Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Anton Leeuwenhoek Int J G 81: 271-282

Scripps Institution of Oceanography, University of California at San Diego, 92093-0202, USA.
Antonie van Leeuwenhoek (Impact Factor: 1.81). 09/2002; 81(1-4):271-82. DOI: 10.1023/A:1020587206351
Source: PubMed


Evidence supporting a key role for anaerobic methane oxidation in the global methane cycle is reviewed. Emphasis is on recent microbiological advances. The driving force for research on this process continues to be the fact that microbial communities intercept and consume methane from anoxic environments, methane that would otherwise enter the atmosphere. Anaerobic methane oxidation is biogeochemically important because methane is a potent greenhouse gas in the atmosphere and is abundant in anoxic environments. Geochemical evidence for this process has been observed in numerous marine sediments along the continental margins, in methane seeps and vents, around methane hydrate deposits, and in anoxic waters. The anaerobic oxidation of methane is performed by at least two phylogenetically distinct groups of archaea, the ANME-1 and ANME-2. These archaea are frequently observed as consortia with sulfate-reducing bacteria, and the metabolism of these consortia presumably involves a syntrophic association based on interspecies electron transfer. The archaeal member of a consortium apparently oxidizes methane and shuttles reduced compounds to the sulfate-reducing bacteria. Despite recent advances in understanding anaerobic methane oxidation, uncertainties still remain regarding the nature and necessity of the syntrophic association, the biochemical pathway of methane oxidation, and the interaction of the process with the local chemical and physical environment. This review will consider the microbial ecology and biogeochemistry of anaerobic methane oxidation with a special emphasis on the interactions between the responsible organisms and their environment.

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    • "In the terrestrial environment, bacteria are mainly responsible for oxidizing methane to CO 2 using O 2 as the electron acceptor (Chistoserdova et al., 2005). In marine sediments archaea consume the majority of upward diffusing methane anaerobically through oxidation of methane (AOM) coupled to sulfate reduction (Valentine, 2002). AOM has also been shown to occur via denitrification (Raghoebarsing et al., 2006;Ettwig et al., 2009Ettwig et al., , 2010Haroon et al., 2013;Norði & Thamdrup, 2014;Shen et al., 2015). "
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    ABSTRACT: Methanogenesis, the microbial methane (CH4 ) production, is traditionally thought to anchor the mineralization of organic matter as the ultimate respiratory process in deep sediments, despite the presence of oxidized mineral phases, such as iron oxides. This process is carried out by archaea that have also been shown to be capable of reducing iron in high levels of electron donors such as hydrogen. The current pure culture study demonstrates that methanogenic archaea (Methanosarcina barkeri) rapidly switch from methanogenesis to iron-oxide reduction close to natural conditions, with nitrogen atmosphere, even when faced with substrate limitations. Intensive, biotic iron reduction was observed following the addition of poorly crystalline ferrihydrite and complex organic matter and was accompanied by inhibition of methane production. The reaction rate of this process was of the first order and was dependent only on the initial iron concentrations. Ferrous iron production did not accelerate significantly with the addition of 9,10-anthraquinone-2,6-disulfonate (AQDS) but increased by 11-28% with the addition of phenazine-1-carboxylate (PCA), suggesting the possible role of methanophenazines in the electron transport. The coupling between ferrous iron and methane production has important global implications. The rapid transition from methanogenesis to reduction of iron-oxides close to the natural conditions in sediments may help to explain the globally-distributed phenomena of increasing ferrous concentrations below the traditional iron reduction zone in the deep 'methanogenic' sediment horizon, with implications for metabolic networking in these subsurface ecosystems and in past geological settings.
    Full-text · Article · Jan 2016 · Geobiology
    • "Given the global biogeochemical relevance of anaerobic methane oxidation, as well as the role methane plays in atmospheric temperature regulation (Valentine, 2002), it is important to understand the structure and function of these deep-sea systems, which are likely critical components of the world's methane source-sink dynamics. More specifically, characterizing the biological diversity that occurs in each of these areas is necessary to understand their common as well as unique features, which may help unravel more completely their underlying biogeochemical properties. "
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    ABSTRACT: Chemosynthetic communities have been described from a variety of deep-sea environments across the world's oceans. They constitute very interesting biological systems in terms of their ecology, evolution and biogeography, and also given their potential as indicators of the presence and abundance of consistent hydrocarbon-based nutritional sources. Up to now such peculiar biotic assemblages have not been reported for the western South Atlantic Ocean, leaving this large region undocumented with respect to the presence, composition and history of such communities. Here we report on the presence of a chemosynthetic community off the coast of southern Brazil, in an area where high levels of methane and the presence of gas hydrates have been detected. We performed metagenomic analyses of the microbial community present at this site, and also employed molecular approaches to identify components of its benthic fauna. We conducted phylogenetic analyses comparing the components of this assemblage to those found elsewhere in the world, which allowed a historical assessment of the structure and dynamics of these systems. Our results revealed that the microbial community at this site is quite diverse, and contains many components that are very closely related to lineages previously sampled in ecologically similar environments across the globe. Anaerobic methanotrophic (ANME) archaeal groups were found to be very abundant at this site, suggesting that methane is indeed an important source of nutrition for this community. In addition, we document the presence at this site of a vestimentiferan siboglinid polychaete and the bivalve Acharax sp., both of which are typical components of deep-sea chemosynthetic communities. The remarkable similarity in biotic composition between this area and other deep-sea communities across the world supports the interpretation that these assemblages are historically connected across the global oceans, undergoing colonization from distant sites and influenced by local ecological features that select a stereotyped suite of specifically adapted organisms.
    No preview · Article · Oct 2015 · Marine and Petroleum Geology
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    • "This could explain the lack of sulfide inhibition in seep sediments that showed AOM activity under conditions where 10 – 15 mM sulfide was produced ( Nauhaus et al . , 2002 ; Valentine , 2002 ; Joye et al . , 2004 ) . "
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    ABSTRACT: 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.
    Full-text · Article · Oct 2015 · Frontiers in Microbiology
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