A new intra-aerobic metabolism in the nitrite-dependent anaerobic methane-oxidizing bacterium Candidatus ‘Methylomirabilis oxyfera’

2011 ◽  
Vol 39 (1) ◽  
pp. 243-248 ◽  
Author(s):  
Ming L. Wu ◽  
Katharina F. Ettwig ◽  
Mike S.M. Jetten ◽  
Marc Strous ◽  
Jan T. Keltjens ◽  
...  
Keyword(s):  
Nitric Oxide ◽  
Methane Oxidation ◽  
Current Knowledge ◽  
Methanogenic Archaea ◽  
Anaerobic Methane Oxidation ◽  
Oxidation Pathway ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Aerobic Methanotrophs ◽  
Reverse Methanogenesis

Biological methane oxidation proceeds either through aerobic or anaerobic pathways. The newly discovered bacterium Candidatus ‘Methylomirabilis oxyfera’ challenges this dichotomy. This bacterium performs anaerobic methane oxidation coupled to denitrification, but does so in a peculiar way. Instead of scavenging oxygen from the environment, like the aerobic methanotrophs, or driving methane oxidation by reverse methanogenesis, like the methanogenic archaea in sulfate-reducing systems, it produces its own supply of oxygen by metabolizing nitrite via nitric oxide into oxygen and dinitrogen gas. The intracellularly produced oxygen is then used for the oxidation of methane by the classical aerobic methane oxidation pathway involving methane mono-oxygenase. The present mini-review summarizes the current knowledge about this process and the micro-organism responsible for it.

scholarly journals Trace methane oxidation studied in several Euryarchaeota under diverse conditions

Archaea ◽  
2005 ◽  
Vol 1 (5) ◽  
pp. 303-309 ◽  
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.

scholarly journals Biomarker Evidence for Widespread Anaerobic Methane Oxidation in Mediterranean Sediments by a Consortium of Methanogenic Archaea and Bacteria

2000 ◽  
Vol 66 (3) ◽  
pp. 1126-1132 ◽  
Author(s):  
Richard D. Pancost ◽  
Jaap S. Sinninghe Damsté ◽  
Saskia de Lint ◽  
Marc J. E. C. van der Maarel ◽  
Jan C. Gottschal
Keyword(s):  
Methane Oxidation ◽  
Heterotrophic Bacteria ◽  
Methanogenic Archaea ◽  
Anaerobic Methane Oxidation ◽  
Geochemical Data ◽  
Mud Volcanoes ◽  
Terminal Electron Acceptor ◽  
Sulfate Reducing ◽  
Microbiological Process ◽  
Reducing Bacteria

ABSTRACT Although abundant geochemical data indicate that anaerobic methane oxidation occurs in marine sediments, the linkage to specific microorganisms remains unclear. In order to examine processes of methane consumption and oxidation, sediment samples from mud volcanoes at two distinct sites on the Mediterranean Ridge were collected via the submersible Nautile. Geochemical data strongly indicate that methane is oxidized under anaerobic conditions, and compound-specific carbon isotope analyses indicate that this reaction is facilitated by a consortium of archaea and bacteria. Specifically, these methane-rich sediments contain high abundances of methanogen-specific biomarkers that are significantly depleted in13C (δ13C values are as low as −95‰). Biomarkers inferred to derive from sulfate-reducing bacteria and other heterotrophic bacteria are similarly depleted. Consistent with previous work, such depletion can be explained by consumption of13C-depleted methane by methanogens operating in reverse and as part a consortium of organisms in which sulfate serves as the terminal electron acceptor. Moreover, our results indicate that this process is widespread in Mediterranean mud volcanoes and in some localized settings is the predominant microbiological process.

scholarly journals Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

2021 ◽  
Author(s):  
Grayson L Chadwick ◽  
Connor T Skennerton ◽  
Rafael Laso-Perez ◽  
Andy O Leu ◽  
Daan R Speth ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Comparative Analysis ◽  
Comparative Genomics ◽  
Pure Culture ◽  
Methanogenic Archaea ◽  
Anaerobic Oxidation Of Methane ◽  
Genomic Features ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Reducing Bacteria

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features which separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well-distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

scholarly journals Anaerobic oxidation of methane in grassland soils used for cattle husbandry

2012 ◽  
Vol 9 (4) ◽  
pp. 4919-4945
Author(s):  
A. Bannert ◽  
C. Bogen ◽  
J. Esperschütz ◽  
A. Koubová ◽  
F. Buegger ◽  
...  
Keyword(s):  
Methane Oxidation ◽  
Anaerobic Methane Oxidation ◽  
Anaerobic Oxidation Of Methane ◽  
Type I ◽  
Anaerobic Oxidation ◽  
Nutrient Source ◽  
Oxidation Activity ◽  
Oxidation Of Methane ◽  
Cattle Husbandry

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.

scholarly journals Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor

2003 ◽  
Vol 69 (9) ◽  
pp. 5472-5482 ◽  
Author(s):  
Peter R. Girguis ◽  
Victoria J. Orphan ◽  
Steven J. Hallam ◽  
Edward F. DeLong
Keyword(s):  
Methane Oxidation ◽  
Continuous Flow ◽  
Molecular Techniques ◽  
Anaerobic Methane Oxidation ◽  
Cold Seep ◽  
Microbial Consortia ◽  
Sulfate Reducing ◽  
Oxidation Rates ◽  
In Situ Conditions ◽  
Pure Cultures

ABSTRACT Anaerobic methanotrophic archaea have recently been identified in anoxic marine sediments, but have not yet been recovered in pure culture. Physiological studies on freshly collected samples containing archaea and their sulfate-reducing syntrophic partners have been conducted, but sample availability and viability can limit the scope of these experiments. To better study microbial anaerobic methane oxidation, we developed a novel continuous-flow anaerobic methane incubation system (AMIS) that simulates the majority of in situ conditions and supports the metabolism and growth of anaerobic methanotrophic archaea. We incubated sediments collected from within and outside a methane cold seep in Monterey Canyon, Calif., for 24 weeks on the AMIS system. Anaerobic methane oxidation was measured in all sediments after incubation on AMIS, and quantitative molecular techniques verified the increases in methane-oxidizing archaeal populations in both seep and nonseep sediments. Our results demonstrate that the AMIS system stimulated the maintenance and growth of anaerobic methanotrophic archaea, and possibly their syntrophic, sulfate-reducing partners. Our data demonstrate the utility of combining physiological and molecular techniques to quantify the growth and metabolic activity of anaerobic microbial consortia. Further experiments with the AMIS system should provide a better understanding of the biological mechanisms of methane oxidation in anoxic marine environments. The AMIS may also enable the enrichment, purification, and isolation of methanotrophic archaea as pure cultures or defined syntrophic consortia.

scholarly journals Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane

Life ◽  
2021 ◽  
Vol 11 (9) ◽  
pp. 953
Author(s):  
Alexander Y. Merkel ◽  
Nikolay A. Chernyh ◽  
Nikolai V. Pimenov ◽  
Elizaveta A. Bonch-Osmolovskaya ◽  
Alexander I. Slobodkin
Keyword(s):  
Methane Oxidation ◽  
Current Knowledge ◽  
High Abundance ◽  
Rrna Gene ◽  
Anaerobic Oxidation Of Methane ◽  
Community Members ◽  
Metabolic Potential ◽  
Oxidation Of Methane ◽  
Complete Set ◽  
Phylogenetic Composition

Terrestrial mud volcanoes (TMVs) are important natural sources of methane emission. The microorganisms inhabiting these environments remain largely unknown. We studied the phylogenetic composition and metabolic potential of the prokaryotic communities of TMVs located in the Taman Peninsula, Russia, using a metagenomic approach. One of the examined sites harbored a unique community with a high abundance of anaerobic methane-oxidizing archaea belonging to ANME-3 group (39% of all 16S rRNA gene reads). The high number of ANME-3 archaea was confirmed by qPCR, while the process of anaerobic methane oxidation was demonstrated by radioisotopic experiments. We recovered metagenome-assembled genomes (MAGs) of archaeal and bacterial community members and analyzed their metabolic capabilities. The ANME-3 MAG contained a complete set of genes for methanogenesis as well as of ribosomal RNA and did not encode proteins involved in dissimilatory nitrate or sulfate reduction. The presence of multiheme c-type cytochromes suggests that ANME-3 can couple methane oxidation with the reduction of metal oxides or with the interspecies electron transfer to a bacterial partner. The bacterial members of the community were mainly represented by autotrophic, nitrate-reducing, sulfur-oxidizing bacteria, as well as by fermentative microorganisms. This study extends the current knowledge of the phylogenetic and metabolic diversity of prokaryotes in TMVs and provides a first insight into the genomic features of ANME-3 archaea.

scholarly journals Biogeochemical evidence of anaerobic methane oxidation and anaerobic ammonium oxidation in a stratified lake using stable isotopes

2020 ◽  
Vol 17 (20) ◽  
pp. 5149-5161
Author(s):  
Florian Einsiedl ◽  
Anja Wunderlich ◽  
Mathieu Sebilo ◽  
Ömer K. Coskun ◽  
William D. Orsi ◽  
...  
Keyword(s):  
Stable Isotope ◽  
Methane Oxidation ◽  
Water Depth ◽  
Methane Concentration ◽  
Methane Emissions ◽  
Freshwater Ecosystems ◽  
Anaerobic Methane Oxidation ◽  
Ammonium Oxidation ◽  
Anaerobic Oxidation ◽  
Oxidation Of Methane

Abstract. Nitrate pollution of freshwaters and methane emissions into the atmosphere are crucial factors in deteriorating the quality of drinking water and in contributing to global climate change. The n-damo (nitrite-dependent anaerobic methane oxidation), nitrate-dependent anaerobic methane oxidation and the anaerobic oxidation of ammonium (anammox) represent two microbially mediated processes that can reduce nitrogen loading of aquatic ecosystems and associated methane emissions to the atmosphere. Here, we report vertical concentration and stable-isotope profiles of CH4, NO3-, NO2-, and NH4+ in the water column of Fohnsee (lake in southern Bavaria, Germany) that may indicate linkages between denitrification, anaerobic oxidation of methane (AOM), and anammox. At a water depth from 12 to 20 m, a methane–nitrate transition zone (NMTZ) was observed, where δ13C values of methane and δ15N and δ18O of dissolved nitrate markedly increased in concert with decreasing concentrations of methane and nitrate. These data patterns, together with the results of a simple 1-D diffusion model linked with a degradation term, show that the nonlinear methane concentration profile cannot be explained by diffusion and that microbial oxidation of methane coupled with denitrification under anaerobic conditions is the most parsimonious explanation for these data trends. In the methane zone at the bottom of the NMTZ (20 to 22 m) δ15N of ammonium increased by 4 ‰, while ammonium concentrations decreased. In addition, a strong 15N enrichment of dissolved nitrate was observed at a water depth of 20 m, suggesting that anammox is occurring together with denitrification. The conversion of nitrite to N2 and nitrate during anammox is associated with an inverse N isotope fractionation and may explain the observed increasing offset (Δδ15N) of 26 ‰ between δ15N values of dissolved nitrate and nitrite at a water depth of 20 m compared to the Δδ15Nnitrate-nitrite of 11 ‰ obtained in the NMTZ at a water depth between 16 and 18 m. The associated methane concentration and stable-isotope profiles indicate that some of the denitrification may be coupled to AOM, an observation supported by an increased concentration of bacteria known to be involved in n-damo/denitrification with AOM (NC10 and Crenothrix) and anammox (“Candidatus Anammoximicrobium”) whose concentrations were highest in the methane and ammonium oxidation zones, respectively. This study shows the potential for a coupling of microbially mediated nitrate-dependent methane oxidation with anammox in stratified freshwater ecosystems, which may be important for affecting both methane emissions and nitrogen concentrations in lakes.

scholarly journals Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea

PLoS Biology ◽  
2022 ◽  
Vol 20 (1) ◽  
pp. e3001508
Author(s):  
Grayson L. Chadwick ◽  
Connor T. Skennerton ◽  
Rafael Laso-Pérez ◽  
Andy O. Leu ◽  
Daan R. Speth ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Comparative Analysis ◽  
Comparative Genomics ◽  
Pure Culture ◽  
Methanogenic Archaea ◽  
Anaerobic Oxidation Of Methane ◽  
Genomic Features ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Reducing Bacteria

The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.

scholarly journals Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea

2003 ◽  
Vol 69 (9) ◽  
pp. 5483-5491 ◽  
Author(s):  
Steven J. Hallam ◽  
Peter R. Girguis ◽  
Christina M. Preston ◽  
Paul M. Richardson ◽  
Edward F. DeLong
Keyword(s):  
Methane Oxidation ◽  
Evolutionary Relationship ◽  
Methanogenic Archaea ◽  
Small Subunit ◽  
Anaerobic Methane Oxidation ◽  
Small Subunit Rrna ◽  
Genomic Context ◽  
Coenzyme M ◽  
Phylogenetic Groups ◽  
Methyl Coenzyme M Reductase

ABSTRACT Phylogenetic and stable-isotope analyses implicated two methanogen-like archaeal groups, ANME-1 and ANME-2, as key participants in the process of anaerobic methane oxidation. Although nothing is known about anaerobic methane oxidation at the molecular level, the evolutionary relationship between methane-oxidizing archaea (MOA) and methanogenic archaea raises the possibility that MOA have co-opted key elements of the methanogenic pathway, reversing many of its steps to oxidize methane anaerobically. In order to explore this hypothesis, the existence and genomic conservation of methyl coenzyme M reductase (MCR), the enzyme catalyzing the terminal step in methanogenesis, was studied in ANME-1 and ANME-2 archaea isolated from various marine environments. Clone libraries targeting a conserved region of the alpha subunit of MCR (mcrA) were generated and compared from environmental samples, laboratory-incubated microcosms, and fosmid libraries. Four out of five novel mcrA types identified from these sources were associated with ANME-1 or ANME-2 group members. Assignment of mcrA types to specific phylogenetic groups was based on environmental clone recoveries, selective enrichment of specific MOA and mcrA types in a microcosm, phylogenetic congruence between mcrA and small-subunit rRNA tree topologies, and genomic context derived from fosmid sequences. Analysis of the ANME-1 and ANME-2 mcrA sequences suggested the potential for catalytic activity based on conservation of active-site amino acids. These results provide a basis for identifying methanotrophic archaea with mcrA sequences and define a functional genomic link between methanogenic and methanotrophic archaea.

scholarly journals Biogeochemical and Molecular Signatures of Anaerobic Methane Oxidation in a Marine Sediment

2001 ◽  
Vol 67 (4) ◽  
pp. 1646-1656 ◽  
Author(s):  
Trine R. Thomsen ◽  
Kai Finster ◽  
Niels B. Ramsing
Keyword(s):  
Phylogenetic Analysis ◽  
Transition Zone ◽  
Methane Oxidation ◽  
Marine Sediment ◽  
Anaerobic Methane Oxidation ◽  
Molecular Signatures ◽  
Gene Sequences ◽  
Sulfate Reducing ◽  
Reducing Bacteria ◽  
Eel River Basin

ABSTRACT Anaerobic methane oxidation was investigated in 6-m-long cores of marine sediment from Aarhus Bay, Denmark. Measured concentration profiles for methane and sulfate, as well as in situ rates determined with isotope tracers, indicated that there was a narrow zone of anaerobic methane oxidation about 150 cm below the sediment surface. Methane could account for 52% of the electron donor requirement for the peak sulfate reduction rate detected in the sulfate-methane transition zone. Molecular signatures of organisms present in the transition zone were detected by using selective PCR primers for sulfate-reducing bacteria and for Archaea. One primer pair amplified the dissimilatory sulfite reductase (DSR) gene of sulfate-reducing bacteria, whereas another primer (ANME) was designed to amplify archaeal sequences found in a recent study of sediments from the Eel River Basin, as these bacteria have been suggested to be anaerobic methane oxidizers (K. U. Hinrichs, J. M. Hayes, S. P. Sylva, P. G. Brewer, and E. F. DeLong, Nature 398:802–805, 1999). Amplification with the primer pairs produced more amplificate of both target genes with samples from the sulfate-methane transition zone than with samples from the surrounding sediment. Phylogenetic analysis of the DSR gene sequences retrieved from the transition zone revealed that they all belonged to a novel deeply branching lineage of diverse DSR gene sequences not related to any previously described DSR gene sequence. In contrast, DSR gene sequences found in the top sediment were related to environmental sequences from other estuarine sediments and to sequences of members of the generaDesulfonema, Desulfococcus, andDesulfosarcina. Phylogenetic analysis of 16S rRNA sequences obtained with the primers targeting the archaeal group of possible anaerobic methane oxidizers revealed two clusters of ANME sequences, both of which were affiliated with sequences from the Eel River Basin.

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