The methane cycle in tropical Lake Matano: Methanogenesis, methane accumulation, and anaerobic methane oxidation (original) (raw)
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The methane cycle in ferruginous Lake Matano
2011
Abstract In Lake Matano, Indonesia, the world's largest known ferruginous basin, more than 50% of authigenic organic matter is degraded through methanogenesis, despite high abundances of Fe (hydr) oxides in the lake sediments. Biogenic CH 4 accumulates to high concentrations (up to 1.4 mmol L− 1) in the anoxic bottom waters, which contain a total of 7.4× 10 5 tons of CH 4.
The methane cycle in tropical Lake Matano: An analogue for Precambrian methane cycling?
2008
In Lake Matano, Indonesia, the world's largest known ferruginous basin, more than 50% of authigenic organic matter is degraded through methanogenesis, despite high abundances of Fe (hydr)oxides in the lake sediments. Biogenic CH 4 accumulates to high concentrations (up to 1.4 mmol L )1 ) in the anoxic bottom waters, which contain a total of 7.4 · 10 5 tons of CH 4 . Profiles of dissolved inorganic carbon (RCO 2 ) and carbon isotopes (d 13 C) show that CH 4 is oxidized in the vicinity of the persistent pycnocline and that some of this CH 4 is likely oxidized anaerobically. The dearth of NO 3 ) and SO 4 2) in Lake Matano waters suggests that anaerobic methane oxidation may be coupled to the reduction of Fe (and ⁄ or Mn) (hydr)oxides. Thermodynamic considerations reveal that CH 4 oxidation coupled to Fe(III) or Mn(III ⁄ IV) reduction would yield sufficient free energy to support microbial growth at the substrate levels present in Lake Matano. Flux calculations imply that Fe and Mn must be recycled several times directly within the water column to balance the upward flux of CH 4 . 16S gene cloning identified methanogens in the anoxic water column, and these methanogens belong to groups capable of both acetoclastic and hydrogenotrophic methanogenesis. We find that methane is important in C cycling, even in this very Fe-rich environment. Such Fe-rich environments are rare on Earth today, but they are analogous to conditions in the ferruginous oceans thought to prevail during much of the Archean Eon. By analogy, methanogens and methanotrophs could have formed an important part of the Archean Ocean ecosystem.
Aerobic methane production by planktonic microbes in lakes
Science of The Total Environment, 2019
Methanogenesis in freshwater lakes has classically been considered to arise from anaerobic methanogens in oxygen-depleted sediments. However, the accumulation of supersaturated methane in fully oxygenated water columns is commonly observed in many lakes, and factors responsible for the formation of the subsurface methane maximum (SMM) remain largely unknown. The present study conducted in 14 Japanese freshwater lakes showed that the SMM formation during the summer stratification period is a common feature in large and deep oligotrophic lakes. The seasonal survey of a deep oligotrophic lake revealed that SMM formation may be uncoupled with the dissolution of atmospheric methane, as well as with the transport of methane from tributary rivers, littoral sediments, and hypolimnetic anoxic sources, suggesting the contribution of in situ methane production. In fact, batch-culture experiments confirmed that bacterioplankton present in lake subsurface waters produce methane aerobically through the decomposition of methylphosphonic acid. Moreover, the development of SMM was closely associated with the seasonal dynamics of planktonic cyanobacteria such as Synechococcus, which may carry the enzyme to catabolize organophosphonate compounds. Therefore, we suggest that the predominance of Synechococcus during the thermal stratification
Microbial methane production in oxygenated water column of an oligotrophic lake
Proceedings of the National Academy of Sciences , 2011
The prevailing paradigm in aquatic science is that microbial methanogenesis happens primarily in anoxic environments. Here, we used multiple complementary approaches to show that microbial methane production could and did occur in the well-oxygenated water column of an oligotrophic lake (Lake Stechlin, Germany). Oversaturation of methane was repeatedly recorded in the well-oxygenated upper 10 m of the water column, and the methane maxima coincided with oxygen oversaturation at 6 m. Laboratory incubations of unamended epilimnetic lake water and inoculations of photoautotrophs with a lake-enrichment culture both led to methane production even in the presence of oxygen, and the production was not affected by the addition of inorganic phosphate or methylated compounds. Methane production was also detected by in-lake incubations of lake water, and the highest production rate was 1.8-2.4 nM·h −1 at 6 m, which could explain 33-44% of the observed ambient methane accumulation in the same month. Temporal and spatial uncoupling between methanogenesis and methanotrophy was supported by field and laboratory measurements, which also helped explain the oversaturation of methane in the upper water column. Potentially methanogenic Archaea were detected in situ in the oxygenated, methane-rich epilimnion, and their attachment to photoautotrophs might allow for anaerobic growth and direct transfer of substrates for methane production. Specific PCR on mRNA of the methyl coenzyme M reductase A gene revealed active methanogenesis. Microbial methane production in oxygenated water represents a hitherto overlooked source of methane and can be important for carbon cycling in the aquatic environments and water to air methane flux. epilimnic methane peak | methanogens A lthough methane makes up <2 parts per million by volume (ppmv) of the atmosphere, it accounts for 20% of the total radiative forcing among all long-lived greenhouse gases (1). In the aquatic environments, methane is also an important substrate for microbial production (2). The prevailing paradigm is that microbial methanogenesis occurs primarily in anoxic environments (3, 4). A commonly observed paradox is methane accumulation in well-oxygenated waters (2, 5), which is often assumed to be the result of physical transport from anoxic sediment and water (6-8) or in situ production within microanoxic zones (9-11). Two recent studies challenged this paradigm and suggested that microbes in oligotrophic ocean can metabolize methylated compounds and release methane even aerobically (12, 13). These claims are not without caveats, because the amounts of methylated compounds added [1-10 μM methylphosphonate (12) and 50 μM dimethyl sulfoniopropionate (13)] were far higher than their environmental concentrations, and therefore, the ecological relevance remains obscure. Moreover, dissolved oxygen (DO) was not monitored during the long incubation (5-6 d), and the possibility that the experimental setups had become anoxic before methane production could not be dismissed.* Despite the uncertainty, if microbial methane production can occur in oxygenated water, it will have profound implications for carbon cycling and climate.
2020
Despite growing evidence that methane (CH 4) formation could also occur in well-oxygenated surface fresh waters, its significance at the ecosystem scale is uncertain. Empirical models based on data gathered at high latitude predict that the contribution of oxic CH 4 increases with lake size and should represent the majority of CH 4 emissions in large lakes. However, such predictive models could not directly apply to tropical lakes, which differ from their temperate counterparts in some fundamental characteristics, such as year-round elevated water temperature. We conducted stableisotope tracer experiments, which revealed that oxic CH 4 production is closely related to phytoplankton metabolism and is a common feature in five contrasting African lakes. Nevertheless, methanotrophic activity in surface waters and CH 4 emissions to the atmosphere were predominantly fuelled by CH 4 generated in sediments and physically transported to the surface. Indeed, CH 4 bubble dissolution flux and diffusive benthic CH 4 flux were several orders of magnitude higher than CH 4 production in surface waters. Microbial CH 4 consumption dramatically decreased with increasing sunlight intensity, suggesting that the freshwater "CH 4 paradox" might be also partly explained by photo-inhibition of CH 4 oxidizers in the illuminated zone. Sunlight appeared as an overlooked but important factor determining the CH 4 dynamics in surface waters, directly affecting its production by photoautotrophs and consumption by methanotrophs.
Frontiers in Microbiology, 2016
Lakes represent a considerable natural source of methane to the atmosphere compared to their small global surface area. Methanotrophs in sediments and in the water column largely control methane fluxes from these systems, yet the diversity, electron accepting capacity, and nutrient requirements of these microorganisms have only been partially identified. Here, we investigated the role of electron acceptors alternative to oxygen and sulfate in microbial methane oxidation at the oxycline and in anoxic waters of the ferruginous meromictic Lake La Cruz, Spain. Active methane turnover in a zone extending well below the oxycline was evidenced by stable carbon isotope-based rate measurements. We observed a strong methane oxidation potential throughout the anoxic water column, which did not vary substantially from that at the oxic/anoxic interface. Both in the redox-transition and anoxic zones, only aerobic methane-oxidizing bacteria (MOB) were detected by fluorescence in situ hybridization and sequencing techniques, suggesting a close coupling of cryptic photosynthetic oxygen production and aerobic methane turnover. Additions of nitrate, nitrite and to a lesser degree iron and manganese oxides also stimulated bacterial methane consumption. We could not confirm a direct link between the reduction of these compounds and methane oxidation and we cannot exclude the contribution of unknown anaerobic methanotrophs. Nevertheless, our findings from Lake La Cruz support recent laboratory evidence that aerobic methanotrophs may be able to utilize alternative terminal electron acceptors under oxygen limitation.
Production and consumption of methane in freshwater lake ecosystems
Research in Microbiology, 2011
The atmospheric concentration of methane (CH 4 ), a major greenhouse gas, is mainly controlled by the activities of methane-producing (methanogens) and methane-consuming (methanotrophs) microorganisms. Freshwater lakes are identified as one of the main CH 4 sources, as it was estimated that they contribute to 6e16% of natural CH 4 emissions. It is therefore critical to better understanding the biogeochemical cycling of CH 4 in these ecosystems. In this paper, the effects of environmental factors on methanogenic and methanotrophic rates are reviewed and an inventory of the methanogens and methanotrophs at the genus/species level in freshwater lakes is given. We focus on the anaerobic oxidation of methane, which is a still poorly known process but increasingly reported in freshwater lakes. (N. Morel-Desrosiers), J-Pierre.Morel@ univ-bpclermont.fr (J.-P. Morel), pipeyret@univ-bpclermont.fr (P. Peyret), gerard.fonty@univ-bpclermont.fr (G. Fonty), a-catherine.lehours@lbp.univbpclermont.fr (A.-C. Lehours). www.elsevier.com/locate/resmic 0923-2508/$ -see front matter Ó
Multiple Groups of Methanotrophic Bacteria Mediate Methane Oxidation in Anoxic Lake Sediments
Frontiers in Microbiology, 2022
Freshwater lakes represent an important source of the potent greenhouse gas methane (CH 4) to the atmosphere. Methane emissions are regulated to large parts by aerobic (MOx) and anaerobic (AOM) oxidation of methane, which are important CH 4 sinks in lakes. In contrast to marine benthic environments, our knowledge about the modes of AOM and the related methanotrophic microorganisms in anoxic lake sediments is still rudimentary. Here, we demonstrate the occurrence of AOM in the anoxic sediments of Lake Sempach (Switzerland), with maximum in situ AOM rates observed within the surface sediment layers in presence of multiple groups of methanotrophic bacteria and various oxidants known to support AOM. However, substrate-amended incubations (with NO 2 − , NO 3 − , SO 4 2− , Fe-, and Mn-oxides) revealed that none of the electron acceptors previously reported to support AOM enhanced methane turnover in Lake Sempach sediments under anoxic conditions. In contrast, the addition of oxygen to the anoxic sediments resulted in an approximately 10-fold increase in methane oxidation relative to the anoxic incubations. Phylogenetic and isotopic evidence indicate that both Type I and Type II aerobic methanotrophs were growing on methane under both oxic and anoxic conditions, although methane assimilation rates were an order of magnitude higher under oxic conditions. While the anaerobic electron acceptor responsible for AOM could not be identified, these findings expand our understanding of the metabolic versatility of canonically aerobic methanotrophs under anoxic conditions, with important implications for future investigations to identify methane oxidation processes. Bacterial AOM by facultative aerobic methane oxidizers might be of much larger environmental significance in reducing methane emissions than previously thought.
2019
Freshwater lakes are a significant site for biological methane production and its subsequent emission into the atmosphere as a potent greenhouse gas. Methane in freshwater lakes is mostly produced in anoxic sediments by archaea from the taxon Euryarchaeota. The archaea metabolize substrates derived from the decomposition of organic matter by anaerobic bacteria. This indicates that both organic matter supply and microbial community composition are drivers behind methanogenesis. However, the interaction betw e n these two factors and the extent of their role remains mostly unexplored. We sampled from Morris Lake, a mesotrophic lake situated at the University of Notre Dame Environmental Research Center, and constructed sediment incubations treated with algal a dditions and antibiotic additions in full factorial. The rates of methane and carbon dioxide were estimated and used to determine the influence of organic matter supply and microbial community composition. We hypothesized that tr...
Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake
Applied and Environmental Microbiology, 2011
Anaerobic oxidation of methane (AOM) with sulfate as terminal electron acceptor has been reported for various environments, including freshwater habitats, and also, nitrate and nitrite were recently shown to act as electron acceptors for methane oxidation in eutrophic freshwater habitats. Radiotracer experiments with sediment material of Lake Constance, an oligotrophic freshwater lake, were performed to follow 14 CO 2 formation from 14 CH 4 in sediment incubations in the presence of different electron acceptors, namely, nitrate, nitrite, sulfate, or oxygen. Whereas 14 CO 2 formation without and with sulfate addition was negligible, addition of nitrate increased 14 CO 2 formation significantly, suggesting that AOM could be coupled to denitrification. Nonetheless, denitrification-dependent AOM rates remained at least 1 order of magnitude lower than rates of aerobic methane oxidation. Using molecular techniques, putative denitrifying methanotrophs belonging to the NC10 phylum were detected on the basis of the pmoA and 16S rRNA gene sequences. These findings show that sulfate-dependent AOM was insignificant in Lake constant sediments. However, AOM can also be coupled to denitrification in this oligotrophic freshwater habitat, providing first indications that this might be a widespread process that plays an important role in mitigating methane emissions.