scholarly journals Reverse Methanogenesis and Respiration in Methanotrophic Archaea

Archaea ◽  
2017 ◽  
Vol 2017 ◽  
pp. 1-22 ◽  
Author(s):  
Peer H. A. Timmers ◽  
Cornelia U. Welte ◽  
Jasper J. Koehorst ◽  
Caroline M. Plugge ◽  
Mike S. M. Jetten ◽  
...  

Anaerobic oxidation of methane (AOM) is catalyzed by anaerobic methane-oxidizing archaea (ANME) via a reverse and modified methanogenesis pathway. Methanogens can also reverse the methanogenesis pathway to oxidize methane, but only during net methane production (i.e., “trace methane oxidation”). In turn, ANME can produce methane, but only during net methane oxidation (i.e., enzymatic back flux). Net AOM is exergonic when coupled to an external electron acceptor such as sulfate (ANME-1, ANME-2abc, and ANME-3), nitrate (ANME-2d), or metal (oxides). In this review, the reversibility of the methanogenesis pathway and essential differences between ANME and methanogens are described by combining published information with domain based (meta)genome comparison of archaeal methanotrophs and selected archaea. These differences include abundances and special structure of methyl coenzyme M reductase and of multiheme cytochromes and the presence of menaquinones or methanophenazines. ANME-2a and ANME-2d can use electron acceptors other than sulfate or nitrate for AOM, respectively. Environmental studies suggest that ANME-2d are also involved in sulfate-dependent AOM. ANME-1 seem to use a different mechanism for disposal of electrons and possibly are less versatile in electron acceptors use than ANME-2. Future research will shed light on the molecular basis of reversal of the methanogenic pathway and electron transfer in different ANME types.

Archaea ◽  
2005 ◽  
Vol 1 (5) ◽  
pp. 303-309 ◽  
Author(s):  
James J. Moran ◽  
Christopher H. House ◽  
Katherine H. Freeman ◽  
James G. Ferry

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.


2011 ◽  
Vol 77 (13) ◽  
pp. 4429-4436 ◽  
Author(s):  
Jörg S. Deutzmann ◽  
Bernhard Schink

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.


2021 ◽  
Author(s):  
Hanni Vigderovich ◽  
Werner Eckert ◽  
Michal Elul ◽  
Maxim Rubin-Blum ◽  
Marcus Elvert ◽  
...  

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.


2019 ◽  
Author(s):  
Guangyi Su ◽  
Jakob Zopfi ◽  
Haoyi Yao ◽  
Lea Steinle ◽  
Helge Niemann ◽  
...  

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.


2018 ◽  
Vol 84 (11) ◽  
Author(s):  
Shawn E. McGlynn ◽  
Grayson L. Chadwick ◽  
Ariel O'Neill ◽  
Mason Mackey ◽  
Andrea Thor ◽  
...  

ABSTRACTPhylogenetically diverse environmental ANME archaea and sulfate-reducing bacteria cooperatively catalyze the anaerobic oxidation of methane oxidation (AOM) in multicelled consortia within methane seep environments. To better understand these cells and their symbiotic associations, we applied a suite of electron microscopy approaches, including correlative fluorescencein situhybridization-electron microscopy (FISH-EM), transmission electron microscopy (TEM), and serial block face scanning electron microscopy (SBEM) three-dimensional (3D) reconstructions. FISH-EM of methane seep-derived consortia revealed phylogenetic variability in terms of cell morphology, ultrastructure, and storage granules. Representatives of the ANME-2b clade, but not other ANME-2 groups, contained polyphosphate-like granules, while some bacteria associated with ANME-2a/2c contained two distinct phases of iron mineral chains resembling magnetosomes. 3D segmentation of two ANME-2 consortium types revealed cellular volumes of ANME and their symbiotic partners that were larger than previous estimates based on light microscopy. Polyphosphate-like granule-containing ANME (tentatively termed ANME-2b) were larger than both ANME with no granules and partner bacteria. This cell type was observed with up to 4 granules per cell, and the volume of the cell was larger in proportion to the number of granules inside it, but the percentage of the cell occupied by these granules did not vary with granule number. These results illuminate distinctions between ANME-2 archaeal lineages and partnering bacterial populations that are apparently unified in their ability to perform anaerobic methane oxidation.IMPORTANCEMethane oxidation in anaerobic environments can be accomplished by a number of archaeal groups, some of which live in syntrophic relationships with bacteria in structured consortia. Little is known of the distinguishing characteristics of these groups. Here, we applied imaging approaches to better understand the properties of these cells. We found unexpected morphological, structural, and volume variability of these uncultured groups by correlating fluorescence labeling of cells with electron microscopy observables.


2012 ◽  
Vol 9 (10) ◽  
pp. 3891-3899 ◽  
Author(s):  
A. Bannert ◽  
C. Bogen ◽  
J. Esperschütz ◽  
A. Koubová ◽  
F. Buegger ◽  
...  

Abstract. While the importance of anaerobic methane oxidation has been reported for marine ecosystems, the role of this process in soils is still questionable. Grasslands used as pastures for cattle overwintering show an increase in anaerobic soil micro-sites caused by animal treading and excrement deposition. Therefore, anaerobic potential methane oxidation activity of severely impacted soil from a cattle winter pasture was investigated in an incubation experiment under anaerobic conditions using 13C-labelled methane. We were able to detect a high microbial activity utilizing CH4 as nutrient source shown by the respiration of 13CO2. Measurements of possible terminal electron acceptors for anaerobic oxidation of methane were carried out. Soil sulfate concentrations were too low to explain the oxidation of the amount of methane added, but enough nitrate and iron(III) were detected. However, only nitrate was consumed during the experiment. 13C-PLFA analyses clearly showed the utilization of CH4 as nutrient source mainly by organisms harbouring 16:1ω7 PLFAs. These lipids were also found as most 13C-enriched fatty acids by Raghoebarsing et al. (2006) after addition of 13CH4 to an enrichment culture coupling denitrification of nitrate to anaerobic oxidation of methane. This might be an indication for anaerobic oxidation of methane by relatives of "Candidatus Methylomirabilis oxyfera" in the investigated grassland soil under the conditions of the incubation experiment.


2018 ◽  
Author(s):  
Jeanine L. Ash ◽  
Matthias Egger ◽  
Tina Treude ◽  
Issaku Kohl ◽  
Barry Cragg ◽  
...  

The anaerobic oxidation of methane (AOM) is a crucial component of the methane cycle, but its enzymatic versatility under environmental conditions remains poorly understood. We use sediment samples collected during IODP Expedition 347 to the Baltic Sea to show that relative abundances of 12CH2D2 and 13CH3D molecules in methane gas trace the reversibility of methyl-coenzyme M reductase during AOM by driving methane towards internal, thermodynamic isotopic equilibrium. These data suggest that 12CH2D2 and 13CH3D together can identify the influence of methanotrophy in environments where conventional bulk isotope ratios are ambiguous, and these findings may lead to new insights regarding the global significance of enzymatic back-flux in the methane cycle.


2012 ◽  
Vol 9 (4) ◽  
pp. 4919-4945
Author(s):  
A. Bannert ◽  
C. Bogen ◽  
J. Esperschütz ◽  
A. Koubová ◽  
F. Buegger ◽  
...  

Abstract. While the importance of anaerobic methane oxidation has been reported for marine ecosystems, the role of this process in soils is still questionable. Grasslands used as pastures for cattle-overwintering show an increase in anaerobic soil micro-sites caused by animal treading and excrement deposition. Therefore anaerobic potential methane oxidation activity of severely impacted soil from a cattle winter pasture was investigated in an incubation experiment under anaerobic conditions using 13C-labeled methane. We were able to detect a high microbial activity utilizing CH4 as nutrient source shown by the respiration of 13CO2. Measurements of possible terminal electron acceptors for anaerobic oxidation of methane were carried out. Soil sulfate concentrations were too low to explain the oxidation of the amount of methane added, but enough nitrate and iron(III) were detected. However, only nitrate was consumed during the experiment. 13C-PLFA analyses clearly showed the utilization of CH4 as nutrient source mainly by organisms harbouring 16:1ω7 PLFAs. These lipids were found in Gram-negative microorganisms and anaerobes. The fact that these lipids are also typical for type I methanotrophs, known as aerobic methane oxidizers, might indicate a link between aerobic and anaerobic methane oxidation.


Author(s):  
Sabrina Beckmann ◽  
Ibrahim F. Farag ◽  
Rui Zhao ◽  
Glenn D Christman ◽  
Nancy G Prouty ◽  
...  

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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