Extracellular electron transfer through microbial reduction of solid-phase humic substances

Roden, Eric E.; Kappler, Andreas; Bauer, Iris; Jiang, Jie; Paul, Andrea; Stoêsser, R.; Konishi, Hiromi; Xu, Huifang

doi:10.1038/ngeo870

Cited by 424 publications

(315 citation statements)

References 29 publications

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“…Humic acids should therefore be more effective in electron shuttling than natural soil organic matter. Previous studies have shown that the presence of dissolved humic acids leads to complexation of Fe(II) (Royer et al, 2002), and complexation and dissolution of Fe(III) (Jones et al, 2009), but also potentially enhance Fe(III) reduction via electron shuttling (Hansel et al, 2004;Jiang and Kappler, 2008;Lovley et al, 1996;Roden et al, 2010). Furthermore, the concentrations of dissolved humic acid or the mineral / humic acid ratios have been shown by some studies to increase Fe(III) reduction rates while other studies have not reproduced this result (Amstaetter et al, 2012;Jiang and Kappler, 2008).…”

Section: Introductionmentioning

confidence: 80%

Ferrihydrite-associated organic matter (OM) stimulates reduction by Shewanella oneidensis MR-1 and a complex microbial consortia

et al. 2017

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Abstract. The formation of Fe(III) oxides in natural environments occurs in the presence of natural organic matter (OM), resulting in the formation of OM-mineral complexes that form through adsorption or coprecipitation processes. Thus, microbial Fe(III) reduction in natural environments most often occurs in the presence of OM-mineral complexes rather than pure Fe(III) minerals. This study investigated to what extent does the content of adsorbed or coprecipitated OM on ferrihydrite influence the rate of Fe(III) reduction by Shewanella oneidensis MR-1, a model Fe(III)-reducing microorganism, in comparison to a microbial consortium extracted from the acidic, Fe-rich Schlöppnerbrunnen fen. We found that increased OM content led to increased rates of microbial Fe(III) reduction by S. oneidensis MR-1 in contrast to earlier findings with the model organism Geobacter bremensis. Ferrihydrite-OM coprecipitates were reduced slightly faster than ferrihydrites with adsorbed OM. Surprisingly, the complex microbial consortia stimulated by a mixture of electrons donors (lactate, acetate, and glucose) mimics S. oneidensis under the same experimental Fe(III)-reducing conditions suggesting similar mechanisms of electron transfer whether or not the OM is adsorbed or coprecipitated to the mineral surfaces. We also followed potential shifts of the microbial community during the incubation via 16S rRNA gene sequence analyses to determine variations due to the presence of adsorbed or coprecipitated OM-ferrihydrite complexes in contrast to pure ferrihydrite. Community profile analyses showed no enrichment of typical model Fe(III)-reducing bacteria, such as Shewanella or Geobacter sp., but an enrichment of fermenters (e.g., Enterobacteria) during pure ferrihydrite incubations which are known to use Fe(III) as an electron sink. Instead, OM-mineral complexes favored the enrichment of microbes including Desulfobacteria and Pelosinus sp., both of which can utilize lactate and acetate as an electron donor under Fe(III)-reducing conditions. In summary, this study shows that increasing concentrations of OM in OM-mineral complexes determines microbial Fe(III) reduction rates and shapes the microbial community structure involved in the reductive dissolution of ferrihydrite. Similarities observed between the complex Fe(III)-reducing microbial consortia and the model Fe(III)-reducer S. oneidensis MR-1 suggest electron-shuttling mechanisms dominate in OM-rich environments, including soils, sediments, and fens, where natural OM interacts with Fe(III) oxides during mineral formation.

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Section: Introductionmentioning

confidence: 80%

Ferrihydrite-associated organic matter (OM) stimulates reduction by Shewanella oneidensis MR-1 and a complex microbial consortia

et al. 2017

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“…Microbial reduction of humics coupled to organic matter oxidation was first demonstrated by Lovley et al [28], and a number of bacteria capable of utilizing humics as TEA were isolated from natural wetlands [10]. More recently, Roden et al [40] reported microbial reduction of solid-phase humics by iron-reducing bacteria in wetlands. Respiration with humics provides more energy than methanogenesis, and is able to competitively suppress CH 4 production [8].…”

Section: Introductionmentioning

confidence: 99%

Extracellular Quinones Affecting Methane Production and Methanogenic Community in Paddy Soil

Yang

et al. 2013

Microb Ecol

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This study investigated the change of CH 4 production and methanogenic community in response to the presence of humic substances (humics) analogue, anthraquinone-2,6-disulfonate (AQDS). Anaerobic experiments used a Chinese paddy soil, and three concentration levels of 0.5, 5, and 20 mM AQDS were conducted. Results suggested that the effect of AQDS on methanogenesis was time-dependent and concentration-dependent. Twenty millimolars of AQDS was toxic for methanogenic activity almost for the entire experimental period. Slight inhibition of methanogenesis by AQDS respiration in the 0.5-and 5-mM AQDS-supplemented treatments occurred within the early period, while CH 4 accumulated throughout the later period was approximately five and ten times greater than that of the controls without AQDS, respectively. AQDS reduction coupling to acetate oxidization enriched Geobacter species, and the mcrA-targeted T-RFLP profiles revealed significant increase of Methanosarcina at the expense of Methanobacterium in the 0.5-and 5-mM AQDS treatments. The enriched syntrophic association between Geobacter and Methanosarcina was deduced to be an effective methanogenic pathway for converting acetate to CH 4 via direct interspecies electron transfer. This study implied the ecological importance of syntrophic interaction between methanogens and microorganisms enriched by anaerobic respiration of non-methanogenic terminal electron acceptors in paddy soils.

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“…It was suggested that they may enhance Fe(III) reduction by electron shuttling (Lovley et al, 1996;Hansel et al, 2004;Jiang and Kappler, 2008;Roden et al, 2010), complexation of Fe(II) (Royer et al, 2002), or complexation and dissolution of Fe(III) (Jones et al, 2009). Amstaetter et al (2012) and Jiang and Kappler (2008) observed that the concentration of humic acid or the mineral / humic acid ratio may control whether humic acids increase reduction or not.…”

Section: K Eusterhues Et Al: Fh-associated Om Inhibits Fe(iii) Redumentioning

confidence: 99%

Reduction of ferrihydrite with adsorbed and coprecipitated organic matter: microbial reduction by Geobacter bremensis vs. abiotic reduction by Na-dithionite

et al. 2014

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Abstract. Ferrihydrite is a widespread poorly crystalline Fe oxide which becomes easily coated by natural organic matter in the environment. This mineral-bound organic matter entirely changes the mineral surface properties and therefore the reactivity of the original mineral. Here, we investigated 2-line ferrihydrite, ferrihydrite with adsorbed organic matter, and ferrihydrite coprecipitated with organic matter for microbial and abiotic reduction of Fe(III). Ferrihydrite-organic matter associations with different organic matter loadings were reduced either by Geobacter bremensis or abiotically by Na-dithionite. Both types of experiments showed decreasing initial Fe-reduction rates and decreasing degrees of reduction with increasing amounts of mineral-bound organic matter. At similar organic matter loadings, coprecipitated ferrihydrites were more reactive than ferrihydrites with adsorbed organic matter. The difference can be explained by the smaller crystal size and poor crystallinity of such coprecipitates. At small organic matter loadings the poor crystallinity of coprecipitates led to even faster Fe-reduction rates than found for pure ferrihydrite. The amount of mineral-bound organic matter also affected the formation of secondary minerals: goethite was only found after reduction of organic matter-free ferrihydrite and siderite was only detected when ferrihydrites with relatively low amounts of mineral-bound organic matter were reduced. We conclude that direct contact of G. bremensis to the Fe oxide mineral surface was inhibited by attached organic matter. Consequently, mineral-bound organic matter shall be taken into account as a factor in slowing down reductive dissolution.

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Extracellular electron transfer through microbial reduction of solid-phase humic substances

Cited by 424 publications

References 29 publications

Ferrihydrite-associated organic matter (OM) stimulates reduction by <i>Shewanella oneidensis</i> MR-1 and a complex microbial consortia

Ferrihydrite-associated organic matter (OM) stimulates reduction by <i>Shewanella oneidensis</i> MR-1 and a complex microbial consortia

Extracellular Quinones Affecting Methane Production and Methanogenic Community in Paddy Soil

Reduction of ferrihydrite with adsorbed and coprecipitated organic matter: microbial reduction by <i>Geobacter bremensis</i> vs. abiotic reduction by Na-dithionite

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Extracellular electron transfer through microbial reduction of solid-phase humic substances

Cited by 424 publications

References 29 publications

Ferrihydrite-associated organic matter (OM) stimulates reduction by &lt;i&gt;Shewanella oneidensis&lt;/i&gt; MR-1 and a complex microbial consortia

Ferrihydrite-associated organic matter (OM) stimulates reduction by &lt;i&gt;Shewanella oneidensis&lt;/i&gt; MR-1 and a complex microbial consortia

Extracellular Quinones Affecting Methane Production and Methanogenic Community in Paddy Soil

Reduction of ferrihydrite with adsorbed and coprecipitated organic matter: microbial reduction by &lt;i&gt;Geobacter bremensis&lt;/i&gt; vs. abiotic reduction by Na-dithionite

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Ferrihydrite-associated organic matter (OM) stimulates reduction by <i>Shewanella oneidensis</i> MR-1 and a complex microbial consortia

Ferrihydrite-associated organic matter (OM) stimulates reduction by <i>Shewanella oneidensis</i> MR-1 and a complex microbial consortia

Reduction of ferrihydrite with adsorbed and coprecipitated organic matter: microbial reduction by <i>Geobacter bremensis</i> vs. abiotic reduction by Na-dithionite