Manganese/iron-supported sulfate-dependent anaerobic oxidation of methane by archaea in lake sediments

Su, Guangyi; Zopfi, Jakob; Yao, Haoyi; Steinle, Lea; Niemann, Helge; Lehmann, Moritz F.

doi:10.1101/636621

Cited by 11 publications

(16 citation statements)

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“…In addition, sulfaterich environments could support S-dAOM mediated by Methanoperedens archaea, with the possible involvement of iron +3 or manganese +4 according to geochemical evidence and the detection of these archaea in sulfate-rich freshwater lake Cadagno (Schubert et al, 2011). A follow-up study proposed S-dAOM to be carried out by M. nitroreducens in a consortium with Desulfobulbaceae (Su et al, 2020). The debate whether metal oxides alone can be used as electron acceptors or serve a stimulatory role to support S-dAOM, persists since no genome of the Methanoperedens archaea known to date, contains dissimilatory sulfate reductases (Leu et al, 2020b).…”

Section: Environmental Studiesmentioning

confidence: 98%

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

et al. 2021

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Methane is the final product of the anaerobic decomposition of organic matter. The conversion of organic matter to methane (methanogenesis) as a mechanism for energy conservation is exclusively attributed to the archaeal domain. Methane is oxidized by methanotrophic microorganisms using oxygen or alternative terminal electron acceptors. Aerobic methanotrophic bacteria belong to the phyla Proteobacteria and Verrucomicrobia, while anaerobic methane oxidation is also mediated by more recently discovered anaerobic methanotrophs with representatives in both the bacteria and the archaea domains. The anaerobic oxidation of methane is coupled to the reduction of nitrate, nitrite, iron, manganese, sulfate, and organic electron acceptors (e.g., humic substances) as terminal electron acceptors. This review highlights the relevance of methanotrophy in natural and anthropogenically influenced ecosystems, emphasizing the environmental conditions, distribution, function, co-existence, interactions, and the availability of electron acceptors that likely play a key role in regulating their function. A systematic overview of key aspects of ecology, physiology, metabolism, and genomics is crucial to understand the contribution of methanotrophs in the mitigation of methane efflux to the atmosphere. We give significance to the processes under microaerophilic and anaerobic conditions for both aerobic and anaerobic methane oxidizers. In the context of anthropogenically influenced ecosystems, we emphasize the current and potential future applications of methanotrophs from two different angles, namely methane mitigation in wastewater treatment through the application of anaerobic methanotrophs, and the biotechnological applications of aerobic methanotrophs in resource recovery from methane waste streams. Finally, we identify knowledge gaps that may lead to opportunities to harness further the biotechnological benefits of methanotrophs in methane mitigation and for the production of valuable bioproducts enabling a bio-based and circular economy.

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Section: Environmental Studiesmentioning

confidence: 98%

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

et al. 2021

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“…Direct anaerobic CH 4 oxidation via Mn‐oxides as electron acceptors might be quantitatively significant but subordinated to the anaerobic CH 4 oxidation via SO 4 2− due to the dominance of SO 4 2− reduction in the sediments of Lake Willersinnweiher. However, it is more likely that Mn supports sedimentary anaerobic CH 4 oxidation via SO 4 2− through re‐oxidation of reduced S species, as it was also recently described for Lake Cadagno (Su et al 2019).…”

Section: Discussionmentioning

confidence: 55%

The impact of seasonal sulfate–methane transition zones on methane cycling in a sulfate‐enriched freshwater environment

Kleint

Wellach

Schroll

et al. 2021

Limnology & Oceanography

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Lake Willersinnweiher located in south-western Germany is a small eutrophic gravel pit lake fed by sulfateenriched groundwater. The aim of this study was to investigate the total methane (CH 4 ) mass balance of Lake Willersinnweiher with a particular focus on the interaction of carbon and sulfur cycling within the lake sediments and the redoxcline of the water column. Our results show that Lake Willersinnweiher permanently releases CH 4 to the atmosphere throughout the whole year 2018 at rates ranging from 5 to 120 mol d −1 . Sediment data show the presence of intense anaerobic oxidation of CH 4 in the upper sediment layers during early summer. Here, CH 4 is most likely consumed via sulfate in sulfate-methane transition zones (SMTZs) that have been observed for a few specific freshwater environments only. Seasonal dynamics in biogeochemical processes trigger the non-steady state conditions within the sediments and the CH 4 consumption in the SMTZs. In parallel, CH 4 released from the sediments is completely consumed by aerobic oxidation processes in the redoxcline indicated by minimum CH 4 concentrations with high δ 13 C-CH 4 values. This zone acts as an effective barrier, minimizing CH 4 release into the surface water and the atmosphere and thus CH 4 oversaturation along with near-atmospheric isotopic composition indicate the presence of an additional CH 4 source in the epilimnion of Lake Willersinnweiher.The emission of the greenhouse gas methane (CH 4 ) from freshwater lakes has been suggested to play a substantial role in the global methane budget (e.g., Bastviken et al. 2004). Here, significant amounts of CH 4 are emitted, even though CH 4 produced in aquatic systems is largely consumed by anaerobic and aerobic methanotrophs (up to 30-99%; Bastviken et al. 2008). The amount of emitted CH 4 is thereby depending on bioproduction, degradation and mineralization of organic substances in the sediments and the water column of the freshwater lake.Carbon mineralization in anoxic lake sediments is affected by manganese (Mn) and iron (Fe) reducing bacteria metabolizing competitive substrates, outcompeting CH 4 forming microorganisms (methanogens) within the upper sediment layers (e.g., Whiticar 1999). Sulfate (SO 4 2− ) reduction often has minor implications on organic matter degradation due to low SO 4 2− availability in most freshwater environments (Holmer and Storkholm 2001), so that SO 4 2− is rapidly depleted with sediment depth and SO 4 2− reducing bacteria become inactive or are absent. As a consequence, methanogenesis is the most important process in overall carbon mineralization in anoxic lacustrine sediments (e.g., Rudd and Hamilton 1978). Competitive metabolisms are not only affecting methanogenesis, but also consumption of CH 4 by bacteria (methanotrophs) in the sediments. The anaerobic oxidation of methane in the sediments of lakes is usually coupled to the reduction of the energetically more favorable electron acceptors, such as nitrate and nitrite (e.g., Raghoebarsing et al. 2006) or Fe(III) and/or Mn(I...

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“…It is known that CH 4 solubility and a well established methanotrophic community are important factors to control CH 4 emission in aquatic ecosystems (Wen et al, 2018;Valenzuela et al, 2020). This methanotrophic community can include aerobic methanotrophic bacteria or anaerobic methanotrophic archaea (ANME), the last one participating of CH 4 oxidation by reversion of the methanogenic pathway (Timmers et al, 2017) and by association with bacteria (Su et al, 2020). This interaction between archaeal and bacterial domains for CH 4 oxidation is coupled to the reduction of compounds such as sulfates or nitrates/nitrites, and elements such as metallic ions, removing them from the environment (Cui et al, 2015;Kiran et al, 2015;Naqvi et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Higher Abundance of Sediment Methanogens and Methanotrophs Do Not Predict the Atmospheric Methane and Carbon Dioxide Flows in Eutrophic Tropical Freshwater Reservoirs

et al. 2021

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Freshwater reservoirs emit greenhouse gases (GHGs) such as methane (CH4) and carbon dioxide (CO2), contributing to global warming, mainly when impacted by untreated sewage and other anthropogenic sources. These gases can be produced by microbial organic carbon decomposition, but little is known about the microbiota and its participation in GHG production and consumption in these environments. In this paper we analyzed the sediment microbiota of three eutrophic tropical urban freshwater reservoirs, in different seasons and evaluated the correlations between microorganisms and the atmospheric CH4 and CO2 flows, also correlating them to limnological variables. Our results showed that deeper water columns promote high methanogen abundance, with predominance of acetoclastic Methanosaeta spp. and hydrogenotrophs Methanoregula spp. and Methanolinea spp. The aerobic methanotrophic community was affected by dissolved total carbon (DTC) and was dominated by Crenothrix spp. However, both relative abundance of the total methanogenic and aerobic methanotrophic communities in sediments were uncoupled to CH4 and CO2 flows. Network based approach showed that fermentative microbiota, including Leptolinea spp. and Longilinea spp., which produces substrates for methanogenesis, influence CH4 flows and was favored by anthropogenic pollution, such as untreated sewage loads. Additionally, less polluted conditions favored probable anaerobic methanotrophs such as Candidatus Bathyarchaeota, Sva0485, NC10, and MBG-D/DHVEG-1, which promoted lower gaseous flows, confirming the importance of sanitation improvement to reduce these flows in tropical urban freshwater reservoirs and their local and global warming impact.

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Manganese/iron-supported sulfate-dependent anaerobic oxidation of methane by archaea in lake sediments

Cited by 11 publications

References 69 publications

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

Methanotrophs: Discoveries, Environmental Relevance, and a Perspective on Current and Future Applications

The impact of seasonal sulfate–methane transition zones on methane cycling in a sulfate‐enriched freshwater environment

Higher Abundance of Sediment Methanogens and Methanotrophs Do Not Predict the Atmospheric Methane and Carbon Dioxide Flows in Eutrophic Tropical Freshwater Reservoirs

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