Multiple evidence for methylotrophic methanogenesis as the dominant methanogenic pathway in hypersaline sediments from the Orca Basin, Gulf of Mexico

Zhuang, Guang‐Chao; Elling, Felix J.; Nigro, Lisa M.; Samarkin, V.; Joye, Samantha B.; Teske, Andreas; Hinrichs, Kai‐Uwe

doi:10.1016/j.gca.2016.05.005

Cited by 93 publications

(75 citation statements)

References 122 publications

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“…Likewise, acetate varied slightly within a narrow range between 1 and 5 μ mol L −1 at ROV2 and ROV3. Interestingly, methanol was more abundant at W22 (4.3–111 μ mol L −1 ), and the concentrations were higher than the reported values from different sediment settings of Japan Sea, Black Sea, and Gulf of Mexico (Zhuang et al ; Yanagawa et al ; Zhuang et al ). Instead of a dynamic equilibrium state, the accumulation of methanol with depth could be attributed to the elevated production or reduced consumption in the deeper sediment, which is supported by the increasing turnover time of methanol to CO 2 with depth.…”

Section: Discussionmentioning

confidence: 59%

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: Discussionmentioning

confidence: 59%

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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“…In spite of potential for methanogenesis in surface sediment which has been demonstrated by several earlier studies (Oremland et al, 1982; King, 1984; Mitterer et al, 2001; Maltby et al, 2016; Zhuang et al, 2016), methane production is seldom reflected in the geochemical profiles of CH 4 due to a characteristic concave-up shape most of the time, which is thought to be an indication of diffusion combined with net CH 4 oxidation (Iversen and Blackburn, 1981; Alperin et al, 1988). The closely coupled CH 4 production and oxidation in surface sediment in our study ( Figure 4 ) may partially explain this.…”

Section: Discussionmentioning

confidence: 92%

Concurrent Methane Production and Oxidation in Surface Sediment from Aarhus Bay, Denmark

et al. 2017

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Marine surface sediments, which are replete with sulfate, are typically considered to be devoid of endogenous methanogenesis. Yet, methanogenic archaea are present in those sediments, suggesting a potential for methanogenesis. We used an isotope dilution method based on sediment bag incubation and spiking with 13C-CH4 to quantify CH4 turnover rates in sediment from Aarhus Bay, Denmark. In two independent experiments, highest CH4 production and oxidation rates (>200 pmol cm-3 d-1) were found in the top 0–2 cm, below which rates dropped below 100 pmol cm-3 d-1 in all other segments down to 16 cm. This drop in overall methane turnover with depth was accompanied by decreasing rates of organic matter mineralization with depth. Molecular analyses based on quantitative PCR and MiSeq sequencing of archaeal 16S rRNA genes showed that the abundance of methanogenic archaea also peaked in the top 0–2 cm segment. Based on the community profiling, hydrogenotrophic and methylotrophic methanogens dominated among the methanogenic archaea in general, suggesting that methanogenesis in surface sediment could be driven by both CO2 reduction and fermentation of methylated compounds. Our results show the existence of elevated methanogenic activity and a dynamic recycling of CH4 at low concentration in sulfate-rich marine surface sediment. Considering the common environmental conditions found in other coastal systems, we speculate that such a cryptic methane cycling can be ubiquitous.

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“…This inhibition could be due to thermodynamics, where increases of methane concentration methanogenesis less favorable, due to the reduced Gibbs free energy yield. In contrast to hydrogenotrophic methanogenesis, methane production from methylated compounds are highly exergonic processes (Zhuang et al ), thus these processes are unlikely to be reversible. As a result, instead of the enzymatic back reaction of AOM, methane could be alternatively produced by methanogenic microorganisms.…”

Section: Discussionmentioning

confidence: 99%

“…Due to the high concentrations and production rates, methylamines might be the key metabolites fueling methanogenesis, particularly in salt marsh or hypersaline sediment (King 1988;McGenity 2010). In spite of the high turnover rate, the importance of methanol or methylamine for methane production requires further investigation, as the in situ abundance of those compounds and their precursors remains largely unconstrained in marine sediments (Wang and Lee 1995;Zhuang et al 2014;Zhuang et al 2017).…”

Section: Inhibitor Experimentsmentioning

confidence: 99%

“…For example, acetoclastic methanogenesis increased significantly with elevated temperature in deep subseafloor sediment (> 400 m) (Wellsbury et al ). In hypersaline environments, methylotrophic methanogenesis was the dominant methanogenic pathway (McGenity ; Lazar et al ; Zhuang et al ). Low pH appears to inhibit the production of methane in peatlands (Ye et al ).…”

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confidence: 99%

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Effects of pressure, methane concentration, sulfate reduction activity, and temperature on methane production in surface sediments of the Gulf of Mexico

Zhuang

Montgomery

Sibert

et al. 2018

Limnology & Oceanography

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Microbial methanogenesis is a known source of methane in marine environment, but the factors affecting the production of methane from different pathways remain largely unconstrained. We investigated the effects of pressure, methane concentration, temperature, and sulfate reduction activity on the conversion of methanogenic substrates to methane using radiotracers in nearshore and offshore surface sediments in the northern Gulf of Mexico. The transformation of bicarbonate to methane increased with methane concentrations under quasi in situ conditions of deep‐sea sediment, potentially reflecting, to some degree, enhancement of the enzymatic back reaction under high‐methane conditions. In coastal sediments, a positive effect of both increased methane concentration and inhibition of sulfate reduction by molybdate on 14CH4 accumulation suggests that anaerobic oxidation of methane and methanogenesis occur concurrently. In contrast, methane production from methanol was suppressed by increased methane concentration likely due to the reduced energy yield of methanogenesis at elevated methane concentrations. Temperature could limit hydrogenotrophic and acetoclastic methanogenesis under in situ conditions, as higher rates were observed at 40°C in nearshore sediments. Inhibitor experiments with 2‐bromoethanesulfonate and molybdate indicated that sulfate‐reducing bacteria preferentially utilized acetate, as well as H2. Methanol was a noncompetitive substrate for methanogens in the deep‐sea sediments but was competitively cycled in coastal sediments. An authentic noncompetitive substrate, methylamine, was channeled predominantly to methane production under all conditions tested. The different response of methanogenic activity to substrate availability, metabolic competition, temperature, and pressure between sites suggest variable environmental controls on the methane production in coastal vs. deep‐sea surface sediments.

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Multiple evidence for methylotrophic methanogenesis as the dominant methanogenic pathway in hypersaline sediments from the Orca Basin, Gulf of Mexico

Cited by 93 publications

References 122 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

Concurrent Methane Production and Oxidation in Surface Sediment from Aarhus Bay, Denmark

Effects of pressure, methane concentration, sulfate reduction activity, and temperature on methane production in surface sediments of the Gulf of Mexico

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