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 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 Comparative Analysis of Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in Anoxic Marine Sediments

2001 ◽  
Vol 67 (4) ◽  
pp. 1922-1934 ◽  
Author(s):  
V. J. Orphan ◽  
K.-U. Hinrichs ◽  
W. Ussler ◽  
C. K. Paull ◽  
L. T. Taylor ◽  
...  
Keyword(s):  
Marine Sediments ◽  
Sulfate Reducing Bacteria ◽  
Rrna Gene ◽  
Anaerobic Oxidation Of Methane ◽  
Ether Lipids ◽  
Methane Seep ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Close Relatives ◽  
Reducing Bacteria

ABSTRACT The oxidation of methane in anoxic marine sediments is thought to be mediated by a consortium of methane-consuming archaea and sulfate-reducing bacteria. In this study, we compared results of rRNA gene (rDNA) surveys and lipid analyses of archaea and bacteria associated with methane seep sediments from several different sites on the Californian continental margin. Two distinct archaeal lineages (ANME-1 and ANME-2), peripherally related to the orderMethanosarcinales, were consistently associated with methane seep marine sediments. The same sediments contained abundant13C-depleted archaeal lipids, indicating that one or both of these archaeal groups are members of anaerobic methane-oxidizing consortia. 13C-depleted lipids and the signature 16S rDNAs for these archaeal groups were absent in nearby control sediments. Concurrent surveys of bacterial rDNAs revealed a predominance of δ-proteobacteria, in particular, close relatives ofDesulfosarcina variabilis. Biomarker analyses of the same sediments showed bacterial fatty acids with strong 13C depletion that are likely products of these sulfate-reducing bacteria. Consistent with these observations, whole-cell fluorescent in situ hybridization revealed aggregations of ANME-2 archaea and sulfate-reducing Desulfosarcina andDesulfococcus species. Additionally, the presence of abundant 13C-depleted ether lipids, presumed to be of bacterial origin but unrelated to ether lipids of members of the orderDesulfosarcinales, suggests the participation of additional bacterial groups in the methane-oxidizing process. Although theDesulfosarcinales and ANME-2 consortia appear to participate in the anaerobic oxidation of methane in marine sediments, our data suggest that other bacteria and archaea are also involved in methane oxidation in these environments.

scholarly journals Pressure sensitivity of ANME-3 predominant anaerobic methane oxidizing community from coastal marine Lake Grevelingen sediment

2018 ◽  
Author(s):  
C. Cassarini ◽  
Y. Zhang ◽  
P. N. Lens
Keyword(s):  
Microbial Community ◽  
Anaerobic Oxidation Of Methane ◽  
Pressure Sensitivity ◽  
Methane Pressure ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Coastal Marine ◽  
Reducing Bacteria ◽  
Marine Lake Grevelingen ◽  
Lake Grevelingen

AbstractAnaerobic oxidation of methane (AOM) coupled to sulfate reduction is mediated by, respectively, anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria (SRB). When a microbial community from coastal marine Lake Grevelingen sediment, containing ANME-3 as the most abundant type of ANME, was incubated under a pressure gradient (0.1-40 MPa) for 77 days, ANME-3 was more pressure sensitive than the SRB. ANME-3 activity was higher at lower (0.1, 0.45 MPa) over higher (10, 20 and 40 MPa) CH4total pressures. Moreover, the sulfur metabolism was shifted upon changing the incubation pressure: only at 0.1 MPa elemental sulfur was detected in a considerable amount and SRB of theDesulfobacteralesorder were more enriched at elevated pressures than theDesulfubulbaceae. This study provides evidence that ANME-3 can be constrained at shallow environments, despite the scarce bioavailable energy, because of its pressure sensitivity. Besides, the association between ANME-3 and SRB can be steered by changing solely the incubation pressure.ImportanceAnaerobic oxidation of methane (AOM) coupled to sulfate reduction is a biological process largely occurring in marine sediments, which contributes to the removal of almost 90% of sedimentary methane, thereby controlling methane emission to the atmosphere. AOM is mediated by slow growing archaea, anaerobic methanotrophs (ANME) and sulfate reducing bacteria. The enrichment of these microorganisms has been challenging, especially considering the low solubility of methane at ambient temperature and pressure. Previous studies showed strong positive correlations between the growth of ANME and the methane pressure, since the higher the pressure the more methane is dissolved. In this research, a shallow marine sediment was incubated under methane pressure gradients. The investigated effect of pressure on the AOM-SR activity, the formation sulfur intermediates and the microbial community structure is important to understand the pressure influence on the processes and the activity of the microorganisms involved to further understand their metabolism and physiology.

scholarly journals In Vitro Study of Lipid Biosynthesis in an Anaerobically Methane-Oxidizing Microbial Mat

2005 ◽  
Vol 71 (8) ◽  
pp. 4345-4351 ◽  
Author(s):  
Martin Blumenberg ◽  
Richard Seifert ◽  
Katja Nauhaus ◽  
Thomas Pape ◽  
Walter Michaelis
Keyword(s):  
In Vitro Study ◽  
Methanogenic Archaea ◽  
Microbial Mat ◽  
The Black Sea ◽  
Anaerobic Oxidation Of Methane ◽  
Methane Cycle ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Lipid Compounds

ABSTRACT The anaerobic oxidation of methane (AOM) is a key process in the global methane cycle, and the majority of methane formed in marine sediments is oxidized in this way. Here we present results of an in vitro 13CH4 labeling study (δ13CH4, ∼5,400‰) in which microorganisms that perform AOM in a microbial mat from the Black Sea were used. During 316 days of incubation, the 13C uptake into the mat biomass increased steadily, and there were remarkable differences for individual bacterial and archaeal lipid compounds. The greatest shifts were observed for bacterial fatty acids (e.g., hexadec-11-enoic acid [16:1Δ11]; difference between the δ13C at the start and the end of the experiment [Δδ13Cstart-end], ∼160‰). In contrast, bacterial glycerol diethers exhibited only slight changes in δ13C (Δδ13Cstart-end, ∼10‰). Differences were also found for individual archaeal lipids. Relatively high uptake of methane-derived carbon was observed for archaeol (Δδ13Cstart-end, ∼25‰), a monounsaturated archaeol, and biphytanes, whereas for sn-2-hydroxyarchaeol there was considerably less change in the δ13C (Δδ13Cstart-end, ∼2‰). Moreover, an increase in the uptake of 13C for compounds with a higher number of double bonds within a suite of polyunsaturated 2,6,10,15,19-pentamethyleicosenes indicated that in methanotrophic archaea there is a biosynthetic pathway similar to that proposed for methanogenic archaea. The presence of group-specific biomarkers (for ANME-1 and ANME-2 associations) and the observation that there were differences in 13C uptake into specific lipid compounds confirmed that multiple phylogenetically distinct microorganisms participate to various extents in biomass formation linked to AOM. However, the greater 13C uptake into the lipids of the sulfate-reducing bacteria (SRB) than into the lipids of archaea supports the hypothesis that there is autotrophic growth of SRB on small methane-derived carbon compounds supplied by the methane oxidizers.

scholarly journals Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions

2008 ◽  
Vol 5 (3) ◽  
pp. 1933-1967 ◽  
Author(s):  
B. Orcutt ◽  
C. Meile
Keyword(s):  
Sulfate Reducing Bacteria ◽  
Substrate Affinity ◽  
Main Process ◽  
Anaerobic Oxidation Of Methane ◽  
Anaerobic Oxidation ◽  
Intermediate Species ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Reducing Bacteria ◽  
The Impact

Abstract. Anaerobic oxidation of methane (AOM) is the main process responsible for the removal of methane generated in Earth's marine subsurface environments. However, the biochemical mechanism of AOM remains elusive. By explicitly resolving the observed spatial arrangement of methanotrophic archaea and sulfate reducing bacteria found in consortia mediating AOM, potential intermediates involved in the electron transfer between the methane oxidizing and sulfate reducing partners were investigated via a consortium-scale reaction transport model that integrates the effect of diffusional transport with thermodynamic and kinetic controls on microbial activity. Model simulations were used to assess the impact of poorly constrained microbial characteristics such as minimum energy requirements to sustain metabolism, substrate affinity and cell specific rates. The role of environmental conditions such as the influence of methane levels on the feasibility of H2, formate and acetate as intermediate species, and the impact of the abundance of intermediate species on pathway reversal was examined. The results show that higher production rates of intermediates via AOM lead to increased diffusive fluxes from the methane oxidizing archaea to sulfate reducing bacteria, but the build-up of the exchangeable species causes the energy yield of AOM to drop below that required for ATP production. Comparison to data from laboratory experiments shows that under the experimental conditions of Nauhaus et al. (2007), neither hydrogen nor formate is exchanged fast enough between the consortia partners to achieve measured rates of metabolic activity, but that acetate exchange might support rates that approach those observed.

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

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

<p>Anaerobic oxidation of methane (AOM) is a globally important CH<sub>4</sub> sink that is offsetting potential CH<sub>4</sub> 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. NO<sub>3</sub><sup>-</sup>, Fe<sup>3+</sup>, SO<sub>4</sub><sup>2-</sup>), 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 – NO<sub>3</sub><sup>-</sup>, Fe<sup>3+</sup>, SO<sub>4</sub><sup>2-</sup>, and humic acids – 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 <sup>13</sup>C-CH<sub>4</sub> during AOM into CO<sub>2</sub> 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.</p><p>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 SO<sub>4</sub><sup>2-</sup> and humic acids were factors contributing to microbiome variation. Network analysis indicated that microbial communities involved in CH<sub>4</sub> 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 <sup>13</sup>C-enriched PLFA biomarkers confirming the incorporation of C-CH<sub>4</sub> into bacteria. AOM and <sup>13</sup>C-PLFA were significantly higher under Pig manure relative to other fertilizations. AOM was more intensive under NO<sub>3</sub><sup>-</sup> than Fe<sup>3+</sup> and humic acids, but was close to zero under SO<sub>4</sub><sup>2-</sup> amendment. However, the relative abundance of NC10 phylum which includes organisms performing AOM, and sulfate-reducing bacteria were higher under SO<sub>4</sub><sup>2-</sup>. The relative abundance of <em>Geobacter</em> was highest under biochar and NPK fertilization with SO<sub>4</sub><sup>2-</sup> and humic acids amendments. Taken together, NO<sub>3</sub><sup>-</sup>-driven AOM is the most potent AOM pathway in paddy soil, which however co-exists with the AOM pathways via reduction of NO<sub>2</sub><sup>- </sup>by NC10 bacteria and reduction of Fe<sup>3+</sup> and humic acids by consortia of ANME with <em>Geobacter</em>. Consequently, the co-occurrence network and evidence from <sup>13</sup>C incorporation into CO<sub>2</sub> and PLFAs indicate the multiple competitive pathways of AOM in paddy soil.</p>

scholarly journals Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions

2008 ◽  
Vol 5 (6) ◽  
pp. 1587-1599 ◽  
Author(s):  
B. Orcutt ◽  
C. Meile
Keyword(s):  
Sulfate Reducing Bacteria ◽  
Energy Yield ◽  
Main Process ◽  
Anaerobic Oxidation Of Methane ◽  
Anaerobic Oxidation ◽  
Intermediate Species ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Reducing Bacteria ◽  
The Impact

Abstract. Anaerobic oxidation of methane (AOM) is the main process responsible for the removal of methane generated in Earth's marine subsurface environments. However, the biochemical mechanism of AOM remains elusive. By explicitly resolving the observed spatial arrangement of methanotrophic archaea and sulfate reducing bacteria found in consortia mediating AOM, potential intermediates involved in the electron transfer between the methane oxidizing and sulfate reducing partners were investigated via a consortium-scale reaction transport model that integrates the effect of diffusional transport with thermodynamic and kinetic controls on microbial activity. Model simulations were used to assess the impact of poorly constrained microbial characteristics such as minimum energy requirements to sustain metabolism and cell specific rates. The role of environmental conditions such as the influence of methane levels on the feasibility of H2, formate and acetate as intermediate species, and the impact of the abundance of intermediate species on pathway reversal were examined. The results show that higher production rates of intermediates via AOM lead to increased diffusive fluxes from the methane oxidizing archaea to sulfate reducing bacteria, but the build-up of the exchangeable species can cause the energy yield of AOM to drop below that required for ATP production. Comparison to data from laboratory experiments shows that under the experimental conditions of Nauhaus et al. (2007), none of the potential intermediates considered here is able to support metabolic activity matching the measured rates.

scholarly journals Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

mBio ◽  
2021 ◽  
Vol 12 (3) ◽  
Author(s):  
Xiaojia He ◽  
Grayson L. Chadwick ◽  
Christopher P. Kempes ◽  
Victoria J. Orphan ◽  
Christof Meile
Keyword(s):  
Electron Transfer ◽  
Greenhouse Gas ◽  
Metabolic Activity ◽  
Electron Donors ◽  
Microbial Consortia ◽  
Anaerobic Oxidation Of Methane ◽  
Bacterial Cells ◽  
Model Simulations ◽  
Sulfate Reducing ◽  
Oxidation Of Methane

ABSTRACT About 382 Tg yr−1 of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia. IMPORTANCE Anaerobic oxidation of methane is a globally important, microbially mediated process reducing the emission of methane, a potent greenhouse gas. In this study, we investigate the mechanism of how a microbial consortium consisting of archaea and bacteria carries out this process and how these organisms interact with each other through the sharing of electrons. We present a process-based model validated by novel experimental measurements of the metabolic activity of individual, phylogenetically identified cells in very large (>20-μm-diameter) microbial aggregates. Model simulations indicate that extracellular electron transfer between archaeal and bacterial cells within a consortium is limited by potential losses and suggest that a flexible use of electron donors can provide energetic advantages for syntrophic consortia.

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