Dataset Information

Cryptic CH4 cycling in the sulfate-methane transition of marine sediments apparently mediated by ANME-1 archaea.

ABSTRACT: Methane in the seabed is mostly oxidized to CO2 with sulfate as the oxidant before it reaches the overlying water column. This microbial oxidation takes place within the sulfate-methane transition (SMT), a sediment horizon where the downward diffusive flux of sulfate encounters an upward flux of methane. Across multiple sites in the Baltic Sea, we identified a systematic discrepancy between the opposing fluxes, such that more sulfate was consumed than expected from the 1:1 stoichiometry of methane oxidation with sulfate. The flux discrepancy was consistent with an oxidation of buried organic matter within the SMT, as corroborated by stable carbon isotope budgets. Detailed radiotracer experiments showed that up to 60% of the organic matter oxidation within the SMT first produced methane, which was concurrently oxidized to CO2 by sulfate reduction. This previously unrecognized "cryptic" methane cycling in the SMT is not discernible from geochemical profiles due to overall net methane consumption. Sedimentary gene pools suggested that nearly all potential methanogens within and beneath the SMT belonged to ANME-1 archaea, which are typically associated with anaerobic methane oxidation. Analysis of a metagenome-assembled genome suggests that predominant ANME-1 do indeed have the enzymatic potential to catalyze both methane production and consumption.

SUBMITTER: Beulig F

PROVIDER: S-EPMC6331549 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Cryptic CH<sub>4</sub> cycling in the sulfate-methane transition of marine sediments apparently mediated by ANME-1 archaea.

Beulig F F Røy H H McGlynn S E SE Jørgensen B B BB

The ISME journal 20180907 2

Methane in the seabed is mostly oxidized to CO<sub>2</sub> with sulfate as the oxidant before it reaches the overlying water column. This microbial oxidation takes place within the sulfate-methane transition (SMT), a sediment horizon where the downward diffusive flux of sulfate encounters an upward flux of methane. Across multiple sites in the Baltic Sea, we identified a systematic discrepancy between the opposing fluxes, such that more sulfate was consumed than expected from the 1:1 stoichiomet ...[more]

PMID: 30194429

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Project description:Extensive geochemical data showed that significant methane oxidation activity exists in marine sediments. The organisms responsible for this activity are anaerobic methane-oxidizing archaea (ANME) that occur in consortia with sulfate-reducing bacteria. A distinct zonation of different clades of ANME (ANME-1, ANME-2a/b, and ANME-2c) exists in marine sediments, which could be related to the localized concentrations of methane, sulfate, and sulfide. In order to test this hypothesis we performed long-term incubation of marine sediments under defined conditions with methane as a headspace gas: low or high sulfate (±4 and ±21 mM, respectively) in combination with low or high sulfide (±0.1 and ±4 mM, respectively) concentrations. Control incubations were also performed, with only methane, high sulfate, or high sulfide. Methane oxidation was monitored and growth of subtypes ANME-1, ANME-2a/b, and ANME-2c assessed using qPCR analysis. A preliminary archaeal community analysis was performed to gain insight into the ecological and taxonomic diversity. Almost all of the incubations with methane had methane oxidation activity, with the exception of the incubations with combined low sulfate and high sulfide concentrations. Sulfide inhibition occurred only with low sulfate concentrations, which could be due to the lower Gibbs free energy available as well as sulfide toxicity. ANME-2a/b appears to mainly grow in incubations which had high sulfate levels and methane oxidation activity, whereas ANME-1 did not show this distinction. ANME-2c only grew in incubations with only sulfate addition. These findings are consistent with previously published in situ profiling analysis of ANME subclusters in different marine sediments. Interestingly, since all ANME subtypes also grew in incubations with only methane or sulfate addition, ANME may also be able to perform anaerobic methane oxidation under substrate limited conditions or alternatively perform additional metabolic processes.

Project description:As marine sediments are buried, microbial communities transition from sulfate-reduction to methane-production after sulfate is depleted. When this biogenic methane diffuses into the overlying sulfate-rich sediments, it forms a sulfate-methane transition zone (SMTZ) because sulfate reducers deplete hydrogen concentrations and make hydrogenotrophic methanogenesis exergonic in the reverse direction, a process called the anaerobic oxidation of methane (AOM). Microbial participation in these processes is often inferred from geochemistry, genes, and gene expression changes with sediment depth, using sedimentation rates to convert depth to time. Less is known about how natural sediments transition through these geochemical states transition in real-time. We examined 16S rRNA gene amplicon libraries and metatranscriptomes in microcosms of anoxic sediment from the White Oak River estuary, NC, with three destructively sampled replicates with methane added (586-day incubations) and three re-sampled un-amended replicates (895-day incubations). Sulfate dropped to a low value (∼0.3 mM) on similar days for both experiments (312 and 320 days, respectively), followed by a peak in hydrogen, intermittent increases in methane-cycling archaea starting on days 375 and 362 (mostly Methanolinea spp. and Methanosaeta spp., and Methanococcoides sp. ANME-3), and a methane peak 1 month later. However, methane δ13C values only show net methanogenesis 6 months after methane-cycling archaea increase and 4 months after the methane peak, when sulfate is consistently below 0.1 mM and hydrogen increases to a stable 0.61 ± 0.13 nM (days 553-586, n = 9). Sulfate-reducing bacteria (mostly Desulfatiglans spp. and Desulfosarcina sp. SEEP-SRB1) increase in relative abundance only during this period of net methane production, suggesting syntrophy with methanogens in the absence of sulfate. The transition from sulfate reduction to methane production in marine sediments occurs through a prolonged period of methane-cycling by methanogens at low sulfate concentrations, and steady growth of sulfate reducers along with methanogens after sulfate is depleted.

Dataset Information

Cryptic CH4 cycling in the sulfate-methane transition of marine sediments apparently mediated by ANME-1 archaea.

Publications

Cryptic CH<sub>4</sub> cycling in the sulfate-methane transition of marine sediments apparently mediated by ANME-1 archaea.

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