Microbial Drivers of Methane Emissions from Unrestored Industrial Salt Ponds
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Wetlands are important carbon sinks, yet many have been destroyed and converted to other uses over the past few centuries, including industrial salt making. A renewed focus on wetland ecosystem services (e.g., flood control, habitat) has resulted in numerous restoration efforts whose effect on microbial communities is largely unexplored. We investigated the impact of restoration on microbial community composition, metabolic functional potential, and methane flux by analyzing sediment cores from two unrestored former industrial salt ponds, a restored former industrial salt pond, and a historic wetland. We observed elevated methane emissions from unrestored salt ponds compared to the restored and historic wetlands, which was positively correlated with salinity and sulfate. 16S amplicon and shotgun metagenomic data revealed that the restored salt pond harbored communities more phylogenetically and functionally similar to the historic wetland than to unrestored ponds. Archaeal methanogenesis genes were positively correlated with methane flux, as were genes encoding enzymes for bacterial methylphosphonate degradation, suggesting methane is generated both from bacterial methylphosphonate degradation and archaeal methanogenesis in these sites. These observations demonstrate that restoration effectively converted industrial salt pond microbial communities back to compositions more similar to historic wetlands and lowered salinities, sulfate concentrations and methane emissions.Anaerobic methane oxidation is a globally important but poorly understood process. Four lines of evidence have recently improved our understanding of this process. First, studies of recent marine sediments indicate that a consortium of methanogens and sulphate-reducing bacteria are responsible for anaerobic methane oxidation; a mechanism of 'reverse methanogenesis' was proposed, based on the principle of interspecies hydrogen transfer. Second, studies of known methanogens under low hydrogen and high methane conditions were unable to induce methane oxidation, indicating that 'reverse methanogenesis' is not a widespread process in methanogens. Third, lipid biomarker studies detected isotopically depleted archaeal and bacterial biomarkers from marine methane vents, and indicate that Archaea are the primary consumers of methane. Finally, phylogenetic studies indicate that only specific groups of Archaea and SRB are involved in methane oxidation. This review integrates results from these recent studies to constrain the responsible mechanisms.
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Methanogenesis has recently been shown to fuel anaerobic oxidation of methane (AOM) within the sulfate-reducing zone of marine sediments, coining the term "cryptic methane cycle". Here we present research on the relationship between methanogenesis and AOM in a shallow hypersaline pool (∼130 PSU) within a southern California coastal wetland. Sediment (top 20 cm) was subjected to geochemical analyses, in-vitro slurry experiments, and radiotracer incubations using 35S-SO42−, 14C-mono-methylamine, and 14C-CH4, to study sulfate reduction, methylotrophic methanogenesis, and AOM. An adapted radioisotope method was used to follow cryptic methane cycling in 14C-mono-methylamine labeling incubations with increasing incubation times (1 hour to three weeks). Results showed peaks in AOM (max 13 nmol cm−3 d−1) and sulfate reduction activity (max 728 nmol cm−3 d−1) within the top 6 cm. Below 6 cm, AOM activity continued (max 15 nmol cm−3 d−1), while sulfate reduction was absent despite 67 mM sulfate, suggesting AOM was coupled to the reduction of iron. Methane concentrations were low (<50 nM) throughout the sediment. Batch sediment slurry incubations with methylated substrates (mono-methylamine and methanol) stimulated methanogenesis, pointing to the presence of methylotrophic methanogens. Incubations with 14C-mono-methylamine revealed the simultaneous activity of methanogenesis and coupled AOM through the stepwise transfer of 14C from mono-methylamine to CO2 via methane. Our results suggest that AOM is a crucial process in coastal wetland sediments to prevent the buildup of methane in the sulfate-reducing zone. We propose that cryptic methane cycling has been largely overlooked in coastal wetlands resulting in incomplete understanding of carbon cycling in this environment.
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Freshwater ecosystems are responsible for an important part of the methane (CH4) emissions which are likely to change with global warming. This study aims to evaluate temperature-induced (from 5 to 20 °C) changes on microbial community structure and methanogenic pathways in five sub-Antarctic lake sediments from Magallanes strait to Cape Horn, Chile. We combined in situ CH4 flux measurements, CH4 production rates (MPRs), gene abundance quantification and microbial community structure analysis (metabarcoding of the 16S rRNA gene). Under unamended conditions, a temperature increase of 5 °C doubled MPR while microbial community structure was not affected. Stimulation of methanogenesis by methanogenic precursors as acetate and H2/CO2, resulted in an increase of MPRs up to 127-fold and 19-fold, respectively, as well as an enrichment of mcrA-carriers strikingly stronger under acetate amendment. At low temperatures, H2/CO2-derived MPRs were considerably lower (down to 160-fold lower) than the acetate-derived MPRs, but the contribution of hydrogenotrophic methanogenesis increased with temperature. Temperature dependence of MPRs was significantly higher in incubations spiked with H2/CO2 (c. 1.9 eV) compared to incubations spiked with acetate or unamended (c. 0.8 eV). Temperature was not found to shape the total microbial community structure, that rather exhibited a site-specific variability among the studied lakes. However, the methanogenic archaeal community structure was driven by amended methanogenic precursors with a dominance of Methanobacterium in H2/CO2-based incubations and Methanosarcina in acetate-based incubations. We also suggested the importance of acetogenic H2-production outcompeting hydrogenotrohic methanogenesis especially at low temperatures, further supported by homoacetogen proportion in the microcosm communities. The combination of in situ-, and laboratory-based measurements and molecular approaches indicates that the hydrogenotrophic pathway may become more important with increasing temperatures than the acetoclastic pathway. In a continuously warming environment driven by climate change, such issues are crucial and may receive more attention.
Methanobacterium
Methanosaeta
Dominance (genetics)
Acetogenesis
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A series of molecular and geochemical studies were performed to study microbial, coal bed methane formation in the eastern Illinois Basin. Results suggest that organic matter is biodegraded to simple molecules, such as H(2) and CO(2), which fuel methanogenesis and the generation of large coal bed methane reserves. Small-subunit rRNA analysis of both the in situ microbial community and highly purified, methanogenic enrichments indicated that Methanocorpusculum is the dominant genus. Additionally, we characterized this methanogenic microorganism using scanning electron microscopy and distribution of intact polar cell membrane lipids. Phylogenetic studies of coal water samples helped us develop a model of methanogenic biodegradation of macromolecular coal and coal-derived oil by a complex microbial community. Based on enrichments, phylogenetic analyses, and calculated free energies at in situ subsurface conditions for relevant metabolisms (H(2)-utilizing methanogenesis, acetoclastic methanogenesis, and homoacetogenesis), H(2)-utilizing methanogenesis appears to be the dominant terminal process of biodegradation of coal organic matter at this location.
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Summary While it is clear that microbial consortia containing Archaea and sulfate‐reducing bacteria (SRB) can mediate the anaerobic oxidation of methane (AOM), the interplay between these microorganisms remains unknown. The leading explanation of the AOM metabolism is ‘reverse methanogenesis’ by which a methanogenesis substrate is produced and transferred between species. Conceptually, the reversal of methanogenesis requires low H 2 concentrations for energetic favourability. We used 13 C‐labelled CH 4 as a tracer to test the effects of elevated H 2 pressures on incubations of active AOM sediments from both the Eel River basin and Hydrate Ridge. In the presence of H 2 , we observed a minimal reduction in the rate of CH 4 oxidation, and conclude H 2 does not play an interspecies role in AOM. Based on these results, as well as previous work, we propose a new model for substrate transfer in AOM. In this model, methyl sulfides produced by the Archaea from both CH 4 oxidation and CO 2 reduction are transferred to the SRB. Metabolically, CH 4 oxidation provides electrons for the energy‐yielding reduction of CO 2 to a methyl group (‘methylogenesis’). Methylogenesis is a dominantly reductive pathway utilizing most methanogenesis enzymes in their forward direction. Incubations of seep sediments demonstrate, as would be expected from this model, that methanethiol inhibits AOM and that CO can be substituted for CH 4 as the electron donor for methylogenesis.
Sulfate-Reducing Bacteria
Methanethiol
Microbial Metabolism
Acetogenesis
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Two different fluid venting structures, marine cold seeps of the Black Sea and terrestrial mud volcanoes of Italy, were part of this thesis. Both were formed by the expulsion of water, mud and gases, which consist mainly of methane and higher hydrocarbons. The methane gas acts as substrate for various microorganisms, which perform, amongst other, the anaerobic oxidation of methane (AOM). The AOM is one key process of the methane consumption in the oceans worldwide. According to phylogenetic and metagenomic analyses, the AOM is mediated by consortia of anaerobic methane oxidizing archaea (ANME) and sulfate reducing bacteria (SRB). To get a deeper insight into the methanotrophic consortia, microbial mats of the Black Sea were used to assign one of the specific key enzymes of the methanogenesis to the AOM-performing microorganism. By using a specific antibody as marker, the metabolic activity of one part of the syntrophic partners could be identified. The key enzyme methyl coenzyme M reductase (MCR) of the (reverse) methanogenic pathway was detected on cellular and sub-cellular level in the ANME cells. The study confirms the assumption of the reversed methanogenic pathway for the anaerobic oxidation of methane. Furthermore, trace element concentrations were measured in the microbial mats and the methane derived carbonates of the Black Sea to test if nickel could be a geochemical indicator for the anaerobic oxidation of methane or for methanogenesis. Nickel is part of the MCR cofactor F430 and the iron sulfide greigite (Fe3S4), which can be found in the microbial mats of the Black Sea. The results have shown that Ni together with stable carbon isotopic ratios could act as a geochemical tracer for methanogenesis or the anaerobic oxidation of methane in both recent and fossil environments. The second part of my thesis deals with the terrestrial mud volcanoes in Italy. Fluids expelled from this type of fluid venting structures were analyzed organo-geochemically (lipid biomarkers) and geochemically (composition of water and gas). In general, mud volcanoes also release a three phase mixture of gas (mainly methane and higher hydrocarbons), water and sediment particles from a source that is often associated with an active petroleum reservoir. Organo-chemical analyzes of the expelled fluids revealed that the biological signals are superimposed by higher hydrocarbons originating from associated active petroleum reservoirs and the underlying organic-rich geological formations. However, signals of various eukaryal, bacterial and archaeal organisms in the mud volcanoes were also found. In addition to signals from higher plants, most likely originated from the surrounding flora and soils, specific bacterial dialkyl glycerol diethers (DAGE) were found which are putatively sourced by sulfate-reducing bacteria (SRB). The presence of archaea is evidenced by archaeol and hydroxyarchaeol. The latter is indicative for the anaerobic oxidation of methane. The results have shown that the complexity of microbial communities in the different mud volcanoes is very high and that some of the microorganisms were involved in the anaerobic turnover of methane. Furthermore, analyzes of sediments from the underlying geological formations have shown that most of the biomarker signals found in the fluids derived from the sediments. Therefore, mud volcanoes could act as a window in the deep bio- and geosphere as well as into in situ microbial processes.
Cold seep
Microbial mat
Sulfate-Reducing Bacteria
Mud volcano
Anaerobic respiration
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In situ rates of methanogenesis and methane oxidation were measured in meromictic Big Soda Lake. Methane production was measured by the accumulation of methane in the headspaces of anaerobically sealed water samples; radiotracer was used to follow methane oxidation. Nearly all the methane oxidation occurred in the anoxic zones of the lake. Rates of anaerobic oxidation exceeded production at all depths studied in both the mixolimnion (2–6 vs. 0.1–1 nmol liter −1 d −1 ) and monimolimnion (49–85 vs. 1.6–12 nmol liter −1 d −1 ) of the lake. Thus, a net consumption of methane equivalent to 1.36 mmol m −2 d −1 occurred in the anoxic water column. Anaerobic methane oxidation had a first‐order rate constant of 8.1±0.5 × 10 −4 d −1 , and activity was eliminated by filter sterilization. However, in situ methane oxidation was of insufficient magnitude to cause a noticeable decrease of ambient dissolved methane levels over an incubation period of 97 h.
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This dissertation seeks to understand the seasonal controls of methane cycling in freshwater sediments. Using a combination of field measurements, radiotracer incubations, porewater characterization, lipid biomarker analysis, and stable carbon isotopes, pronounced seasonal variations in microbial carbon turnover were documented in a freshwater sediment and in two peat wetlands. Constraints of the methane budget in shallow (< 40 cm) sediments revealed a seasonal imbalance between methane fluxes and methane production that may be relieved through tidal pumping of methane-laden porewaters derived from adjacent high marsh through the creekbank. Rate measurements of sulfate reduction and the anaerobic oxidation of methane (AOM), two processes not typically considered relevant in low salinity habitats, revealed their importance in freshwater settings. Seasonal variations in AOM may be driven by fluctuations in hydrogen and acetate dynamics generated by variations in other microbial metabolisms (e.g. sulfate reduction and methanogenesis). Lipid biomarker analysis revealed the presence of sulfate-reducing bacteria and archaea associated with methane cycling. However, seasonal variations in microbial metabolisms were not associated with changes in the lipid distribution. Stable carbon isotope analyses revealed the imprint of AOM on the signatures of methane and dissolved inorganic carbon. The influence of methanotrophy, however, was not as pronounced in the microbial lipid signatures. A potential AOM isotopic signal may have been diluted by methanogenesis and other autotrophic and heterotrophic processes, which may mask a clear methanotrophic signature. While sulfate reduction activity is sufficient to support all observed AOM activity, no conclusive evidence was found to link these processes. Long-term enrichments of coastal sediments with various electron acceptors demonstrated a positive influence of sulfate and ferric citrate additions on AOM. Other electron acceptors such as nitrate and manganese may also support AOM in these coastal settings. These studies advance the understanding of the seasonal controls on methane emissions, methane production, and methane consumption via AOM in freshwater ecosystems. Future efforts are aimed at closer examinations of these mediating factors, especially temperature changes and substrate availability.
Autotroph
Isotopic signature
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Genomic markers for anaerobic microbial processes in marine sediments—sulfate reduction, methanogenesis, and anaerobic methane oxidation—reveal the structure of sulfate-reducing, methanogenic, and methane-oxidizing microbial communities (including uncultured members); they allow inferences about the evolution of these ancient microbial pathways; and they open genomic windows into extreme microbial habitats, such as deep subsurface sediments and hydrothermal vents, that are analogs for the early Earth and for extraterrestrial microbiota.
Microbial Metabolism
Microbial mat
Acetogenesis
Extreme environment
Geomicrobiology
Sulfate-Reducing Bacteria
Cold seep
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