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Acetate oxidation by syntrophic association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen.

ABSTRACT: Anodic microbial communities in acetate-fed microbial fuel cells (MFCs) were analyzed using stable-isotope probing of 16S rRNA genes followed by denaturing gradient gel electrophoresis. The results revealed that Geobacter sulfurreducens and Hydrogenophaga sp. predominated in the anodic biofilm. Although the predominance of Geobacter sp. as acetoclastic exoelectrogens in acetate-fed MFC systems has been often reported, the ecophysiological role of Hydrogenophaga sp. is unknown. Therefore, we isolated and characterized a bacterium closely related to Hydrogenophaga sp. (designated strain AR20). The newly isolated strain AR20 could use molecular hydrogen (H2), but not acetate, with carbon electrode as the electron acceptor, indicating that the strain AR20 was a hydrogenotrophic exoelectrogen. This evidence raises a hypothesis that acetate was oxidized by G. sulfurreducens in syntrophic cooperation with the strain AR20 as a hydrogen-consuming partner in the acetate-fed MFC. To prove this hypothesis, G. sulfurreducens strain PCA was cocultivated with the strain AR20 in the acetate-fed MFC without any dissolved electron acceptors. In the coculture MFC of G. sulfurreducens and strain AR20, current generation and acetate degradation were the highest, and the growth of strain AR20 was observed. No current generation, acetate degradation and cell growth occurred in the strain AR20 pure culture MFC. These results show for the first time that G. sulfurreducens can oxidize acetate in syntrophic cooperation with the isolated Hydrogenophaga sp. strain AR20, with electrode as the electron acceptor.

SUBMITTER: Kimura Z

PROVIDER: S-EPMC3721111 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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Acetate oxidation by syntrophic association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen.

Kimura Zen-ichiro Z Okabe Satoshi S

The ISME journal 20130314 8

Anodic microbial communities in acetate-fed microbial fuel cells (MFCs) were analyzed using stable-isotope probing of 16S rRNA genes followed by denaturing gradient gel electrophoresis. The results revealed that Geobacter sulfurreducens and Hydrogenophaga sp. predominated in the anodic biofilm. Although the predominance of Geobacter sp. as acetoclastic exoelectrogens in acetate-fed MFC systems has been often reported, the ecophysiological role of Hydrogenophaga sp. is unknown. Therefore, we isol ...[more]

PMID: 23486252

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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:Biomineralization of Cu has been shown to control contaminant dynamics and transport in soils. However, very little is known about the role that subsurface microorganisms may play in the biogeochemical cycling of Cu. In this study, we investigate the bioreduction of Cu(II) by the subsurface metal-reducing bacterium Geobacter sulfurreducens Rapid removal of Cu from solution was observed in cell suspensions of G. sulfurreducens when Cu(II) was supplied, while transmission electron microscopy (TEM) analyses showed the formation of electron-dense nanoparticles associated with the cell surface. Energy-dispersive X-ray spectroscopy (EDX) point analysis and EDX spectrum image maps revealed that the nanoparticles are rich in both Cu and S. This finding was confirmed by X-ray absorption near-edge structure (XANES) and extended X-ray absorption fine structure (EXAFS) analyses, which identified the nanoparticles as Cu2S. Biomineralization of CuxS nanoparticles in soils has been reported to enhance the colloidal transport of a number of contaminants, including Pb, Cd, and Hg. However, formation of these CuxS nanoparticles has only been observed under sulfate-reducing conditions and could not be repeated using isolates of implicated organisms. As G. sulfurreducens is unable to respire sulfate, and no reducible sulfur was supplied to the cells, these data suggest a novel mechanism for the biomineralization of Cu2S under anoxic conditions. The implications of these findings for the biogeochemical cycling of Cu and other metals as well as the green production of Cu catalysts are discussed.IMPORTANCE Dissimilatory metal-reducing bacteria are ubiquitous in soils and aquifers and are known to utilize a wide range of metals as terminal electron acceptors. These transformations play an important role in the biogeochemical cycling of metals in pristine and contaminated environments and can be harnessed for bioremediation and metal bioprocessing purposes. However, relatively little is known about their interactions with Cu. As a trace element that becomes toxic in excess, Cu can adversely affect soil biota and fertility. In addition, biomineralization of Cu nanoparticles has been reported to enhance the mobilization of other toxic metals. Here, we demonstrate that when supplied with acetate under anoxic conditions, the model metal-reducing bacterium Geobacter sulfurreducens can transform soluble Cu(II) to Cu2S nanoparticles. This study provides new insights into Cu biomineralization by microorganisms and suggests that contaminant mobilization enhanced by Cu biomineralization could be facilitated by Geobacter species and related organisms.

Dataset Information

Acetate oxidation by syntrophic association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen.

Publications

Acetate oxidation by syntrophic association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen.

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