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Methane (CH4) is a potent greenhouse gas with rising atmospheric concentrations.
Microorganisms are essential players in the global methane cycle. In fact, the largest part of methane emissions derives from microbial production by methanogenic Archaea (methanogens). Microorganisms do not only produce methane: methanotrophs can also oxidize the methane produced by methanogens. In addition, soil methanotrophs are the only biological methane sink, oxidizing up to 30-40 Tg of this potent greenhouse gas per year worldwide.
However, intensified management of grasslands and forests may reduce the methane sink capacity of soils.
In general, the interaction of methanogens and methanotrophs determines whether a soil is a source or a sink for methane. It is, therefore, crucial to understand the microbial part of the methane cycle and which factors influence the abundance and activity of methane-cycling microbes. However, capturing the soil microbiome's abundances, activity, and identity is
challenging. There are numerous target molecules and myriad methods, each with certain
limitations. Linking microbial markers to methane fluxes is therefore challenging. This thesis aimed to understand how methane-cycling microbes in the soil are related to soil methane fluxes and how soil characteristics and human activity influence them.
The first publication investigated the biotic and abiotic drivers of the atmospheric methane sink of soils. It assessed the influence of grassland land-use intensity (150 sites) and forest management type (149 sites) on potential atmospheric methane oxidation rates (PMORs) and the abundance and diversity of CH4-oxidizing bacteria (MOB) with qPCR in topsoils of three temperate regions in Germany. PMORs measured in microcosms under defined conditions were approximately twice as high in forest than in grassland soils. High land-use intensity of grasslands negatively affected PMORs (−40%) in almost all regions. Among the different aspects of land-use intensity, fertilization had the most adverse effect reducing PMORs by 20%.
In contrast, forest management did not affect PMORs in forest soils. Upland soil cluster (USC)α was the dominant group of MOBs in the forests. In contrast, USCγ was absent in more than half of the forest soils but present in almost all grassland soils. USCα abundance had a direct positive effect on PMOR in forests, while in grasslands, USCα and USCγ abundance affected PMOR positively with a more pronounced contribution of USCγ than USCα.
In the second publication, we used quantitative metatranscriptomics to link methane-cycling microbiomes to net surface methane fluxes throughout a year in two grassland soils. Methane fluxes were highly dynamic: both soils were net methane sources in autumn and winter and net methane sinks in spring and summer. Correspondingly, methanogen mRNA abundances per
gram soil correlated well with methane fluxes. Methanotroph to methanogen mRNA ratios were higher in spring and summer when the soils acted as net methane sinks. Furthermore, methane uptake was associated with an increased proportion of USCα and γ pmoA and pmoA2 transcripts. High methanotroph to methanogen ratios would indicate methane sink properties.
Our study links the seasonal transcriptional dynamics of methane-cycling soil microbiomes for the first time to gas fluxes in situ. It suggests mRNA transcript abundances as promising indicators of dynamic ecosystem-level processes.
We conclude that reduction in grassland land-use intensity and afforestation can potentially increase the methane sink function of soils and that different parameters determine the microbial methane sink in forest and grassland soils. Furthermore, this thesis suggests mRNA transcript abundances as promising indicators of dynamic ecosystem-level processes. Methanogen transcript abundance may be used as a proxy for changes in net surface methane emissions from grassland soils.
Abstract
Aerated topsoils are important sinks for atmospheric methane (CH4) via oxidation by CH4‐oxidizing bacteria (MOB). However, intensified management of grasslands and forests may reduce the CH4 sink capacity of soils. We investigated the influence of grassland land‐use intensity (150 sites) and forest management type (149 sites) on potential atmospheric CH4 oxidation rates (PMORs) and the abundance and diversity of MOB (with qPCR) in topsoils of three temperate regions in Germany. PMORs measurements in microcosms under defined conditions yielded approximately twice as much CH4 oxidation in forest than in grassland soils. High land‐use intensity of grasslands had a negative effect on PMORs (−40%) in almost all regions and fertilization was the predominant factor of grassland land‐use intensity leading to PMOR reduction by 20%. In contrast, forest management did not affect PMORs in forest soils. Upland soil cluster (USC)‐α was the dominant group of MOBs in the forests. In contrast, USC‐γ was absent in more than half of the forest soils but present in almost all grassland soils. USC‐α abundance had a direct positive effect on PMOR in forest, while in grasslands USC‐α and USC‐γ abundance affected PMOR positively with a more pronounced contribution of USC‐γ than USC‐α. Soil bulk density negatively influenced PMOR in both forests and grasslands. We further found that the response of the PMORs to pH, soil texture, soil water holding capacity and organic carbon and nitrogen content differ between temperate forest and grassland soils. pH had no direct effects on PMOR, but indirect ones via the MOB abundances, showing a negative effect on USC‐α, and a positive on USC‐γ abundance. We conclude that reduction in grassland land‐use intensity and afforestation has the potential to increase the CH4 sink function of soils and that different parameters determine the microbial methane sink in forest and grassland soils.
Over thousands of years, peatlands around the world have accumulated carbon (C) stocks of global importance. Drainage for agriculture, forestry and peat extraction has transformed many peatlands from long-term sinks into strong sources of carbon dioxide (CO2). Peat extraction is worldwide responsible for about ten percent of drained peatlands and is mainly carried out in northern countries and Eastern Europe. In Belarus, 0.3 Mha of peatlands are drained for peat extraction, which is twelve percent of the country's peatland area. From 2006 to 2013, 21,333 ha of this area have been rewetted to protect these peatlands from fire and further degradation, reduce their greenhouse gas (GHG) emissions, turn them back into C sinks and promote biodiversity. A further 260,000 ha are no longer used for peat extraction and their rewetting would be a great benefit for nature conservation and climate protection.
Rewetting of abandoned peat extraction areas usually leads to inundation of large areas where not adapted plants die and new species establish, depending on water level and nutrient conditions. Beavers, of which there are many in Belarus, also play an important role in the rewetting of peatlands. They dam up ditches in drained and rewetted peatlands, thus contributing to water level increases and vegetation changes. The aim of this PhD thesis was to investigate the impact of inundation on vegetation and GHG emissions in formerly extracted fens in Belarus, to determine the role of water level in this process, and to study whether such fens develop back into C sinks with an almost neutral GHG balance within one or two decades after rewetting (Papers II and III). Also the potential of beaver activities for peatland restoration was assessed (Paper III).
Two very different fens, rewetted after peat extraction, were chosen as study areas. The first one, Giel'cykaŭ Kašyl, is a former flood mire and was rewetted with water from the Jasiel'da River in 1985. During the study period 2010–2012 this site was a shallow lake (~ 1 m deep) dominated by very productive, tall reed. Shallower areas along the edges had a partly floating vegetation cover of cattail (Typha latifolia, T. angustifolia) and sedges (Carex elata, C. vesicaria). The second fen, Barcianicha, is fed by groundwater. Rewetting from 1995 onwards resulted in water levels at or slightly above surface and a lower nutrient availability compared to Giel'cykaŭ Kašyl'. This was reflected in the establishment of mesotrophic communities of Eriophorum angustifolium and Carex rostrata. Phragmites australis stands, which were also dominant here, were shorter and less productive than in Giel'cykaŭ Kašyl'. The southern area of Barcianicha was not used for peat extraction and has not been rewetted. Until 2009 vegetation of this part was characterized by forbs (Urtica dioica) and wet meadows (Agrostis stolonifera). From autumn 2009, a beaver dam in the main drainage ditch caused flooding of these areas and led to diverging vegetation development depending on water levels.
Within the framework of this doctoral thesis annual fluxes of CO2, methane (CH4) and nitrous oxide (N2O) and the development of water levels and vegetation were monitored for two years at nine sites and evaluated (Papers II and III). Three of the sites, respectively, were located (a) in Giel’cykaŭ Kašyl’, flooded in 1985, (b) in the central area of Barcianicha, which was rewetted in 1995, and (c) in the southern part of Barcianicha, which was flooded by beavers end of 2009. GHG measurements were carried out with manual chambers from August 2010 to September 2012. Annual net CO2 exchange rates (NEE) were modeled based on light response curves of gross primary production (GPP) and on temperature response curves of ecosystem respiration (Reco), which were determined every third to fourth week by alternating measurements with transparent (cooled) and opaque chambers (both with fan) along the daily amplitude of photosynthetically active radiation (PAR) and temperature. Annual CH4 emissions were calculated mainly based on the temperature response of CH4 fluxes over the course of the year, based on biweekly (in summer) to monthly (in winter) repeated single measurements with opaque chambers (without fan). This was done, although all longer rewetted sites were dominated by aerenchymatic plants whose gas transport during the vegetation period may change over the course of the day and can be influenced by shading. This might apply to the six longer rewetted sites, two of which were dominated by Phragmites australis, and the others by Typha latifolia, Carex elata, Carex rostrata or Eriophorum angustifolium. For these six sites therefore studies on the daily course of CH4 release and the influence of chamber shade were conducted, covering 8–24 hours and lasting at least from sunrise to afternoon. Also the extent to which flux rates were affected by a lack of chamber headspace mixing by fans was investigated in the mentioned studies (Papers I and II).
The daytime course of CH4 emissions showed a pronounced dynamic for Phragmites australis in both fens, with minimum release during the night and maximum during the day (Paper I). The other sites in contrast did not show a significant diurnal CH4 flux dynamic (Paper II). Lack of headspace mixing by fans as compared to chambers with fan resulted in a slight underestimation of CH4 emissions at very high chambers (220 and 250 cm), as used for Phragmites australis in Giel'cykaŭ Kašyl', while there was no difference at lower chambers (≤185 cm), as used for the other sites. Opaque chambers resulted for sites dominated by Typha latifolia and Carex elata in significantly (1.2 times and 1.1 times, respectively) lower CH4 fluxes compared to transparent chambers. For the other sites, opaque chambers did not significantly reduce CH4 emissions. This result was unexpected, especially for Phragmites australis, as PAR out of all parameters tested had the strongest influence on CH4 emissions from both reed sites, and clouds directly led to reduction of their emissions. Presumably the gas flow in the reed shoots located within opaque chambers was maintained by shoots outside the chamber that were connected to the enclosed shoots by rhizomes (Paper I). The investigations showed that single measurements between 9 a.m. and 6 p.m. with opaque chambers without fan, as performed for the determination of annual CH4 fluxes, resulted for Carex rostrata and Eriophorum angustifolium in estimates similar to the daily mean, but for Phragmites australis in estimates that were rather above the daily mean. Annual CH4 fluxes from Phragmites australis could therefore be slightly overestimated. CH4 fluxes from Typha latifolia and Carex elata during the vegetation period were corrected by a factor of 1.2, although darkness inside of opaque chambers matters only at day, not at night. Daily and annual CH4 fluxes from these sites have been therefore most likely slightly overestimated, too.
Water saturation and the establishment of adapted vegetation were the most important conditions for the restoration of C sinks (gaseous CO2 and CH4 fluxes) in the investigated peatlands. The only site with falling water levels in summer and thus temporarily aerated peat was the beaver flooded forbs (Urtica dioica) site at Barcianicha. This site was a very strong CO2 emitter and the only significant N2O source of the entire study (Paper III). All other sites were permanently wet, had much lower CO2 emissions or were even net C sinks (Papers II and III). Establishment of adapted vegetation depended on inundation depth and time since rewetting. For example, within one year the meadow site in Barcianicha shallowly flooded by beaver was colonized by Carex rostrata and other adapted helophytes and developed into a CO2 sink, while the deeper flooded site at the same meadow initially attracted only Chara and some individuals of Alisma plantago aquatica and remained a moderate CO2 source. However, the results of the longer rewetted sites show, that also deeply (~ 1 m) flooded fen areas can become densely populated with mire plants in the course of 25 years and develop into net C sinks. Highest annual C uptake in both fens was achieved by the reed sites. Eriophorum angustifolium and Carex rostrata in mesotrophic Barcianicha were smaller C sinks. Typha latifolia and Carex elata in the eutrophic Giel'cykaŭ Kašyl', on the other hand, released CO2, presumably because the high and fluctuating water levels imposed stress to the plants, and because the large supply of nutrients and dead plant material allowed for strong heterotrophic respiration (Paper II). The simultaneously high CH4 emissions made Typha latifolia and Carex elata major sources of GHG. CH4 emissions from Phragmites australis in Giel'cykaŭ Kašyl' were even higher, but due to extremely high CO2 uptake the site was only a small net GHG source. CH4 emissions in Barcianicha were much lower and comparable to undisturbed sedge fens. The difference between Giel'cykaŭ Kašyl' and Barcianicha was mainly due to the different nutrient supply and the related productivity of the plants. Important conclusions are that stable inundation is an appropriate measure for restoration of the C sink of formerly extracted fens, but nutrient input with water needs to be stopped or reduced in order to decrease CH4 production. If this is not possible, establishment of Phragmites australis and other strong C sinks could help to compensate for the climate impact of high CH4 emissions from eutrophic sites.
The effect of the beaver dam on the development of the southern part of Barcianicha depended not only on the initial situation but mainly on the water level. Under optimal conditions, it led to the rapid establishment of adapted mire plants, the restoration of a C sink and a significant reduction of GHG emissions. However, this situation in the shallowly flooded meadow was achieved by chance. In comparison to planned rewetting measures, which aim to raise the water level evenly over the entire peatland, beavers dam ditches in order to improve their immediate habitat, thus influencing water levels only up to a certain distance, but rarely over the entire peatland. Nevertheless, beaver activity is of high value both for mire conservation projects, where existing dams are supplemented by beaver dams, and for abandoned, drained peatlands, like former peat extraction areas in Belarus, many of which at least partially have been rewetted by beavers.
Drained peatlands are significant sources of the greenhouse gas (GHG) carbon dioxide.Rewetting is a proven strategy used to protect carbon stocks; however, it can lead to increasedemissions of the potent GHG methane. The response to rewetting of soil microbiomes as drivers ofthese processes is poorly understood, as are the biotic and abiotic factors that control communitycomposition. We analyzed the pro- and eukaryotic microbiomes of three contrasting pairs ofminerotrophic fens subject to decade-long drainage and subsequent long-term rewetting. Abiotic soilproperties including moisture, dissolved organic matter, methane fluxes, and ecosystem respirationrates were also determined. The composition of the microbiomes was fen-type-specific, but allrewetted sites showed higher abundances of anaerobic taxa compared to drained sites. Based onmulti-variate statistics and network analyses, we identified soil moisture as a major driver ofcommunity composition. Furthermore, salinity drove the separation between coastal and freshwaterfen communities. Methanogens were more than 10-fold more abundant in rewetted than in drainedsites, while their abundance was lowest in the coastal fen, likely due to competition with sulfatereducers. The microbiome compositions were reflected in methane fluxes from the sites. Our resultsshed light on the factors that structure fen microbiomes via environmental filtering.