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

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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The Formation of Authigenic Carbonates at a Methane Seep Site in the Northern Part of the Laptev Sea

Minerals ◽

10.3390/min10110948 ◽

2020 ◽

Vol 10 (11) ◽

pp. 948

Author(s):

Alexey Ruban ◽

Maxim Rudmin ◽

Oleg Dudarev ◽

Alexey Mazurov

Keyword(s):

Seawater Temperature ◽

Cold Seep ◽

Anaerobic Oxidation Of Methane ◽

Laptev Sea ◽

Cold Seeps ◽

Authigenic Carbonates ◽

Oxidation Of Methane ◽

Major Oxide ◽

Mg Content ◽

The Laptev Sea

Authigenic carbonates from cold seeps are unique archives for studying environmental conditions, including biogeochemical processes associated with methane-rich fluid migration through the sediment column. The aim of this research was to study major oxide, mineralogical, and stable isotopic compositions of cold-seep authigenic carbonates collected in the northern part of the Laptev Sea. These carbonates are represented by Mg-calcite with an Mg content of 2% to 8%. The δ13C values range from −27.5‰ to −28.2‰ Vienna Peedee belemnite (VPDB) and indicate that carbonates formed due to anaerobic oxidation of methane, most likely thermogenic in origin. The authigenic pyrite in Mg-calcite is evidence of sulfate reduction during carbonate precipitation. The δ18O values of carbonates vary from 3.5‰ to 3.8‰ VPDB. The calculated δ18Ofluid values show that pore water temperature for precipitated Mg-calcite was comparable to bottom seawater temperature. The presence of authigenic carbonate in the upper horizons of sediments suggests that the sulfate–methane transition zone is shallowly below the sediment–water interface.

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An experimental study on short-term changes in the anaerobic oxidation of methane in response to varying methane and sulfate fluxes

Biogeosciences ◽

10.5194/bg-6-867-2009 ◽

2009 ◽

Vol 6 (5) ◽

pp. 867-876 ◽

Cited By ~ 24

Author(s):

G. Wegener ◽

A. Boetius

Keyword(s):

Cold Seep ◽

Anaerobic Oxidation Of Methane ◽

Cold Seeps ◽

Anaerobic Oxidation ◽

Short Term ◽

Sulfate Reducing ◽

Oxidation Of Methane ◽

Column System ◽

Methane Fluxes ◽

Anaerobic Methanotrophs

Abstract. A major role in regulation of global methane fluxes has been attributed to the process of anaerobic oxidation of methane (AOM), which is performed by consortia of methanotrophic archaea and sulfate reducing bacteria. An important question remains how these energy limited, slow growing microorganisms with generation times of 3–7 months respond to rapid natural variations in methane fluxes at cold seeps. We used an experimental flow-through column system filled with cold seep sediments naturally enriched in methanotrophic communities, to test their responses to short-term variations in methane and sulfate fluxes. At stable methane and sulfate concentrations of ~2 mM and 28 mM, respectively, we measured constant rates of AOM and sulfate reduction (SR) for up to 160 days of incubation. When percolated with methane-free medium, the anaerobic methanotrophs ceased to produce sulfide. After a starvation phase of 40 days, the addition of methane restored former AOM and SR rates immediately. At methane concentrations between 0–2.3 mM we measured a linear correlation between methane availability, AOM and SR. At constant fluid flow velocities of 30 m yr−1, ca. 50% of the methane was consumed by the anaerobic methanotrophic (ANME) population at all concentrations tested. Reducing the sulfate concentration from 28 to 1 mM, a decrease in AOM and SR by 50% was observed, and 45% of the methane was consumed. Hence, the marine anaerobic methanotrophs (ANME) are capable of oxidizing substantial amounts of methane over a wide and variable range of fluxes of the reaction educts.

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Trace methane oxidation studied in several Euryarchaeota under diverse conditions

Archaea ◽

10.1155/2005/650670 ◽

2005 ◽

Vol 1 (5) ◽

pp. 303-309 ◽

Cited By ~ 64

Author(s):

James J. Moran ◽

Christopher H. House ◽

Katherine H. Freeman ◽

James G. Ferry

Keyword(s):

Methane Oxidation ◽

Methanosarcina Barkeri ◽

Electron Acceptors ◽

Anaerobic Oxidation Of Methane ◽

Methanosarcina Acetivorans ◽

Sulfate Reducing ◽

Oxidation Of Methane ◽

Pure Cultures ◽

Reverse Methanogenesis ◽

Electron Carriers

We used13C-labeled methane to document the extent of trace methane oxidation byArchaeoglobus fulgidus,Archaeoglobus lithotrophicus,Archaeoglobus profundus,Methanobacterium thermoautotrophicum,Methanosarcina barkeriandMethanosarcina acetivorans. The results indicate trace methane oxidation during growth varied among different species and among methanogen cultures grown on different substrates. The extent of trace methane oxidation byMb. thermoautotrophicum(0.05 ± 0.04%, ± 2 standard deviations of the methane produced during growth) was less than that byM. barkeri(0.15 ± 0.04%), grown under similar conditions with H2and CO2.Methanosarcina acetivoransoxidized more methane during growth on trimethylamine (0.36 ± 0.05%) than during growth on methanol (0.07 ± 0.03%). This may indicate that, inM. acetivorans, either a methyltransferase related to growth on trimethylamine plays a role in methane oxidation, or that methanol is an intermediate of methane oxidation. Addition of possible electron acceptors (O2, NO3–, SO22–, SO32–) or H2to the headspace did not substantially enhance or diminish methane oxidation inM. acetivoranscultures.Separate growth experiments with FAD and NAD+showed that inclusion of these electron carriers also did not enhance methane oxidation. Our results suggest trace methane oxidized during methanogenesis cannot be coupled to the reduction of these electron acceptors in pure cultures, and that the mechanism by which methane is oxidized in methanogens is independent of H2concentration. In contrast to the methanogens, species of the sulfate-reducing genusArchaeoglobusdid not significantly oxidize methane during growth (oxidizing 0.003 ± 0.01% of the methane provided toA. fulgidus, 0.002 ± 0.009% toA. lithotrophicusand 0.003 ± 0.02% toA. profundus). Lack of observable methane oxidation in the threeArchaeoglobusspecies examined may indicate that methyl-coenzyme M reductase, which is not present in this genus, is required for the anaerobic oxidation of methane, consistent with the “reverse methanogenesis” hypothesis.

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Microbial activity and carbonate isotope signatures as a tool for identification of spatial differences in methane advection: a case study at the Pacific Costa Rican margin

Biogeosciences ◽

10.5194/bg-11-507-2014 ◽

2014 ◽

Vol 11 (2) ◽

pp. 507-523 ◽

Cited By ~ 7

Author(s):

S. Krause ◽

P. Steeb ◽

C. Hensen ◽

V. Liebetrau ◽

A. W. Dale ◽

...

Keyword(s):

Numerical Modelling ◽

Microbial Activity ◽

Methane Flux ◽

Anaerobic Oxidation Of Methane ◽

Cold Seeps ◽

Authigenic Carbonates ◽

Biogenic Methane ◽

Oxygen And Carbon Isotope ◽

Oxidation Of Methane ◽

Methane Fluxes

Abstract. The forearc of the convergent margin offshore Costa Rica is a region characterized by strong advection of methane-charged fluids causing the formation of ubiquitous cold seeps (mounds). Presented here are the first measurements of microbial anaerobic oxidation of methane (AOM) and sulfate reduction (SR) rates in sediments from two mounds (11 and 12), applying radiotracer techniques in combination with numerical modelling. In addition, analysis of microbial, methane-dependent carbonate δ18O, δ13C, and 87Sr / 86Sr signatures constrained the origin of the carbonate-precipitating fluid. Average rates of microbial activities differed by a factor of ~5 to 6 between Mound 11 (AOM 140.71 (±40.84 SD) mmol m−2 d−1, SR 117.25 (±82.06 SD) mmol m−2 d−1) and Mound 12 (AOM 22.37 (±0.85 SD) mmol m−2 d−1, SR 23.99 (±5.79 SD) mmol m−2 d−1). Modelling results yielded upward fluid advection velocities of 200 cm yr−1 at Mound 11 and 15 cm yr−1 at Mound 12. Analysis of oxygen and carbon isotope variations of authigenic carbonates from the two locations revealed more enriched values for Mound 11 (δ18O : 3.18 to 6.15‰; δ13C: −14.14 to −29.56‰) compared to Mound 12 (δ18O : 3.09 to 4.48‰; δ13C : −39.53 to −48.98‰). The variation of carbonate 87Sr / 86Sr indicated considerable admixture of deep-source fluid at Mound 11, while seawater 87Sr / 86Sr characteristics prevailed at Mound 12 during precipitation. The present study is in accordance with previous work supporting considerable differences of methane flux between the two mounds. It also strengthens the hypothesis of a dominant deep fluid source with thermogenic methane at Mound 11 versus a shallow source of biogenic methane at Mound 12. The results demonstrate that measurements of methane-driven microbial activity in combination with numerical modelling are a valid tool for constraining recent methane fluxes in the study area. In addition, the analysis of methane-derived authigenic carbonates provides an independent line of evidence for long-term fluid contribution to the porewater chemistry of shallow sediments in the study area.

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Paddy soil fertilization, organic and inorganic alternative electron acceptors shape microbial community network and determine competitive pathways of Anaerobic Oxidation of Methane

10.5194/egusphere-egu2020-861 ◽

2020 ◽

Author(s):

Lichao Fan

Keyword(s):

Network Analysis ◽

Humic Acids ◽

Paddy Soil ◽

Electron Acceptors ◽

Pig Manure ◽

Anaerobic Oxidation Of Methane ◽

Anaerobic Incubation ◽

Sulfate Reducing ◽

Oxidation Of Methane ◽

Reducing Bacteria

Anaerobic oxidation of methane (AOM) is a globally important CH4 sink that is offsetting potential CH4 emission into the atmosphere. The AOM depends on the availability of the alternative to oxygen electron acceptors (AEAs) which can be of inorganic (e.g. NO3-, Fe3+, SO42-), and organic (e.g. humic acids) origin. Flooded paddy soils are among the ecosystems with pronounced AOM. Due to a variety of fertilization practices, including combinations of mineral (NPK) and organic (pig manure, biochar) fertilizers, there is a range of AEAs available in paddy soil under anaerobic conditions. However, it remains unclear whether (i) AOM has a preferential pathway in paddy soil, and (ii) how do AEAs and fertilization type affect anaerobic microbial interactions. Therefore, we tested the effects of key AEAs &#8211; NO3-, Fe3+, SO42-, and humic acids &#8211; on bacterial community structure (by 16s rRNA gene sequencing) in paddy soil with ongoing AOM experiment under mineral and organic fertilization. We hypothesized that incorporation of labeled 13C-CH4 during AOM into CO2 and phospholipid fatty acid biomarkers (PLFA) along with co-occurrence bacterial network analysis will reveal the preferential AOM pathway as related to a type of fertilization.Bacterial alpha-diversity was significantly increased after 84-day anaerobic incubation. Pig manure significantly increased the microbial biomass as compared with NPK and Biochar, but the AEAs amendment did not affect the biomass. Anaerobic incubation, fertilization treatments specific biochar and NPK, and AEAs amendments specific SO42- and humic acids were factors contributing to microbiome variation. Network analysis indicated that microbial communities involved in CH4 cycling (i.e. NC10, sulfate-reducing bacteria, Geobacter, syntrophic bacteria with methanogens and ANME-2) had non-random co-occurrence patterns and was modularized. There were 16 13C-enriched PLFA biomarkers confirming the incorporation of C-CH4 into bacteria. AOM and 13C-PLFA were significantly higher under Pig manure relative to other fertilizations. AOM was more intensive under NO3- than Fe3+ and humic acids, but was close to zero under SO42- amendment. However, the relative abundance of NC10 phylum which includes organisms performing AOM, and sulfate-reducing bacteria were higher under SO42-. The relative abundance of Geobacter was highest under biochar and NPK fertilization with SO42- and humic acids amendments. Taken together, NO3--driven AOM is the most potent AOM pathway in paddy soil, which however co-exists with the AOM pathways via reduction of NO2- by NC10 bacteria and reduction of Fe3+ and humic acids by consortia of ANME with Geobacter. Consequently, the co-occurrence network and evidence from 13C incorporation into CO2 and PLFAs indicate the multiple competitive pathways of AOM in paddy soil.

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Cold seeps and benthic habitat on the Pacific margin of Canada

Continental Shelf Research ◽

10.1016/j.csr.2010.02.013 ◽

2011 ◽

Vol 31 (2) ◽

pp. S85-S92 ◽

Cited By ~ 15

Author(s):

J. Vaughn Barrie ◽

Sarah Cook ◽

Kim W. Conway

Keyword(s):

Benthic Habitat ◽

Cold Seeps ◽

The Pacific ◽

Pacific Margin

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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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Phosphorus Species in Deep-Sea Carbonate Deposits: Implications for Phosphorus Cycling in Cold Seep Environments

Minerals ◽

10.3390/min10070645 ◽

2020 ◽

Vol 10 (7) ◽

pp. 645

Author(s):

Junlie Zhou ◽

Mengran Du ◽

Jiwei Li ◽

Hengchao Xu ◽

Kaiwen Ta ◽

...

Keyword(s):

Deep Sea ◽

Cold Seep ◽

Anaerobic Oxidation Of Methane ◽

Cold Seeps ◽

Organic P ◽

Anaerobic Oxidation ◽

Phosphorus Species ◽

China Sea ◽

Oxidation Of Methane ◽

Deep Sediments

Phosphorus (P) is an important nutrient for biological communities in cold seeps. However, our knowledge on the source, species, and cycling of P in cold seep environments is limited. In this study, the concentration, species, and micro to nanometer scale distribution of P in seep carbonates were examined at three deep-sea cold seeps in the South China Sea and East China Sea. The Ca-P accounts for the largest proportion of P—followed by detrital-P, Fe-P, organic-P, and exchangeable-P. The distribution patterns of Ca-P, detrital-P, and organic-P in the seep carbonates differ from one another, as shown by elemental mapping with NanoSIMS and scanning electron microscopy. The covariation of P with Ca and C reveals that Ca-P co-precipitates with Ca-carbonate, which is linked to the process of sulfate-driven anaerobic oxidation of methane. Organic-P is also observed within biofilm-like organic carbon aggregates, revealing the microbial enrichment of P by fluids in the process of anaerobic oxidation of methane. P with a granulated morphology was identified as detrital-P derived from deep sediments. Most importantly, it is evident that Ca-P is positively correlated to the Fe content in all the seep carbonates. This indicates the likelihood that the dissolved P in cold-seep fluids is released primarily from Fe oxides through Fe-driven anaerobic oxidation of methane in deep sediments. These processes associated with different species of P may have significant implications for P geochemical cycling and anaerobic oxidation of methane impelled by Fe and sulfate reduction in cold seep environments.

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Characterization of Specific Membrane Fatty Acids as Chemotaxonomic Markers for Sulfate-Reducing Bacteria Involved in Anaerobic Oxidation of Methane

Geomicrobiology Journal ◽

10.1080/01490450303894 ◽

2003 ◽

Vol 20 (4) ◽

pp. 403-419 ◽

Cited By ~ 171

Author(s):

Marcus Elvert ◽

Antje Boetius ◽

Katrin Knittel ◽

Bo Barker Jørgensen

Keyword(s):

Fatty Acids ◽

Sulfate Reducing Bacteria ◽

Anaerobic Oxidation Of Methane ◽

Sulfate Reducing ◽

Membrane Fatty Acids ◽

Oxidation Of Methane ◽

Chemotaxonomic Markers ◽

Reducing Bacteria ◽

Specific Membrane

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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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