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Conductive Fe3O4 Nanoparticles Accelerate Syntrophic Methane Production from Butyrate Oxidation in Two Different Lake Sediments.

ABSTRACT: Syntrophic methanogenesis is an essential link in the global carbon cycle and a key bioprocess for the disposal of organic waste and production of biogas. Recent studies suggest direct interspecies electron transfer (DIET) is involved in electron exchange in methanogenesis occurring in paddy soils, anaerobic digesters, and specific co-cultures with Geobacter. In this study, we evaluate the possible involvement of DIET in the syntrophic oxidation of butyrate in the enrichments from two lake sediments (an urban lake and a natural lake). The results showed that the production of CH4 was significantly accelerated in the presence of conductive nanoscale Fe3O4 or carbon nanotubes in the sediment enrichments. Observations made with fluorescence in situ hybridization and scanning electron microscope indicated that microbial aggregates were formed in the enrichments. It appeared that the average cell-to-cell distance in aggregates in nanomaterial-amended enrichments was larger than that in aggregates in the non-amended control. These results suggested that DIET-mediated syntrophic methanogenesis could occur in the lake sediments in the presence of conductive materials. Microbial community analysis of the enrichments revealed that the genera of Syntrophomonas, Sulfurospirillum, Methanosarcina, and Methanoregula were responsible for syntrophic oxidation of butyrate in lake sediment samples. The mechanism for the conductive-material-facilitated DIET in butyrate syntrophy deserves further investigation.

SUBMITTER: Zhang J

PROVIDER: S-EPMC4992681 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Conductive Fe3O4 Nanoparticles Accelerate Syntrophic Methane Production from Butyrate Oxidation in Two Different Lake Sediments.

Zhang Jianchao J Lu Yahai Y

Frontiers in microbiology 20160822

Syntrophic methanogenesis is an essential link in the global carbon cycle and a key bioprocess for the disposal of organic waste and production of biogas. Recent studies suggest direct interspecies electron transfer (DIET) is involved in electron exchange in methanogenesis occurring in paddy soils, anaerobic digesters, and specific co-cultures with Geobacter. In this study, we evaluate the possible involvement of DIET in the syntrophic oxidation of butyrate in the enrichments from two lake sedim ...[more]

PMID: 27597850

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Project description:Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure, and their survival depends on successful partnership. Here, we demonstrate that conductive particles enable the partnership between SAO bacteria (i.e., Geobacter spp.) and methanogens (Methanosarcina spp.) from the coastal sediments of the Bothnian Bay of the Baltic Sea. Baltic methanogenic sediments were rich in conductive minerals, had an apparent isotopic fractionation characteristic of CO2-reductive methanogenesis, and were inhabited by Geobacter and Methanosarcina As long as conductive particles were delivered, Geobacter and Methanosarcina persisted, whereas exclusion of conductive particles led to the extinction of Geobacter Baltic Geobacter did not establish a direct electric contact with Methanosarcina, necessitating conductive particles as electrical conduits. Within SAO consortia, Geobacter was an efficient [13C]acetate utilizer, accounting for 82% of the assimilation and 27% of the breakdown of acetate. Geobacter benefits from the association with the methanogen, because in the absence of an electron acceptor it can use Methanosarcina as a terminal electron sink. Consequently, inhibition of methanogenesis constrained the SAO activity of Geobacter as well. A potential benefit for Methanosarcina partnering with Geobacter is that together they competitively exclude acetoclastic methanogens like Methanothrix from an environment rich in conductive particles. Conductive particle-mediated SAO could explain the abundance of acetate oxidizers like Geobacter in the methanogenic zone of sediments where no electron acceptors other than CO2 are available.IMPORTANCE Acetate-oxidizing bacteria are known to thrive in mutualistic consortia in which H2 or formate is shuttled to a methane-producing Archaea partner. Here, we discovered that such bacteria could instead transfer electrons via conductive minerals. Mineral SAO (syntrophic acetate oxidation) could be a vital pathway for CO2-reductive methanogenesis in the environment, especially in sediments rich in conductive minerals. Mineral-facilitated SAO is therefore of potential importance for both iron and methane cycles in sediments and soils. Additionally, our observations imply that agricultural runoff or amendments with conductive chars could trigger a significant increase in methane emissions.

Project description:In syntrophic conversion of butyrate to methane and CO2, butyrate is oxidized to acetate by secondary fermenting bacteria such as Syntrophomonas wolfei in close cooperation with methanogenic partner organisms, e.g., Methanospirillum hungatei. This process involves an energetically unfavourable shift of electrons from the level of butyryl-CoA oxidation to the substantially lower redox potential of proton and/or CO2 reduction, in order to transfer these electrons to the methanogenic partner via hydrogen and/or formate. In the present study, all prominent membrane-bound and soluble proteins expressed in S. wolfei specifically during syntrophic growth with butyrate, in comparison to pure-culture growth with crotonate, were examined by one- and two-dimensional gel electrophoresis, and identified by peptide fingerprinting-mass spectrometry. A membrane-bound, externally oriented, quinone-linked formate dehydrogenase complex was expressed at high level specifically during syntrophic butyrate oxidation, comprising a selenocystein-linked catalytic subunit with a membrane-translocation pathway signal (TAT), a membrane-bound iron-sulfur subunit, and a membrane-bound cytochrome. Soluble hydrogenases were expressed at high levels specifically during growth with crotonate. The results were confirmed by native protein gel electrophoresis, by formate dehydrogenase and hydrogenase-activity staining, and by analysis of formate dehydrogenase and hydrogenase activities in intact cells and cell extracts. Furthermore, constitutive expression of a membrane-bound, internally oriented iron-sulfur oxidoreductase (DUF224) was confirmed, together with expression of soluble electron-transfer flavoproteins (EtfAB) and two previously identified butyryl-CoA dehydrogenases. Our findings allow to depict an electron flow scheme for syntrophic butyrate oxidation in S. wolfei. Electrons derived from butyryl-CoA are transferred through a membrane-bound EtfAB:quinone oxidoreductase (DUF224) to a menaquinone cycle and further via a b-type cytochrome to an externally oriented formate dehydrogenase. Hence, an ATP hydrolysis-driven proton-motive force across the cytoplasmatic membrane would provide the energy input for the electron potential shift necessary for formate formation.

Dataset Information

Conductive Fe3O4 Nanoparticles Accelerate Syntrophic Methane Production from Butyrate Oxidation in Two Different Lake Sediments.

Publications

Conductive Fe3O4 Nanoparticles Accelerate Syntrophic Methane Production from Butyrate Oxidation in Two Different Lake Sediments.

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