Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction

Scheller, Silvan; Yu, Hang; Chadwick, Grayson L.; McGlynn, Shawn E.; Orphan, Victoria J.

doi:10.1126/science.aad7154

Cited by 371 publications

(316 citation statements)

References 56 publications

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“…According to 16S rRNA gene sequences from wetland sediment samples performing AOM, anaerobic methanotrophic archaea (ANME), which are traditionally linked to anaerobic methanotrophy under sulfatereducing (2,26), Fe(III)-reducing (6,8), and artificial electron acceptor-reducing conditions (27), were barely detected in our experiments, with ANME-1b and ANME-3 representing less than 0.5% and 0.2%, respectively, from the archaeal community in all experimental treatments (Fig. 5).…”

Section: Figmentioning

confidence: 94%

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Valenzuela

Prieto-Davó

López-Lozano

et al. 2017

Appl Environ Microbiol

132

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Wetlands constitute the main natural source of methane on Earth due to their high content of natural organic matter (NOM), but key drivers, such as electron acceptors, supporting methanotrophic activities in these habitats are poorly understood. We performed anoxic incubations using freshly collected sediment, along with water samples harvested from a tropical wetland, amended with 13 C-methane (0.67 atm) to test the capacity of its microbial community to perform anaerobic oxidation of methane (AOM) linked to the reduction of the humic fraction of its NOM. Collected evidence demonstrates that electron-accepting functional groups (e.g., quinones) present in NOM fueled AOM by serving as a terminal electron acceptor. Indeed, while sulfate reduction was the predominant process, accounting for up to 42.5% of the AOM activities, the microbial reduction of NOM concomitantly occurred. Furthermore, enrichment of wetland sediment with external NOM provided a complementary electron-accepting capacity, of which reduction accounted for ϳ100 nmol 13 CH 4 oxidized · cm Ϫ3 · day Ϫ1 . Spectroscopic evidence showed that quinone moieties were heterogeneously distributed in the wetland sediment, and their reduction occurred during the course of AOM. Moreover, an enrichment derived from wetland sediments performing AOM linked to NOM reduction stoichiometrically oxidized methane coupled to the reduction of the humic analogue anthraquinone-2,6-disulfonate. Microbial populations potentially involved in AOM coupled to microbial reduction of NOM were dominated by divergent biota from putative AOMassociated archaea. We estimate that this microbial process potentially contributes to the suppression of up to 114 teragrams (Tg) of CH 4 · year Ϫ1 in coastal wetlands and more than 1,300 Tg · year Ϫ1 , considering the global wetland area. IMPORTANCEThe identification of key processes governing methane emissions from natural systems is of major importance considering the global warming effects triggered by this greenhouse gas. Anaerobic oxidation of methane (AOM) coupled to the microbial reduction of distinct electron acceptors plays a pivotal role in mitigating methane emissions from ecosystems. Given their high organic content, wetlands constitute the largest natural source of atmospheric methane. Nevertheless, processes controlling methane emissions in these environments are poorly understood. Here, we provide tracer analysis with 13 CH 4 and spectroscopic evidence revealing that AOM linked to the microbial reduction of redox functional groups in natural organic matter (NOM) prevails in a tropical wetland. We suggest that microbial reduction of NOM may largely contribute to the suppression of methane emissions from

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Section: Figmentioning

confidence: 94%

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Valenzuela

Prieto-Davó

López-Lozano

et al. 2017

Appl Environ Microbiol

132

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“…Only two studies investigated methane oxidation coupled to Fe 3+ or Mn 4+ reduction in naturally enriched samples of ANME-2 archaea. Using marine samples, Nauhaus et al reported that methane oxidation was not coupled to the reduction of ferrihydrite, iron citrate, humic acids, and anthraquinone-2,6-disulfonate (AQDS) (21), whereas recently Scheller et al showed that marine samples containing ANME-2a, ANME-2c, and other archaea oxidized methane in the presence of chelated iron and could couple methane oxidation activity to AQDS reduction (22). Nevertheless, in nature, metals predominantly occur in particulate forms, which are more difficult to access (15,16,19,23).…”

Section: Significancementioning

confidence: 99%

“…Recently, using a sample that contained ANME-2a and ANME-2c, Scheller et al reported 13 CO 2 production from 13 CH 4 oxidation in the presence of ferric citrate (22). Due to the notorious difficulties associated with measuring dissolved ferrous (Fe 2+ ) iron in complex media or natural samples, the stoichiometric relationship between the reduction of Fe 3+ and oxidation of CH 4 was not shown (22). Here, in a setup with destructive sampling, where total CO 2 and Fe 2+ could both be measured, we observed a near-perfect fit to the theoretically expected stoichiometry of 1:8 ( Fig.…”

Section: Significancementioning

confidence: 99%

Archaea catalyze iron-dependent anaerobic oxidation of methane

Ettwig

Zhu

Speth

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

514

419

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Anaerobic oxidation of methane (AOM) is crucial for controlling the emission of this potent greenhouse gas to the atmosphere. Nitrite-, nitrate-, and sulfate-dependent methane oxidation is welldocumented, but AOM coupled to the reduction of oxidized metals has so far been demonstrated only in environmental samples. Here, using a freshwater enrichment culture, we show that archaea of the order Methanosarcinales, related to "Candidatus ) were produced in stoichiometric amounts. Our study connects the previous finding of iron-dependent AOM to microorganisms detected in numerous habitats worldwide. Consequently, it enables a better understanding of the interaction between the biogeochemical cycles of iron and methane.anaerobic oxidation of methane | archaea | iron reduction | manganese reduction | multiheme proteins

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“…In marine seeps, AOM is predominantly catalyzed by a symbiosis of anaerobic methane-oxidizing euryarchaeotes (ANME) with sulfate-reducing bacteria (SRB), which form consortia of varying cell numbers (∼10 to ∼10 5 cells) and morphology (7,26). Their syntrophic partnership is hypothesized to be mediated by direct electron transfer (27)(28)(29) and/or diffusible intermediates (30,31).…”

Section: Significancementioning

confidence: 99%

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

Hatzenpichler

Connon

Goudeau

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

175

209

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To understand the biogeochemical roles of microorganisms in the environment, it is important to determine when and under which conditions they are metabolically active. Bioorthogonal noncanonical amino acid tagging (BONCAT) can reveal active cells by tracking the incorporation of synthetic amino acids into newly synthesized proteins. The phylogenetic identity of translationally active cells can be determined by combining BONCAT with rRNAtargeted fluorescence in situ hybridization (BONCAT-FISH). In theory, BONCAT-labeled cells could be isolated with fluorescenceactivated cell sorting (BONCAT-FACS) for subsequent genetic analyses. Here, in the first application, to our knowledge, of BONCAT-FISH and BONCAT-FACS within an environmental context, we probe the translational activity of microbial consortia catalyzing the anaerobic oxidation of methane (AOM), a dominant sink of methane in the ocean. These consortia, which typically are composed of anaerobic methane-oxidizing archaea (ANME) and sulfatereducing bacteria, have been difficult to study due to their slow in situ growth rates, and fundamental questions remain about their ecology and diversity of interactions occurring between ANME and associated partners. Our activity-correlated analyses of >16,400 microbial aggregates provide the first evidence, to our knowledge, that AOM consortia affiliated with all five major ANME clades are concurrently active under controlled conditions. Surprisingly, sorting of individual BONCAT-labeled consortia followed by whole-genome amplification and 16S rRNA gene sequencing revealed previously unrecognized interactions of ANME with members of the poorly understood phylum Verrucomicrobia. This finding, together with our observation that ANME-associated Verrucomicrobia are found in a variety of geographically distinct methane seep environments, suggests a broader range of symbiotic relationships within AOM consortia than previously thought.activity-based cell sorting | BONCAT | click chemistry | ecophysiology | single-cell microbiology

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Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction

Cited by 371 publications

References 56 publications

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Anaerobic Methane Oxidation Driven by Microbial Reduction of Natural Organic Matter in a Tropical Wetland

Archaea catalyze iron-dependent anaerobic oxidation of methane

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

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