Anaerobic oxidation of methane by sulfate in hypersaline groundwater of the Dead Sea aquifer

Avrahamov, Naama; Antler, Gilad; Yechieli, Yoseph; Gavrieli, Ittai; Joye, Samantha B.; Saxton, Matthew; Turchyn, Alexandra V.; Sivan, Orit

doi:10.1111/gbi.12095

Cited by 43 publications

(34 citation statements)

References 108 publications

(179 reference statements)

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“…Previous studies reported that sulfur-cycling AOM can induce sulfur isotope fractionation in marine environments and at sulfate concentrations in the millimolar range Antler et al, 2014Antler et al, , 2015Avrahamov et al, 2014;Deusner et al, 2014;Sivan et al, 2014). A few of these studies assigned ε AOM values of 20-30 for AOM in gas seeps (Deusner et al, 2014;Sivan et al, 2014) and suggested that AOM may cause fractionations of up to 60 in marine SMTZs Deusner et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies showed that sulfurcycling AOM impacts not only sulfur (δ 34 S SO4 ), but also oxygen isotopes (δ 18 O SO4 ) in the dissolved sulfate pool and apparently creates an unique pattern among them that can help to distinguish between organotrophic and methanotrophic SR to be the main drivers of the footprints (e.g., Antler et al, 2014Antler et al, , 2015Avrahamov et al, 2014;Deusner et al, 2014). Therefore, future studies may probably be best approached by combined investigations of oxygen and sulfur isotopes.…”

Section: Discussionmentioning

confidence: 99%

“…A few studies demonstrated that sulfur-cycling AOM influences δ 34 S signatures in the environment Borowski et al, 2013) and concurrently alters the oxygen isotopic value in sulfate Avrahamov et al, 2014;Deusner et al, 2014;Sivan et al, 2014). Two studies investigated sulfate-dependent AOM in slurry incubations fed with Black Sea microbial mats and seep sediments and suggested that AOMdriven sulfur isotope fractionation factors fall in the range of ∼20 to 40 in gas seeps (Deusner et al, 2014;Sivan et al, 2014) and may exceed 60 in marine sulfate-methane-transition zones (SMTZs; Deusner et al, 2014) .…”

Section: Introductionmentioning

confidence: 99%

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High Sulfur Isotope Fractionation Associated with Anaerobic Oxidation of Methane in a Low-Sulfate, Iron-Rich Environment

2016

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Sulfur isotope signatures provide key information for the study of microbial activity in modern systems and the evolution of the Earth surface redox system. Microbial sulfate reducers shift sulfur isotope distributions by discriminating against heavier isotopes. This discrimination is strain-specific and often suppressed at sulfate concentrations in the lower micromolar range that are typical to freshwater systems and inferred for ancient oceans. Anaerobic oxidation of methane (AOM) is a sulfate-reducing microbial process with a strong impact on global sulfur cycling in modern habitats and potentially in the geological past, but its impact on sulfur isotope signatures is poorly understood, especially in low-sulfate environments. We investigated sulfur cycling and 34 S fractionation in a low-sulfate freshwater sediment with biogeochemical conditions analogous to early Earth environments. The zone of highest AOM activity was associated in situ with a zone of strong 34 S depletions in the pool of reduced sulfur species, indicating a coupling of sulfate reduction (SR) and AOM at sulfate concentrations <50 1 µmol L − . In slurry incubations of AOM-active sediment, the addition of methane stimulated SR and induced a bulk sulfur isotope effect of ∼29 . Our results imply that sulfur isotope signatures may be strongly impacted by AOM even at sulfate concentrations two orders of magnitude lower than at present oceanic levels. Therefore, we suggest that sulfur isotope fractionation during AOM must be considered when interpreting 34 S signatures in modern and ancient environments.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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High Sulfur Isotope Fractionation Associated with Anaerobic Oxidation of Methane in a Low-Sulfate, Iron-Rich Environment

2016

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“…Only a few studies have measured both the sulfur and oxygen isotope fractionation during sulfate-driven AOM, predominantly in the environment (12,55,56,70,71). The overall sulfur isotope fractionation during AOM in seeps has been shown to be lower than the sulfur isotope fractionation of traditional organoclastic bacterial sulfate reduction or sulfate-driven AOM in long, diffusive profiles.…”

Section: Discussionmentioning

confidence: 99%

Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps

Sivan

Antler

Turchyn

et al. 2014

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

120

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Seep sediments are dominated by intensive microbial sulfate reduction coupled to the anaerobic oxidation of methane (AOM). Through geochemical measurements of incubation experiments with methane seep sediments collected from Hydrate Ridge, we provide insight into the role of iron oxides in sulfate-driven AOM. Seep sediments incubated with 13 C-labeled methane showed cooccurring sulfate reduction, AOM, and methanogenesis. The isotope fractionation factors for sulfur and oxygen isotopes in sulfate were about 40‰ and 22‰, respectively, reinforcing the difference between microbial sulfate reduction in methane seeps versus other sedimentary environments (for example, sulfur isotope fractionation above 60‰ in sulfate reduction coupled to organic carbon oxidation or in diffusive sedimentary sulfate-methane transition zone). The addition of hematite to these microcosm experiments resulted in significant microbial iron reduction as well as enhancing sulfate-driven AOM. The magnitude of the isotope fractionation of sulfur and oxygen isotopes in sulfate from these incubations was lowered by about 50%, indicating the involvement of iron oxides during sulfate reduction in methane seeps. The similar relative change between the oxygen versus sulfur isotopes of sulfate in all experiments (with and without hematite addition) suggests that oxidized forms of iron, naturally present in the sediment incubations, were involved in sulfate reduction, with hematite addition increasing the sulfate recycling or the activity of sulfur-cycling microorganisms by about 40%. These results highlight a role for natural iron oxides during bacterial sulfate reduction in methane seeps not only as nutrient but also as stimulator of sulfur recycling.redox | anaerobic respiration | deep-sea | methanotrophy | ANME archaea M icrobial dissimilatory processes generate energy through the decomposition of substrates, whereas assimilatory processes use substrates for intracellular biosynthesis of macromolecules. The most known and energetically favorable dissimilatory process is the oxidation of organic carbon coupled to oxygen as terminal electron acceptor (Eq. 1). In sediments with a high supply of organic carbon, oxygen can be depleted within the upper few millimeters, leading to anoxic conditions deeper in the sediment column. Under these conditions, microbial dissimilatory processes are coupled to the reduction of a series of other terminal electron acceptors besides oxygen (1). The largest free-energy yields are associated with nitrate reduction (denitrification), followed by manganese and iron oxide reduction, and then sulfate reduction. Due to the high concentration of sulfate in the ocean, dissimilatory bacterial sulfate reduction (Eq. 2) is responsible for the majority of organic matter oxidation in marine sediments (2). Below the depth of sulfate depletion, traditionally the only presumed process is methanogenesis (methane production), where its main pathways are fermentation of organic matter, mainly acetate (Eq. 3), or the reduction of carbon di...

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“…In spite of the high salinity in the modern Dead Sea, evidence for microbial sulfate reduction, likely coupled to anaerobic methane oxidation, has been found in ground water and sedimentary deposits (Oldenburg et al, 2000a,b;Gavrieli et al, 2001;Avrahamov et al, 2014;Thomas et al, 2016). Microbial sulfate reduction has been inferred from the coexistence of aqueous sulfate and sulfide, as well as measurements of sulfur isotopes that suggest a sulfur isotope fractionation of about 30 in the modern Dead Sea (Gavrieli et al, 2001).…”

Section: Introduction Overviewmentioning

confidence: 99%

Rates and Cycles of Microbial Sulfate Reduction in the Hyper-Saline Dead Sea over the Last 200 kyrs from Sedimentary δ34S and δ18O(SO4)

Torfstein

Turchyn

2017

Front. Earth Sci.

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We report the δ 34 S and δ 18 O (SO4) measured in gypsum, pyrite, and elemental sulfur through a 456-m thick sediment core from the center of the Dead Sea, representing the last ∼200 kyrs, as well as from the exposed glacial outcrops of the Masada M1 section located on the margins of the modern Dead Sea. The results are used to explore and quantify the evolution of sulfur microbial metabolism in the Dead Sea and to reconstruct the lake's water column configuration during the late Quaternary. Layers and laminae of primary gypsum, the main sulfur-bearing mineral in the sedimentary column, display the highest δ 34 S and δ 18 O (SO4) in the range of 13-28 and 13-30 , respectively. Within this group, gypsum layers deposited during interglacials display lower δ 34 S and δ 18 O (SO4) relative to those associated with glacial or deglacial stages. The reduced sulfur phases, including chromium reducible sulfur, and secondary gypsum crystals are characterized by extremely low δ 34 S in the range of −27 to +7 . The δ 18 O (SO4) of the secondary gypsum in the M1 outcrop ranges from 8 to 14 . The relationship between δ 34 S and δ 18 O (SO4) of primary gypsum suggests that the rate of microbial sulfate reduction was lower during glacial relative to interglacial times. This suggests that the freshening of the lake during glacial wet intervals, and the subsequent rise in sulfate concentrations, slowed the rate of microbial metabolism. Alternatively, this could imply that sulfate-driven anaerobic methane oxidation, the dominant sulfur microbial metabolism today, is a feature of the hypersalinity in the modern Dead Sea. Sedimentary sulfides are quantitatively oxidized during epigenetic exposure, retaining the lower δ 34 S signature; the δ 18 O (SO4) of this secondary gypsum is controlled by oxygen atoms derived equally from atmospheric oxygen and from water, which is likely a unique feature in this hyperarid environment.

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Anaerobic oxidation of methane by sulfate in hypersaline groundwater of the Dead Sea aquifer

Cited by 43 publications

References 108 publications

High Sulfur Isotope Fractionation Associated with Anaerobic Oxidation of Methane in a Low-Sulfate, Iron-Rich Environment

High Sulfur Isotope Fractionation Associated with Anaerobic Oxidation of Methane in a Low-Sulfate, Iron-Rich Environment

Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps

Rates and Cycles of Microbial Sulfate Reduction in the Hyper-Saline Dead Sea over the Last 200 kyrs from Sedimentary δ34S and δ18O(SO4)

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