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 unce...
The widely reported paradox of methane oversaturation in oxygenated water challenges the prevailing paradigm that microbial methanogenesis only occurs under anoxic conditions. Using a combination of field sampling, incubation experiments, and modeling, we show that the recurring mid-water methane peak in Lake Stechlin, northeast Germany, was not dependent on methane input from the littoral zone or bottom sediment or on the presence of known micro-anoxic zones. The methane peak repeatedly overlapped with oxygen oversaturation in the seasonal thermocline. Incubation experiments and isotope analysis indicated active methane production, which was likely linked to photosynthesis and/or nitrogen fixation within the oxygenated water, whereas lessening of methane oxidation by light allowed accumulation of methane in the oxygen-rich upper layer. Estimated methane efflux from the surface water was up to 5 mmol m 22 d 21 . Mid-water methane oversaturation was also observed in nine other lakes that collectively showed a strongly negative gradient of methane concentration within 0-20% dissolved oxygen (DO) in the bottom water, and a positive gradient within $ 20% DO in the upper water column. Further investigation into the responsible organisms and biochemical pathways will help improve our understanding of the global methane cycle.
BackgroundLake sediments harbor diverse microbial communities that cycle carbon and nutrients while being constantly colonized and potentially buried by organic matter sinking from the water column. The interaction of activity and burial remained largely unexplored in aquatic sediments. We aimed to relate taxonomic composition to sediment biogeochemical parameters, test whether community turnover with depth resulted from taxonomic replacement or from richness effects, and to provide a basic model for the vertical community structure in sediments.MethodsWe analyzed four replicate sediment cores taken from 30-m depth in oligo-mesotrophic Lake Stechlin in northern Germany. Each 30-cm core spanned ca. 170 years of sediment accumulation according to 137Cs dating and was sectioned into layers 1–4 cm thick. We examined a full suite of biogeochemical parameters and used DNA metabarcoding to examine community composition of microbial Archaea, Bacteria, and Eukaryota.ResultsCommunity β-diversity indicated nearly complete turnover within the uppermost 30 cm. We observed a pronounced shift from Eukaryota- and Bacteria-dominated upper layers (<5 cm) to Bacteria-dominated intermediate layers (5–14 cm) and to deep layers (>14 cm) dominated by enigmatic Archaea that typically occur in deep-sea sediments. Taxonomic replacement was the prevalent mechanism in structuring the community composition and was linked to parameters indicative of microbial activity (e.g., CO2 and CH4 concentration, bacterial protein production). Richness loss played a lesser role but was linked to conservative parameters (e.g., C, N, P) indicative of past conditions.ConclusionsBy including all three domains, we were able to directly link the exponential decay of eukaryotes with the active sediment microbial community. The dominance of Archaea in deeper layers confirms earlier findings from marine systems and establishes freshwater sediments as a potential low-energy environment, similar to deep sea sediments. We propose a general model of sediment structure and function based on microbial characteristics and burial processes. An upper “replacement horizon” is dominated by rapid taxonomic turnover with depth, high microbial activity, and biotic interactions. A lower “depauperate horizon” is characterized by low taxonomic richness, more stable “low-energy” conditions, and a dominance of enigmatic Archaea.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0255-9) contains supplementary material, which is available to authorized users.
Rice is one of the most important nourishments and its cultivation binds large agricultural areas in the world. Its cultivation leads to huge water consumption and high methane emissions. To diminish these problems, crop rotation between paddy rice and maize is introduced in Asia, but can lead to losses of carbon and water by the formation of desiccation cracks. To counteract these problems rice straw can be applied. We analyzed soil microbial responses to different crop rotation systems [rice–rice (RR), maize–maize (MM), maize–rice (MR)] and to rice straw application in the soil and rhizosphere of maize. Zea mays was grown in microcosms using soils from different field locations, each including different crop rotation regimes. The bacterial and fungal community composition was analyzed by 16S rRNA gene and ITS based amplicon sequencing in the bulk soil and rhizosphere. The microbiota was clearly different in soils from the different field locations (analysis of similarity, ANOSIM: R = 0.516 for the bacterial community; R = 0.817 for the fungal community). Within the field locations, crop rotation contributed differently to the variation in microbial community composition. Strong differences were observed in communities inhabiting soils under monosuccession (RR vs. MM) (ANOSIM: R = 0.923 for the bacterial and R = 0.714 for the fungal community), while the communities in soils undergoing MR crop rotation were more similar to those of the corresponding RR soils (ANOSIM: R = 0.111–0.175). The observed differences could be explained by altered oxygen availabilities in RR and MR soils, resulting in an enrichment of anaerobic bacteria in the soils, and the presence of the different crops, leading to the enrichment of host-plant specific microbial communities. The responses of the microbial communities to the application of rice straw in the microcosms were rather weak compared to the other factors. The taxa responding in bulk soil and rhizosphere were mostly distinct. In conclusion, this study revealed that the different agricultural management practices affect microbial community composition to different extent, not only in the bulk soil but also in the rhizosphere, and that the microbial responses in bulk soil and rhizosphere are distinct.
Microbial communities in arctic-alpine soils show biogeographic patterns related to elevation, but the effect of fine-scale heterogeneity and possibly related temperature and soil moisture regimes remains unclear. We collected soil samples from different micro-topographic positions and elevational levels in two mountain regions of the Scandes, Central Norway. Microbial community composition was characterized by 16S rRNA gene amplicon sequencing and was dependent on microtopography and elevation. Underlying environmental drivers were identified by integration of microbial community data with a comprehensive set of site-specific long-term recorded temperature and soil moisture data. Partial least square regression analysis allowed the description of ecological response patterns and the identification of the important environmental drivers for each taxonomic group. This demonstrated for the first time that taxa responding to elevation were indeed most strongly defined by temperature, rather than by other environmental factors. Micro-topography affected taxa were primarily controlled by temperature and soil moisture. In general, 5-year datasets had higher explanatory power than 1year datasets, indicating that the microbial community composition is dependent on long-term developments of near-ground temperature and soil moisture regimes and possesses a certain resilience, which is in agreement with an often observed delayed response in global warming studies in arctic-alpine regions.
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