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

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.

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Pressure Selects Dominant Anaerobic Methanotrophic Phylotype and Sulfate Reducing Bacteria in Coastal Marine Lake Grevelingen Sediment

Frontiers in Environmental Science ◽

10.3389/fenvs.2018.00162 ◽

2019 ◽

Vol 6 ◽

Cited By ~ 9

Author(s):

Chiara Cassarini ◽

Yu Zhang ◽

Piet N. L. Lens

Keyword(s):

Sulfate Reducing Bacteria ◽

Sulfate Reducing ◽

Coastal Marine ◽

Reducing Bacteria ◽

Marine Lake Grevelingen ◽

Lake Grevelingen

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

Applied and Environmental Microbiology ◽

10.1128/aem.67.4.1922-1934.2001 ◽

2001 ◽

Vol 67 (4) ◽

pp. 1922-1934 ◽

Cited By ~ 454

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.

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

10.1101/2021.09.25.461819 ◽

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.

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

PLoS Biology ◽

10.1371/journal.pbio.3001508 ◽

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.

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Methane-related changes in prokaryotes along geochemical profiles in sediments of Lake Kinneret (Israel)

Biogeosciences ◽

10.5194/bg-12-2847-2015 ◽

2015 ◽

Vol 12 (10) ◽

pp. 2847-2860 ◽

Cited By ~ 12

Author(s):

I. Bar-Or ◽

E. Ben-Dov ◽

A. Kushmaro ◽

W. Eckert ◽

O. Sivan

Keyword(s):

Community Structure ◽

Microbial Community ◽

Methane Oxidation ◽

Microbial Community Structure ◽

Iron Reduction ◽

Sulfate Reducing Bacteria ◽

Lake Kinneret ◽

Anaerobic Oxidation Of Methane ◽

Sulfate Reducing ◽

Reducing Bacteria

Abstract. Microbial methane oxidation is the primary control on the emission of the greenhouse gas methane into the atmosphere. In terrestrial environments, aerobic methanotrophic bacteria are largely responsible for this process. In marine sediments, a coupling of anaerobic oxidation of methane (AOM) with sulfate reduction, often carried out by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria, consumes almost all methane produced within those sediments. Motivated by recent evidence for AOM with iron(III) in Lake Kinneret sediments, the goal of the present study was to link the geochemical gradients in the lake porewater to the microbial community structure. Screening of archaeal 16S rRNA gene sequences revealed a shift from hydrogenotrophic to acetoclastic methanogens with depth. The observed changes in microbial community structure suggest possible direct and indirect mechanisms for the AOM coupled to iron reduction in deep sediments. The percentage of members of the Nitrospirales order increased with depth, suggesting their involvement in iron reduction together with Geobacter genus and "reverse methanogenesis". An indirect mechanism through sulfate and ANME seems less probable due to the absence of ANME sequences. This is despite the abundant sequences related to sulfate-reducing bacteria (Deltaproteobacteria) together with the occurrence of dsrA in the deep sediment that could indicate the production of sulfate (disproportionation) from S0 for sulfate-driven AOM. The presence of the functional gene pmoA in the deep anoxic sediment together with sequences related to Methylococcales suggests the existence of a second unexpected indirect pathway – aerobic methane oxidation pathway in an anaerobic environment.

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Pressure Sensitivity of ANME-3 Predominant Anaerobic Methane Oxidizing Community from Coastal Marine Lake Grevelingen Sediment

Anaerobic Oxidation of Methane Coupled to the Reduction of Different Sulfur Compounds as Electron Acceptors in Bioreactors ◽

10.1201/9780429448300-4 ◽

2019 ◽

pp. 81-105

Author(s):

Chiara Cassarini

Keyword(s):

Pressure Sensitivity ◽

Coastal Marine ◽

Marine Lake Grevelingen ◽

Lake Grevelingen

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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

Biogeosciences Discussions ◽

10.5194/bgd-5-1933-2008 ◽

2008 ◽

Vol 5 (3) ◽

pp. 1933-1967 ◽

Cited By ~ 10

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.

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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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