Acetogenesis from CO<sub>2</sub> in an anoxic marine sediment

Hoehler, Tori M.; Albert, Daniel B.; Alperin, Marc J.; Martens, Christopher S.

doi:10.4319/lo.1999.44.3.0662

Cited by 72 publications

(38 citation statements)

References 30 publications

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“…This phenomenon is consistent with the observed (23, 24) accumulation of labile VFAs in anoxic marine sediments for which no mechanism had been identified (25). Although shifts in the microbial community composition could explain varying patterns of substrate abundance (26), VFA accumulation at low temperatures in the absence of apparent microbial population transitions or substrate limitations has been documented (6,(23)(24)(25)27), and differential temperature responses of functional microbial groups can explain such results. The temperature-limited capacity of the hydrolytic͞fermentative production of labile LMW-DOC during the summer months may generate a ''bottleneck'' in organic matter mineralization, leading to carbon limitation of the terminal metabolic microbial community at certain times of year.…”

Section: Discussionsupporting

confidence: 85%

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Weston

Joye

2005

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

111

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The long-term burial of organic carbon in sediments results in the net accumulation of oxygen in the atmosphere, thereby mediating the redox state of the Earth's biosphere and atmosphere. Sediment microbial activity plays a major role in determining whether particulate organic carbon is recycled or buried. A diverse consortium of microorganisms that hydrolyze, ferment, and terminally oxidize organic compounds mediates anaerobic organic matter mineralization in anoxic sediments. Variable temperature regulation of the sequential processes, leading from the breakdown of complex particulate organic carbon to the production and subsequent consumption of labile, low-molecular weight, dissolved intermediates, could play a key role in controlling rates of overall organic carbon mineralization. We examined sediment organic carbon cycling in a sediment slurry and in flow through bioreactor experiments. The data show a variable temperature response of the microbial functional groups mediating organic matter mineralization in anoxic marine sediments, resulting in the temperaturedriven decoupling of the production and consumption of organic intermediates. This temperature-driven decoupling leads to the accumulation of labile, low-molecular weight, dissolved organic carbon at low temperatures and low-molecular weight dissolved organic carbon limitation of terminal metabolism at higher temperatures.carbon cycle ͉ fermentation ͉ terminal metabolism ͉ sulfate reduction M icrobes performing the terminal mineralization of organic carbon to metabolic end products ( Fig. 1) are limited largely to labile, low-molecular weight (LMW), dissolved organic matter [LMW-dissolved organic carbon (DOC)] (molecular mass, Ͻ600 Da) that can be transported across cellular membranes (1). Particulate organic matter is initially broken down into high-molecular weight dissolved organic matter through extracellular enzymatic hydrolysis. High-molecular weight dissolved organic matter is further hydrolyzed and fermented to LMW-DOC, such as volatile fatty acids (VFAs) (2-4), that are available for terminal metabolism ( Fig. 1) (2,5,6). Despite the importance of hydrolysis͞fermentation in organic matter mineralization, relatively little is known about the environmental controls on this process.We examined the regulation of organic carbon mineralization in anoxic coastal marine sediments. A large fraction (55%) of global sediment organic matter oxidation occurs in coastal marine sediments, even though they account for only 7.5% of the total area of marine sediments (7,8). High metabolic rates in these sediments deplete oxygen within millimeters of the sediment-water interface, and the majority of organic matter mineralization proceeds via anaerobic pathways (9), mainly sulfate reduction (9-12). The organic carbon consumed by sulfatereducing bacteria is often VFAs, such as acetic acid (5, 6).Temperature and substrate availability influence the rates and seasonal patterns of microbial activity (13) and, hence, organic matter mineralization (14). For instance,...

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Section: Discussionsupporting

confidence: 85%

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Weston

Joye

2005

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

111

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“…Additionally, this zone is often accompanied by peak hydrogen sulfide and bicarbonate concentrations. Laboratory experiments demonstrated that during the transition from sulfate reduction to methanogenesis, there is a decoupling of H 2 production and consumption and hence a temporary accumulation of H 2 (Hoehler et al, 1999). Isotopic evidence for acetogenesis via CO 2 reduction in an extended sediment interval just below the SMTZ at the Cascadia Margin is also consistent with elevated H 2 concentration in situ (Heuer et al, 2009).…”

Section: Implications For Anoxic Environmentssupporting

confidence: 51%

Microbial conversion of inorganic carbon to dimethyl sulfide in anoxic lake sediment (Plußsee, Germany)

et al. 2010

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Abstract. In anoxic environments, volatile methylated sulfides like methanethiol (MT) and dimethyl sulfide (DMS) link the pools of inorganic and organic carbon with the sulfur cycle. However, direct formation of methylated sulfides from reduction of dissolved inorganic carbon has previously not been demonstrated. When studying the effect of temperature on hydrogenotrophic microbial activity, we observed formation of DMS in anoxic sediment of Lake Plußsee at 55 • C. Subsequent experiments strongly suggested that the formation of DMS involves fixation of bicarbonate via a reductive pathway in analogy to methanogenesis and engages methylation of MT. DMS formation was enhanced by addition of bicarbonate and further increased when both bicarbonate and H 2 were supplemented. Inhibition of DMS formation by 2-bromoethanesulfonate points to the involvement of methanogens. Compared to the accumulation of DMS, MT showed the opposite trend but there was no apparent 1:1 stoichiometric ratio between both compounds. Both DMS and MT had negative δ 13 C values of −62‰ and −55‰, respectively. Labeling with NaH 13 CO 3 showed more rapid incorporation of bicarbonate into DMS than into MT. The stable carbon isotopic evidence implies that bicarbonate was fixed via a reductive pathway of methanogenesis, and the generated methyl coenzyme M became the methyl donor for MT methylation. Neither DMS nor MT accumulation were stimulated by addition of the methyl-group donors methanol and syringic acid or by the methyl-group acceptor hydrogen sulphide. The source of MT was further investigated in a H 35 2 S labeling experiment, which demonstrated a microbially-mediated process of hydrogen sulfide methyCorrespondence to: Y. S. Lin (yushih@uni-bremen.de) lation to MT that accounted for only <10% of the accumulation rates of DMS. Therefore, the major source of the 13 C-depleted MT was neither bicarbonate nor methoxylated aromatic compounds. Other possibilities for isotopically depleted MT, such as other organic precursors like methionine, are discussed. This DMS-forming pathway may be relevant for anoxic environments such as hydrothermally influenced sediments and fluids and sulfate-methane transition zones in marine sediments.

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“…Although the amount of sulfate (0.16 mM) may be above the threshold for sulfate reduction, at least some of this may be the product of recent sulfide oxidation. Inhibition of SRB, which usually outcompete homoacetogens for H 2 , could explain the detection of hydrogen and the abundance of acetogens in the lake (Hoehler et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

An oligarchic microbial assemblage in the anoxic bottom waters of a volcanic subglacial lake

et al. 2008

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In 2006, we sampled the anoxic bottom waters of a volcanic lake beneath the Vatnajö kull ice cap (Iceland). The sample contained 5 Â 10 5 cells per ml, and whole-cell fluorescent in situ hybridization (FISH) and PCR with domain-specific probes showed these to be essentially all bacteria, with no detectable archaea. Pyrosequencing of the V6 hypervariable region of the 16S ribosomal RNA gene, Sanger sequencing of a clone library and FISH-based enumeration of four major phylotypes revealed that the assemblage was dominated by a few groups of putative chemotrophic bacteria whose closest cultivated relatives use sulfide, sulfur or hydrogen as electron donors, and oxygen, sulfate or CO 2 as electron acceptors. Hundreds of other phylotypes are present at lower abundance in our V6 tag libraries and a rarefaction analysis indicates that sampling did not reach saturation, but FISH data limit the remaining biome to o10-20% of all cells. The composition of this oligarchy can be understood in the context of the chemical disequilibrium created by the mixing of sulfidic lake water and oxygenated glacial meltwater.

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Acetogenesis from CO₂ in an anoxic marine sediment

Abstract: A combination of radiotracer and pore-water concentration measurements provide evidence for the occurrence of acetogenesis from CO 2 in anoxic marine sediments that are ordinarily dominated by sulfate reduction and methanogenesis.

Cited by 72 publications

References 30 publications

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Microbial conversion of inorganic carbon to dimethyl sulfide in anoxic lake sediment (Plußsee, Germany)

An oligarchic microbial assemblage in the anoxic bottom waters of a volcanic subglacial lake

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Acetogenesis from CO2 in an anoxic marine sediment

Abstract: A combination of radiotracer and pore-water concentration measurements provide evidence for the occurrence of acetogenesis from CO 2 in anoxic marine sediments that are ordinarily dominated by sulfate reduction and methanogenesis.

Cited by 72 publications

References 30 publications

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Temperature-driven decoupling of key phases of organic matter degradation in marine sediments

Microbial conversion of inorganic carbon to dimethyl sulfide in anoxic lake sediment (Plußsee, Germany)

An oligarchic microbial assemblage in the anoxic bottom waters of a volcanic subglacial lake

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Acetogenesis from CO₂ in an anoxic marine sediment