Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

ABSTRACT Wetlands constitute the main natural source of methane on Earth due to their high content of natural organic matter (NOM), but key drivers, such as electron acceptors, supporting methanotrophic activities in these habitats are poorly understood. We performed anoxic incubations using freshly collected sediment, along with water samples harvested from a tropical wetland, amended with 13C-methane (0.67 atm) to test the capacity of its microbial community to perform anaerobic oxidation of methane (AOM) linked to the reduction of the humic fraction of its NOM. Collected evidence demonstrates that electron-accepting functional groups (e.g., quinones) present in NOM fueled AOM by serving as a terminal electron acceptor. Indeed, while sulfate reduction was the predominant process, accounting for up to 42.5% of the AOM activities, the microbial reduction of NOM concomitantly occurred. Furthermore, enrichment of wetland sediment with external NOM provided a complementary electron-accepting capacity, of which reduction accounted for ∼100 nmol 13CH4 oxidized · cm−3 · day−1. Spectroscopic evidence showed that quinone moieties were heterogeneously distributed in the wetland sediment, and their reduction occurred during the course of AOM. Moreover, an enrichment derived from wetland sediments performing AOM linked to NOM reduction stoichiometrically oxidized methane coupled to the reduction of the humic analogue anthraquinone-2,6-disulfonate. Microbial populations potentially involved in AOM coupled to microbial reduction of NOM were dominated by divergent biota from putative AOM-associated archaea. We estimate that this microbial process potentially contributes to the suppression of up to 114 teragrams (Tg) of CH4 · year−1 in coastal wetlands and more than 1,300 Tg · year−1, considering the global wetland area. IMPORTANCE The identification of key processes governing methane emissions from natural systems is of major importance considering the global warming effects triggered by this greenhouse gas. Anaerobic oxidation of methane (AOM) coupled to the microbial reduction of distinct electron acceptors plays a pivotal role in mitigating methane emissions from ecosystems. Given their high organic content, wetlands constitute the largest natural source of atmospheric methane. Nevertheless, processes controlling methane emissions in these environments are poorly understood. Here, we provide tracer analysis with 13CH4 and spectroscopic evidence revealing that AOM linked to the microbial reduction of redox functional groups in natural organic matter (NOM) prevails in a tropical wetland. We suggest that microbial reduction of NOM may largely contribute to the suppression of methane emissions from tropical wetlands. This is a novel avenue within the carbon cycle in which slowly decaying NOM (e.g., humic fraction) in organotrophic environments fuels AOM by serving as a terminal electron acceptor.

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Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake

Applied and Environmental Microbiology ◽

10.1128/aem.00340-11 ◽

2011 ◽

Vol 77 (13) ◽

pp. 4429-4436 ◽

Cited By ~ 141

Author(s):

Jörg S. Deutzmann ◽

Bernhard Schink

Keyword(s):

Methane Oxidation ◽

Electron Acceptors ◽

Molecular Techniques ◽

Freshwater Lake ◽

Lake Constance ◽

Anaerobic Oxidation Of Methane ◽

Anaerobic Oxidation ◽

Terminal Electron Acceptor ◽

Oxidation Of Methane ◽

Freshwater Habitats

ABSTRACTAnaerobic oxidation of methane (AOM) with sulfate as terminal electron acceptor has been reported for various environments, including freshwater habitats, and also, nitrate and nitrite were recently shown to act as electron acceptors for methane oxidation in eutrophic freshwater habitats. Radiotracer experiments with sediment material of Lake Constance, an oligotrophic freshwater lake, were performed to follow14CO2formation from14CH4in sediment incubations in the presence of different electron acceptors, namely, nitrate, nitrite, sulfate, or oxygen. Whereas14CO2formation without and with sulfate addition was negligible, addition of nitrate increased14CO2formation significantly, suggesting that AOM could be coupled to denitrification. Nonetheless, denitrification-dependent AOM rates remained at least 1 order of magnitude lower than rates of aerobic methane oxidation. Using molecular techniques, putative denitrifying methanotrophs belonging to the NC10 phylum were detected on the basis of thepmoAand 16S rRNA gene sequences. These findings show that sulfate-dependent AOM was insignificant in Lake constant sediments. However, AOM can also be coupled to denitrification in this oligotrophic freshwater habitat, providing first indications that this might be a widespread process that plays an important role in mitigating methane emissions.

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Different impacts of an electron shuttle on nitrate- and nitrite-dependent anaerobic oxidation of methane in paddy soil

Plant Soil and Environment ◽

10.17221/579/2020-pse ◽

2021 ◽

Vol 67 (No. 5) ◽

pp. 264-269

Author(s):

Yaohong Zhang ◽

Fangyuan Wang

Keyword(s):

Organic Matter ◽

Paddy Soil ◽

Anaerobic Oxidation Of Methane ◽

Electron Shuttle ◽

Anaerobic Oxidation ◽

Terminal Electron Acceptor ◽

Electron Shuttles ◽

Oxidation Of Methane ◽

Nitrate And Nitrite ◽

C Assimilation

Quinones, redox-active functional groups in soil organic matter, can act as electron shuttles for microbial anaerobic transformation. Here, we used 13CH4 to trace 13C conversion (13C-CO2 + 13C-SOC) to investigate the influence of an artificial electron shuttle (anthraquinone-2,6-disulfonate, AQDS) on denitrifying anaerobic methane oxidation (DAMO) in paddy soil. The results showed that AQDS could act as the terminal electron acceptor for the anaerobic oxidation of methane (AOM) in the paddy field. Moreover, AQDS significantly enhanced nitrate-dependent AOM rates and the amount of 13C-CH4 assimilation to soil organic carbon (SOC), whereas it was remarkably reduced nitrite-dependent AOM rates and 13C assimilation. Ultimately, AQDS notably increased the total DAMO rates and 13C assimilation to SOC. However, the electron shuttle did not change the percentage of 13C-SOC in total 13C-CH4 conversion. These results suggest that electron shuttles in the natural organic matter might be able to offset methane emission by facilitating AOM coupled with the denitrification process.

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

Frontiers in Microbiology ◽

10.3389/fmicb.2021.678057 ◽

2021 ◽

Vol 12 ◽

Author(s):

Simon Guerrero-Cruz ◽

Annika Vaksmaa ◽

Marcus A. Horn ◽

Helge Niemann ◽

Maite Pijuan ◽

...

Keyword(s):

Organic Matter ◽

Electron Acceptors ◽

Manganese Sulfate ◽

Anaerobic Oxidation Of Methane ◽

Methane Mitigation ◽

Oxidation Of Methane ◽

Decomposition Of Organic Matter ◽

Anaerobic Methanotrophs ◽

Key Aspects ◽

Methane Efflux

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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Anthropogenic and Environmental Constraints on the Microbial Methane Cycle in Coastal Sediments

Frontiers in Microbiology ◽

10.3389/fmicb.2021.631621 ◽

2021 ◽

Vol 12 ◽

Author(s):

Anna J. Wallenius ◽

Paula Dalcin Martins ◽

Caroline P. Slomp ◽

Mike S. M. Jetten

Keyword(s):

Organic Matter ◽

Water Column ◽

Current Knowledge ◽

Methane Emissions ◽

Electron Acceptors ◽

Nitrite Reduction ◽

Coastal Sediments ◽

Anaerobic Oxidation Of Methane ◽

Methane Cycle ◽

Methane Cycling

Large amounts of methane, a potent greenhouse gas, are produced in anoxic sediments by methanogenic archaea. Nonetheless, over 90% of the produced methane is oxidized via sulfate-dependent anaerobic oxidation of methane (S-AOM) in the sulfate-methane transition zone (SMTZ) by consortia of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). Coastal systems account for the majority of total marine methane emissions and typically have lower sulfate concentrations, hence S-AOM is less significant. However, alternative electron acceptors such as metal oxides or nitrate could be used for AOM instead of sulfate. The availability of electron acceptors is determined by the redox zonation in the sediment, which may vary due to changes in oxygen availability and the type and rate of organic matter inputs. Additionally, eutrophication and climate change can affect the microbiome, biogeochemical zonation, and methane cycling in coastal sediments. This review summarizes the current knowledge on the processes and microorganisms involved in methane cycling in coastal sediments and the factors influencing methane emissions from these systems. In eutrophic coastal areas, organic matter inputs are a key driver of bottom water hypoxia. Global warming can reduce the solubility of oxygen in surface waters, enhancing water column stratification, increasing primary production, and favoring methanogenesis. ANME are notoriously slow growers and may not be able to effectively oxidize methane upon rapid sedimentation and shoaling of the SMTZ. In such settings, ANME-2d (Methanoperedenaceae) and ANME-2a may couple iron- and/or manganese reduction to AOM, while ANME-2d and NC10 bacteria (Methylomirabilota) could couple AOM to nitrate or nitrite reduction. Ultimately, methane may be oxidized by aerobic methanotrophs in the upper millimeters of the sediment or in the water column. The role of these processes in mitigating methane emissions from eutrophic coastal sediments, including the exact pathways and microorganisms involved, are still underexplored, and factors controlling these processes are unclear. Further studies are needed in order to understand the factors driving methane-cycling pathways and to identify the responsible microorganisms. Integration of the knowledge on microbial pathways and geochemical processes is expected to lead to more accurate predictions of methane emissions from coastal zones in the future.

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

10.1101/636621 ◽

2019 ◽

Author(s):

Guangyi Su ◽

Jakob Zopfi ◽

Haoyi Yao ◽

Lea Steinle ◽

Helge Niemann ◽

...

Keyword(s):

Lake Sediments ◽

16S Rrna Gene Sequencing ◽

Electron Acceptors ◽

Rrna Gene ◽

Anaerobic Oxidation Of Methane ◽

Anaerobic Oxidation ◽

Sequencing Data ◽

Oxidation Of Methane ◽

Freshwater Habitats ◽

Rrna Gene Sequencing

AbstractAnaerobic oxidation of methane (AOM) by methanotrophic archaea is an important sink of this greenhouse gas in marine sediments. However, evidence for AOM in freshwater habitats is rare, and little is known about the pathways, electron acceptors and microbes involved. Here, we show that AOM occurs in anoxic sediments of a lake in southern Switzerland (Lake Cadagno). Combined AOM-rate and 16S rRNA gene-sequencing data suggest thatCandidatusMethanoperedens archaea are responsible for the observed methane oxidation. Members of the Methanoperedenaceae family were previously reported to conduct nitrate- or iron/manganese-dependent AOM. However, we demonstrate for the first time that the methanotrophic archaea do not necessarily rely upon these oxidants as terminal electron acceptors directly, but mainly perform canonical sulfate-dependent AOM, which under sulfate-starved conditions can be supported by metal (Mn, Fe) oxides through oxidation of reduced sulfur species to sulfate. The correspondence of high abundances of Desulfobulbaceae andCandidatusMethanoperedens at the same sediment depth confirm the interdependence of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria. The relatively high abundance and widespread distribution ofCandidatusMethanoperedens in lake sediments highlight their potentially important role in mitigating methane emissions from terrestrial freshwater environments to the atmosphere, analogous to ANME-1, -2 and -3 in marine settings.

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Glendonites from Mesozoic succession of eastern Barents sea: distribution, genesis and paleoclimatic implications

10.5194/egusphere-egu2020-19076 ◽

2020 ◽

Author(s):

Kseniya Mikhailova ◽

Victoria Ershova ◽

Mikhail Rogov ◽

Boris Pokrovsky ◽

Oleg Vereshchagin

Keyword(s):

Organic Matter ◽

Calcium Carbonate ◽

Sulfate Reduction ◽

Early Cretaceous ◽

Lower Cretaceous ◽

Middle Jurassic ◽

Barents Sea ◽

Upper Jurassic ◽

Anaerobic Oxidation Of Methane ◽

Oxidation Of Methane

Glendonites often used as paleoclimate indicator of cold near-bottom temperature, as these are calcite pseudomorphs of ikaite, a metastable calcium carbonate hexahydrate, precipitates mostly under low temperature (mainly from 0-4oC) and may be stabilized by high phosphate concentrations that occurs due to anaerobic oxidation of methane and/or organic matter; dissolved organic carbon, sulfates and amino acid may contribute ikaite formation as well.&#160; Therefore, glendonites-bearing host rocks frequently include glacial deposits that make them useful as a paleoclimate indicator of near-freezing temperature.Our study is based on material collected from five wells drilled in eastern Barents Sea: Severo-Murmanskaya, Ledovaya &#8211; 1,2; Ludlovskaya &#8211; 1,2. The studied glendonites, mainly represented by relatively small rhombohedral pseudomorphs (0,5-2 cm) and rarely by stellate aggregates, collected from Middle Jurassic to Lower Cretaceous shallow marine clastic deposits. They scattered distributed throughout succession. Totally 18 samples of glendonites were studied. The age of host-bearing rocks were defined by fossils: bivalves or ammonites, microfossils or dinoflagellate. Bajocian-Bathonian glendonites were collected from Ledovaya &#8211; 1 and Ludlovskaya &#8211; 1 and 2 wells; in addition to these occurrences Middle Jurassic glendonites are known also in boreholes drilled at Shtockmanovskoe field. Numerous &#8216;jarrowite-like&#8217; glendonites of the Middle Volgian (~ latest early Tithonian) age were sampled from Severo-Murmanskaya well. Unique Late Barremian glendonites were found in Ledovaya &#8211; 2 well.&#948;18O values of Middle Jurassic glendonite concretions range from &#8211; 5.4 to &#8211;1.7 &#8240; Vienna Pee Dee Belemnite (VPDB); for Upper Jurassic &#8211; Lower Cretaceous &#948;18O values range from &#8211; 4.3 to &#8211;1.6 &#8240; VPDB; for Lower Cretaceous - &#948;18O values range from &#8211; 4.5 to &#8211;3.4 &#8240; VPDB. Carbon isotope composition for Middle Jurassic glendonite concretions &#948;13C values range from &#8211; 33.3 to &#8211;22.6 &#8240; VPDB; for Upper Jurassic &#8211; Lower Cretaceous &#948;13C values range from &#8211; 25.1 to &#8211;18.4 &#8240; VPDB; for Lower Cretaceous - &#948;13C values range from &#8211; 30.1 to &#8211;25.6 &#8240; VPDB.Based on &#948;18O data we supposed that seawater had a strong influence on ikaite-derived calcite precipitation. Received data coincide with &#948;18O values reported from other Mesozoic glendonites and Quaternary glendonites formed in cold environments. Values of &#948;13C of glendonites are close to bacterial sulfate reduction and/or anaerobic oxidation of methane or organic matter. Glendonites consist of carbonates forming a number of phases which different in phosphorus and magnesium content. Mg-bearing calcium carbonate and dolomite both include framboidal pyrite, which can indicate (1) lack of strong rock transformations activity and (2) presence of sulfate-reduction bacteria in sediments.To conclude, Mesozoic climate was generally warm and studied concretions indicate cold climate excursion in Middle Jurassic, Upper Jurassic-Early Cretaceous and Early Cretaceous.&#160;The study was supported by RFBR, project number 20-35-70012.

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Evidence for an expanded repertoire of electron acceptors for the anaerobic oxidation of methane in authigenic carbonates in the Atlantic and Pacific Ocean

10.1101/2020.06.12.148429 ◽

2020 ◽

Cited By ~ 1

Author(s):

Sabrina Beckmann ◽

Ibrahim F. Farag ◽

Rui Zhao ◽

Glenn D Christman ◽

Nancy G Prouty ◽

...

Keyword(s):

Electron Acceptors ◽

Nitrogen Compounds ◽

Anaerobic Oxidation Of Methane ◽

Cold Seeps ◽

Authigenic Carbonates ◽

Sulfate Reducing ◽

Oxidation Of Methane ◽

The Pacific ◽

Pacific Margin ◽

Sulfur And Nitrogen Compounds

AbstractAuthigenic carbonates represent a significant microbial sink for methane, yet little is known about the microbiome responsible for the methane removal. We identify carbonate microbiomes distributed over 21 locations hosted by 7 different cold seeps in the Pacific and Atlantic Oceans by carrying out a gene-based survey using 16S rRNA- and mcrA gene sequencing coupled with metagenomic analyses. These sites were dominated by bacteria affiliated to the Firmicutes, Alpha- and Gammaproteobacteria. ANME-1 and −2 clades were abundant in the carbonates yet their typical syntrophic partners, sulfate reducing bacteria, were not significantly present. Our analysis indicated that methane oxidizers affiliated to the ANME-1 and −2 as well as to the Candidatus Methanoperedens clades, are capable of performing complete methane- and potentially short-chain alkane oxidations independently using oxidized sulfur and nitrogen compounds as terminal electron acceptors. Gammaproteobacteria are hypothetically capable of utilizing oxidized nitrogen compounds in potential syntrophy with methane oxidizing archaea. Carbonate structures represent a window for a more diverse utilization of electron acceptors for anaerobic methane oxidation along the Atlantic and Pacific Margin.

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Impact of natural organic matter coatings on the microbial reduction of iron oxides

Geochimica et Cosmochimica Acta ◽

10.1016/j.gca.2018.01.004 ◽

2018 ◽

Vol 224 ◽

pp. 223-248 ◽

Cited By ~ 17

Author(s):

Christine Poggenburg ◽

Robert Mikutta ◽

Axel Schippers ◽

Reiner Dohrmann ◽

Georg Guggenberger

Keyword(s):

Organic Matter ◽

Iron Oxides ◽

Natural Organic Matter ◽

Microbial Reduction ◽

Reduction Of Iron

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Modification of methane oxidation pathways during long-term incubations of methanic lake sediments

10.5194/bg-2021-223 ◽

2021 ◽

Author(s):

Hanni Vigderovich ◽

Werner Eckert ◽

Michal Elul ◽

Maxim Rubin-Blum ◽

Marcus Elvert ◽

...

Keyword(s):

Lake Sediments ◽

Carbon Isotope ◽

Iron Oxides ◽

Methane Oxidation ◽

Electron Acceptors ◽

Anaerobic Oxidation Of Methane ◽

Methanotrophic Bacteria ◽

Oxidation Of Methane ◽

Isotope Measurements

Abstract. Anaerobic oxidation of methane (AOM) is one of the major processes limiting the release of the greenhouse gas methane from natural environments. In Lake Kinneret sediments, iron-coupled AOM (Fe-AOM) was suggested to play a substantial role (10–15 % relative to methanogenesis) in the methanic zone (> 20 cm sediment depth), based on geochemical profiles and experiments on fresh sediments. Apparently, the oxidation of methane is mediated by a combination of mcr gene bearing archaea and aerobic bacterial methanotrophs. Here we aimed to investigate the survival of this complex microbial interplay under controlled conditions. We followed the AOM process during long-term (~18 months) anaerobic slurry experiments of these methanic sediments with two stages of incubations and additions of 13C-labeled methane, multiple electron acceptors and inhibitors. After these incubation stages carbon isotope measurements in the dissolved inorganic pool still showed considerable AOM (3–8 % relative to methanogenesis). Specific lipid carbon isotope measurements and metagenomic analyses indicate that after the prolonged incubation aerobic methanotrophic bacteria were no longer involved in the oxidation process, whereas mcr gene bearing archaea were most likely responsible for oxidizing the methane. Humic substances and iron oxides are likely electron acceptors to support this oxidation, whereas sulfate, manganese, nitrate, and nitrite did not support the AOM in these methanic sediments. Our results suggest in the natural lake sediments methanotrophic bacteria are responsible for part of the methane oxidation by the reduction of combined micro levels of oxygen and iron oxides in a cryptic cycle, while the rest of the methane is converted by reverse methanogenesis. After long-term incubation, the latter prevails without bacterial methanotropic activity and with a different iron reduction pathway.

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