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.

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 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 Microbial interactions in the anaerobic oxidation of methane: model simulations constrained by process rates and activity patterns

2019 ◽  
Vol 21 (2) ◽  
pp. 631-647 ◽  
Author(s):  
Xiaojia He ◽  
Grayson Chadwick ◽  
Christopher Kempes ◽  
Yimeng Shi ◽  
Shawn McGlynn ◽  
...  
Keyword(s):  
Activity Patterns ◽  
Microbial Interactions ◽  
Anaerobic Oxidation Of Methane ◽  
Anaerobic Oxidation ◽  
Model Simulations ◽  
Oxidation Of Methane

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

2020 ◽  
Author(s):  
Sabrina Beckmann ◽  
Ibrahim F. Farag ◽  
Rui Zhao ◽  
Glenn D Christman ◽  
Nancy G Prouty ◽  
...  
Keyword(s):  
Electron Acceptors ◽  
Nitrogen Compounds ◽  
Anaerobic Oxidation Of Methane ◽  
Cold Seeps ◽  
Authigenic Carbonates ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
The Pacific ◽  
Pacific Margin ◽  
Sulfur And Nitrogen Compounds

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.

scholarly journals ANME-2d anaerobic methanotrophic archaea differ from other ANME archaea in lipid composition and carbon source

2019 ◽  
Author(s):  
Julia M. Kurth ◽  
Nadine T. Smit ◽  
Stefanie Berger ◽  
Stefan Schouten ◽  
Mike S.M. Jetten ◽  
...  
Keyword(s):  
Carbon Source ◽  
Lipid Composition ◽  
Dissolved Inorganic Carbon ◽  
Carbon Sources ◽  
Freshwater Ecosystems ◽  
Anaerobic Oxidation Of Methane ◽  
Marine Environments ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Main Carbon Source

AbstractThe anaerobic oxidation of methane (AOM) is a microbial process present in marine and freshwater environments. AOM is important for reducing the emission of the second most important greenhouse gas methane. In marine environments anaerobic methanotrophic archaea (ANME) are involved in sulfate-reducing AOM. In contrast,Ca. Methanoperedens of the ANME-2d cluster carries out nitrate AOM in freshwater ecosystems. Despite the importance of those organisms for AOM in non-marine environments not much is known about their lipid composition or carbon sources. To close this gap, we analyzed the lipid composition of ANME-2d archaea and found that they mainly synthesize archaeol and hydroxyarchaeol as well as different (hydroxy-) glycerol dialkyl glycerol tetraethers, albeit in much lower amounts. Abundant lipid headgroups were dihexose, monomethyl-phosphatidyl ethanolamine and phosphatidyl hexose. Moreover, a monopentose was detected as a lipid headgroup which is rare among microorganisms. Batch incubations with13C labelled bicarbonate and methane showed that methane is the main carbon source of ANME-2d archaea varying from ANME-1 archaea which primarily assimilate dissolved inorganic carbon (DIC). ANME-2d archaea also assimilate DIC, but to a lower extent than methane. The lipid characterization and analysis of the carbon source ofCa.Methanoperedens facilitates distinction between ANME-2d and other ANMEs.

scholarly journals Anaerobic methanotrophic archaea of the ANME-2d clade feature lipid composition that differs from other ANME archaea

2019 ◽  
Vol 95 (7) ◽  
Author(s):  
Julia M Kurth ◽  
Nadine T Smit ◽  
Stefanie Berger ◽  
Stefan Schouten ◽  
Mike S M Jetten ◽  
...  
Keyword(s):  
Carbon Source ◽  
Lipid Composition ◽  
Dissolved Inorganic Carbon ◽  
Carbon Sources ◽  
Freshwater Ecosystems ◽  
Anaerobic Oxidation Of Methane ◽  
Marine Environments ◽  
Sulfate Reducing ◽  
Oxidation Of Methane ◽  
Main Carbon Source

ABSTRACTThe anaerobic oxidation of methane (AOM) is a microbial process present in marine and freshwater environments. AOM is important for reducing the emission of the second most important greenhouse gas methane. In marine environments anaerobic methanotrophic archaea (ANME) are involved in sulfate-reducing AOM. In contrast, Ca. Methanoperedens of the ANME-2d cluster carries out nitrate AOM in freshwater ecosystems. Despite the importance of those organisms for AOM in non-marine environments little is known about their lipid composition or carbon sources. To close this gap, we analysed the lipid composition of ANME-2d archaea and found that they mainly synthesise archaeol and hydroxyarchaeol as well as different (hydroxy-) glycerol dialkyl glycerol tetraethers, albeit in much lower amounts. Abundant lipid headgroups were dihexose, monomethyl-phosphatidyl ethanolamine and phosphatidyl hexose. Moreover, a monopentose was detected as a lipid headgroup that is rare among microorganisms. Batch incubations with 13C labelled bicarbonate and methane showed that methane is the main carbon source of ANME-2d archaea varying from ANME-1 archaea that primarily assimilate dissolved inorganic carbon (DIC). ANME-2d archaea also assimilate DIC, but to a lower extent than methane. The lipid characterisation and analysis of the carbon source of Ca. Methanoperedens facilitates distinction between ANME-2d and other ANMEs.

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

2009 ◽  
Vol 6 (5) ◽  
pp. 867-876 ◽  
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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