of mineral-methanogen interaction but also for optimizing engineered methanogenic processes.

Methane production by acetate dismutation stimulated by Shewanella oneidensis and carbon materials: An alternative to classical CO2 reduction

“…For instance, S. oneidensis MR-1 increased methane production only by 5% after 6 days of incubation with CH 3 F, whereas the increase reached 22.5% without CH 3 F. Calculations shows that acetoclastic methanogenesis accounted for 70-80% of produced methane, and, conversely, CO 2 reduction accounted for only 20-30% of produced methane (Table 1). Our findings are supported by pure culture and metatranscriptomic data showing that Fe 3 O 4 nanoparticles act as electron shuttles to stimulate acetoclastic methanogenesis [20,21]. However, for this study and the two studies mentioned above [20,21], the experiments were performed with acetate as the sole carbon source.…”

“…are not always detected in improved methane production systems [19]. Two recent studies suggested that conductive magnetite accelerates acetoclastic methanogenesis [20,21]. First, Fu et al showed that nanoFe 3 O 4 acts as solid electron shuttles to accelerate acetoclastic methanogenesis by Methanosarcina barkeri in pure cultures [20].…”

“…Two recent studies suggested that conductive magnetite accelerates acetoclastic methanogenesis [20,21]. First, Fu et al showed that nanoFe 3 O 4 acts as solid electron shuttles to accelerate acetoclastic methanogenesis by Methanosarcina barkeri in pure cultures [20]. Second, Inaba et al provided metatranscriptomic evidence for stimulated acetoclastic methanogenesis by magnetite nanoparticle under continuous agitation [21].…”

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

“…Due to the small difference in redox potentials of these components, it has been proposed that an electrically quantized membrane is important to solidify electron flow efficiency and prevent from thermodynamic dissipation (Duszenko and Buan, ). Accordingly, it has been suggested that the penetration of magnetite nanoparticles into Methanosarcina membrane and entering the cell cytoplasm enhanced the membrane electric quantization and hence the methanogenesis in Methanosarcina (Fu et al ., ). It is unlikely, however, that the penetration of exogenous nanoparticles will not cause a disturbance on cell interior integrity (John et al ., ).…”

Addressing Nanomaterial Immunosafety by Evaluating Innate Immunity across Living Species

“…The interaction between NM and microorganisms is significant, and it is at the basis of an emerging discipline dubbed nanomicrobiology. It is notable that microorganisms naturally synthesize NP as a mechanism to detoxify their environment from toxic elements, normally heavy metals, [167] or use them as electrodes to assist direct interspecies electron transfer [168] or as reservoirs to release with molecular precision some essential elements (upon NM dissolution) at the site of action, for instance bactericidal ions (Ag + ) [169] or pro-proliferating ones (Fe 2+ ). [170] The NM size and water solubility allow them to finely integrate into the biological machinery.…”