Methylotrophic methanogenesis fuels cryptic methane cycling in marine surface sediment

Xiao, Ke‐Qing; Beulig, Felix; Røy, Hans; Jørgensen, Bo Barker; Risgaard-Petersen, Nils

doi:10.1002/lno.10788

Cited by 51 publications

(40 citation statements)

References 41 publications

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“…Although hydrogenotrophic methanogenesis was also detected at ROV2 and ROV3, the higher turnover of methylated compounds as well as the dominance of methylotrophic methanogens ( see below) suggested the methylotrophic pathway could be important for the concurrent methanogenesis with SR in the sulfate‐reducing sediments. Those results were in aggreement with previous studies, which experiemntally demonstrated that methane production in sulfate‐rich sediment could be driven by the fermentation of methylated compounds (Maltby et al ; Xiao et al ; Zhuang et al ).…”

Section: Discussionsupporting

confidence: 91%

Biogeochemistry, microbial activity, and diversity in surface and subsurface deep‐sea sediments of South China Sea

Zhuang

Liu

Liang

et al. 2019

Limnology & Oceanography

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Deep‐sea environments are the largest ecosystem of the global biosphere and constitute a crucial role in global biogeochemical cycles. We integrated biogeochemical and molecular ecological approaches to investigate microbial activity and diversity, with the goal of elucidating pathways and regulations of methane cycling and low molecular weight (LMW) compounds metabolism in different deep‐sea sediments of the South China Sea. We found that methanogenesis, anaerobic oxidation of methane, and sulfate reduction occurred concurrently with low rates in surface sediments of the Haima area (~ 50 cm push cores) and in subsurface sediments of the Shenhu area (~ 8 m piston core). In the presence of sulfate, methanogenesis was fueled by methylotrophic substrates, in agreement with thermodynamic calculations as well as the detection of the methylotrophic methanogenic genus Methanococcoides. Higher oxidation rates of LMW compounds than methanogenesis rates, suggested acetate, and to a lesser extent, methanol and methylamine, were predominantly utilized as an energy source by nonmethanogenic microorganisms (e.g., sulfate‐reducing bacteria). Diverse methanotrophic archaea (e.g., ANME‐1a/b and ANME‐2a/b) and sulfate‐reducing bacteria (e.g., Desulfarculaceae and Desulfobacteraceae) were observed and the abundance of mcrA and dsrA genes varied over depth and between sites. Dominant archaeal groups, such as Bathyarchaeota, Thermoplasmatale, Woesearchaeota, Lokiarchaeota, were consistently detected at both areas. Multivariate statistical analysis demonstrated sulfate was the most relevant environmental variable that correlated with the archaeal community composition. These results suggested that the presence of sulfate controlled methane cycling and LMW carbon metabolism pathways, and also affected the composition of the microbial community.

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Section: Discussionsupporting

confidence: 91%

Biogeochemistry, microbial activity, and diversity in surface and subsurface deep‐sea sediments of South China Sea

Zhuang

Liu

Liang

et al. 2019

Limnology & Oceanography

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“…As an alternative to a benthic source, methane could be produced in the water column as previously suggested (Sansone et al ) and supported by the detection of transcriptionally active methanogenic archaea at anoxic depths in the OMZ (Padilla et al ). Concomitant production and oxidation of methane has been observed in marine surface sediment, where the production is based on C 1 compounds that are not utilized by the otherwise dominating sulfate reducing bacteria (Xiao et al , ). Although methylotrophic methanogens in OMZ waters should face strong competition from nitrate/nitrite‐respiring methylotrophs (Beck et al ), they could potentially be active in nitrate and nitrite‐depleted microniches, e.g., inside organic‐rich aggregates (Bianchi et al ).…”

Section: Discussionmentioning

confidence: 99%

Anaerobic methane oxidation is an important sink for methane in the ocean's largest oxygen minimum zone

Thamdrup

Steinsdóttir

Bertagnolli

et al. 2019

Limnology & Oceanography

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We investigated methane oxidation in the oxygen minimum zone (OMZ) of the eastern tropical North Pacific (ETNP) off central Mexico. Methane concentrations in the anoxic core of the OMZ reached ~ 20 nmol L−1 at off shelf sites and 34 nmol L−1 at a shelf site. Rates of methane oxidation were determined in ship‐board incubations with 3H‐labeled methane at O2 concentrations 0–75 nmol L−1. In vertical profiles at off‐shelf stations, highest rates were found between the secondary nitrite maximum at ~ 130 m and the methane maximum at 300–400 m in the anoxic core. Methane oxidation was inhibited by addition of 1 μmol L−1 oxygen, which, together with the depth distribution, indicated an anaerobic pathway. A coupling to nitrite reduction was further indicated by the inhibitory effect of the nitric oxide scavenger 2‐phenyl‐4,4,5,5‐tetramethylimidazoline‐1‐oxyl‐3‐oxide (PTIO). Metatranscriptomes from the anoxic OMZ core supported the likely involvement of nitrite‐reducing bacteria of the NC10 clade in anaerobic methane oxidation, but also indicated a potential role for nitrate‐reducing euryarchaeotal methane oxidizers (ANME‐2d). Gammaproteobacteria of the Methanococcales were further detected in both 16S rRNA gene amplicons and metatranscriptomes, but the role of these presumed obligately aerobic methane oxidizers in the anoxic OMZ core is unclear. Given available estimates of water residence time, the measured rates and rate constants (up to ~ 1 yr−1) imply that anaerobic methane oxidation is a substantial methane sink in the ETNP OMZ and hence attenuates the emission of methane from this and possibly other OMZs.

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“…However, a similar trend was observed without molybdate addition and in N 2 amended controls ( Supplementary Figures S3-S5). The stimulation of ANMEs in the N 2 controls might have been due to methane supply via co-occurring methanogenesis in these incubations (Supplementary Figure S6) recently termed "cryptic methane cycling" and detected in the SMT of Aarhus Bay and other marine sediments Maltby et al, 2018;Xiao et al, 2018).…”

Section: Microbial Key Players Involved In Fe-aommentioning

confidence: 96%

Rates and Microbial Players of Iron-Driven Anaerobic Oxidation of Methane in Methanic Marine Sediments

et al. 2020

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The flux of methane, a potent greenhouse gas, from the seabed is largely controlled by anaerobic oxidation of methane (AOM) coupled to sulfate reduction (S-AOM) in the sulfate methane transition (SMT). S-AOM is estimated to oxidize 90% of the methane produced in marine sediments and is mediated by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria. An additional methane sink, i.e., iron oxide coupled AOM (Fe-AOM), has been suggested to be active in the methanic zone of marine sediments. Geochemical signatures below the SMT such as high dissolved iron, low to undetectable sulfate and high methane concentrations, together with the presence of iron oxides are taken as prerequisites for this process. So far, Fe-AOM has neither been proven in marine sediments nor have the governing key microorganisms been identified. Here, using a multidisciplinary approach, we show that Fe-AOM occurs in iron oxide-rich methanic sediments of the Helgoland Mud Area (North Sea). When sulfate reduction was inhibited, different iron oxides facilitated AOM in longterm sediment slurry incubations but manganese oxide did not. Especially magnetite triggered substantial Fe-AOM activity and caused an enrichment of ANME-2a archaea. Methane oxidation rates of 0.095 ± 0.03 nmol cm −3 d −1 attributable to Fe-AOM were obtained in short-term radiotracer experiments. The decoupling of AOM from sulfate reduction in the methanic zone further corroborated that AOM was iron oxide-driven below the SMT. Thus, our findings prove that Fe-AOM occurs in methanic marine sediments containing mineral-bound ferric iron and is a previously overlooked but likely important component in the global methane budget. This process has the potential to sustain microbial life in the deep biosphere.

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Methylotrophic methanogenesis fuels cryptic methane cycling in marine surface sediment

Cited by 51 publications

References 41 publications

Biogeochemistry, microbial activity, and diversity in surface and subsurface deep‐sea sediments of South China Sea

Biogeochemistry, microbial activity, and diversity in surface and subsurface deep‐sea sediments of South China Sea

Anaerobic methane oxidation is an important sink for methane in the ocean's largest oxygen minimum zone

Rates and Microbial Players of Iron-Driven Anaerobic Oxidation of Methane in Methanic Marine Sediments

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