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ABSTRACT In the last decades, rewetting of drained peatlands is on the rise worldwide, to restore their significant carbon sink function. Despite the increasing understanding of peat microbiomes, little is known about the seasonal dynamics and network interactions of the microbial communities in these ecosystems, especially in rewetted fens (groundwater-fed peatlands). Here, we investigated the seasonal dynamics in both prokaryotic and eukaryotic microbiomes in three common fen types in Northern Germany. The eukaryotic microbiomes, including fungi, protists and microbial metazoa, showed significant changes in their community structures across the seasons in contrast to largely unaffected prokaryotic microbiomes. Furthermore, our results proved that the dynamics in eukaryotic microbiomes in the rewetted sites differed between fen types, specifically in terms of saprotrophs, arbuscular mycorrhiza and grazers of bacteria. The co-occurrence networks also exhibited strong seasonal dynamics that differed between rewetted and drained sites, and the correlations involving protists and prokaryotes were the major contributors to these dynamics. Our study provides the insight that microbial eukaryotes mainly define the seasonal dynamics of microbiomes in rewetted fen peatlands. Accordingly, future research should unravel the importance of eukaryotes for biogeochemical processes, especially the under-characterized protists and metazoa, in these poorly understood ecosystems. Eukaryotes, especially of under-characterized protists and microbial metazoa, are important in understanding the dynamics of soil food webs and ecosystem functionality of fen peatlands.

Of all terrestrial ecosystems, peatlands store carbon most effectively in long-term scales of millennia. However, many peatlands have been drained for peat extraction or agricultural use. This converts peatlands from sinks to sources of carbon, causing approx. 5% of the anthropogenic greenhouse effect and additional negative effects on other ecosystem services. Rewetting peatlands can mitigate climate change and may be combined with management in the form of paludiculture. Rewetted peatlands, however, do not equal their pristine ancestors and their ecological functioning is not understood. This holds true especially for groundwater-fed fens. Their functioning results from manifold interactions and can only be understood following an integrative approach of many relevant fields of science, which we merge in the interdisciplinary project WETSCAPES. Here, we address interactions among water transport and chemistry, primary production, peat formation, matter transformation and transport, microbial community, and greenhouse gas exchange using state of the art methods. We record data on six study sites spread across three common fen types (Alder forest, percolation fen, and coastal fen), each in drained and rewetted states. First results revealed that indicators reflecting more long-term effects like vegetation and soil chemistry showed a stronger differentiation between drained and rewetted states than variables with a more immediate reaction to environmental change, like greenhouse gas (GHG) emissions. Variations in microbial community composition explained differences in soil chemical data as well as vegetation composition and GHG exchange. We show the importance of developing an integrative understanding of managed fen peatlands and their ecosystem functioning.

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 increased emissions of the potent GHG methane. The response to rewetting of soil microbiomes as drivers of these processes is poorly understood, as are the biotic and abiotic factors that control community composition. We analyzed the pro- and eukaryotic microbiomes of three contrasting pairs of minerotrophic fens subject to decade-long drainage and subsequent long-term rewetting. Abiotic soil properties including moisture, dissolved organic matter, methane fluxes, and ecosystem respiration rates were also determined. The composition of the microbiomes was fen-type-specific, but all rewetted sites showed higher abundances of anaerobic taxa compared to drained sites. Based on multi-variate statistics and network analyses, we identified soil moisture as a major driver of community composition. Furthermore, salinity drove the separation between coastal and freshwater fen communities. Methanogens were more than 10-fold more abundant in rewetted than in drained sites, while their abundance was lowest in the coastal fen, likely due to competition with sulfate reducers. The microbiome compositions were reflected in methane fluxes from the sites. Our results shed light on the factors that structure fen microbiomes via environmental filtering.

The recently established phylogeny of amoA provides a finer resolution than previous studies, allowing clustering of AOA beyond the order level and thus revealing novel clades. While the 16S rRNA gene is mostly appreciated in microbiome studies, this novel phylogeny is in limited use. A highly resolved taxonomy for ammonia-oxidizing archaea (AOA) based on the alpha subunit of ammonia monooxygenase ( amoA ) was recently established, which uncovered novel environmental patterns of AOA, challenging previous generalizations. However, many microbiome studies target the 16S rRNA gene as a marker; thus, the usage of this novel taxonomy is currently limited. Here, we exploited the phylogenetic congruence of archaeal amoA and 16S rRNA genes to link 16S rRNA gene classification to the novel amoA taxonomy. We screened publicly available archaeal genomes and contigs for the co-occurring amoA and 16S rRNA genes and constructed a 16S rRNA gene database with the corresponding amoA clade taxonomy. Phylogenetic trees of both marker genes confirmed congruence, enabling the identification of clades. We validated this approach with 16S rRNA gene amplicon data from peatland soils. We succeeded in linking 16S rRNA gene amplicon sequence variants belonging to the class Nitrososphaeria to seven different AOA ( amoA ) clades, including two of the most frequently detected clades ( Nitrososphaerales γ and δ clades) for which no pure culture is currently available. Water status significantly impacted the distribution of the AOA clades as well as the whole AOA community structure, which was correlated with pH, nitrate, and ammonium, consistent with previous clade predictions. Our study emphasizes the need to distinguish among AOA clades with distinct ecophysiologies and environmental preferences, for a better understanding of the ecology of the globally abundant AOA. IMPORTANCE The recently established phylogeny of amoA provides a finer resolution than previous studies, allowing clustering of AOA beyond the order level and thus revealing novel clades. While the 16S rRNA gene is mostly appreciated in microbiome studies, this novel phylogeny is in limited use. Here, we provide an alternative path to identifying AOA with this novel and highly resolved amoA taxonomy by using 16S rRNA gene sequencing data. We constructed a 16S rRNA gene database with the associated amoA clade taxonomy based on their phylogenetic congruence. With this database, we were able to assign 16S rRNA gene amplicons from peatland soils to different AOA clades, with a level of resolution provided previously only by amoA phylogeny. As 16S rRNA gene amplicon sequencing is still widely employed in microbiome studies, our database may have a broad application for interpreting the ecology of globally abundant AOA.

A highly resolved taxonomy for ammonia-oxidizing archaea (AOA) based on the alpha subunit of ammonia monooxygenase (amoA) was recently established, which uncovered novel environmental patterns of AOA, challenging previous generalizations. However, many microbiome studies target the 16S rRNA gene as a marker; thus, the usage of this novel taxonomy is currently limited. Here, we exploited the phylogenetic congruence of archaeal amoA and 16S rRNA genes to link 16S rRNA gene classification to the novel amoA taxonomy. We screened publicly available archaeal genomes and contigs for the co-occurring amoA and 16S rRNA genes and constructed a 16S rRNA gene database with the corresponding amoA clade taxonomy. Phylogenetic trees of both marker genes confirmed congruence, enabling the identification of clades. We validated this approach with 16S rRNA gene amplicon data from peatland soils. We succeeded in linking 16S rRNA gene amplicon sequence variants belonging to the class Nitrososphaeria to seven different AOA (amoA) clades, including two of the most frequently detected clades (Nitrososphaerales γ and δ clades) for which no pure culture is currently available. Water status significantly impacted the distribution of the AOA clades as well as the whole AOA community structure, which was correlated with pH, nitrate, and ammonium, consistent with previous clade predictions. Our study emphasizes the need to distinguish among AOA clades with distinct ecophysiologies and environmental preferences, for a better understanding of the ecology of the globally abundant AOA. IMPORTANCE The recently established phylogeny of amoA provides a finer resolution than previous studies, allowing clustering of AOA beyond the order level and thus revealing novel clades. While the 16S rRNA gene is mostly appreciated in microbiome studies, this novel phylogeny is in limited use. Here, we provide an alternative path to identifying AOA with this novel and highly resolved amoA taxonomy by using 16S rRNA gene sequencing data. We constructed a 16S rRNA gene database with the associated amoA clade taxonomy based on their phylogenetic congruence. With this database, we were able to assign 16S rRNA gene amplicons from peatland soils to different AOA clades, with a level of resolution provided previously only by amoA phylogeny. As 16S rRNA gene amplicon sequencing is still widely employed in microbiome studies, our database may have a broad application for interpreting the ecology of globally abundant AOA.

Abstract The hydrogen-dependent and methylotrophic order Methanomassiliicoccales consists of the families Methanomethylophilaceae and Methanomassiliicoccaceae. While Methanomethylophilaceae are comparatively well studied, there is a lack of knowledge on Methanomassiliicoccaceae. In this 16S rRNA gene amplicon sequencing-based study we investigated the temporal and spatial dynamics of the Methanomassiliicoccales in drained and rewetted sites of three common temperate fen peatlands. A 2.5-year monitoring of the fen microbiome composition at three peat depths revealed a dynamic methanogen and Methanomassiliicoccales composition across space and time. Four Methanomassiliicoccales phylotypes were found and they were differentially distributed between the fen types. The wetland cluster phylotype was omnipresent and dominant in abundance in all sites along all depths. The Methanomassiliicoccus phylotype was highly abundant in topsoil while the AB364942 phylotype was exclusively found in deeper regions of the rewetted percolation fen. The phylotype affiliated with Methanomassiliicoccales strain U3.2.1 was only detected in the rewetted percolation fen. We discuss the distribution of the four phylotypes with implications for their ecophysiology, where oxygen tolerance and substrate spectrum might play major roles. In conclusion, the Methanomassiliicoccales are widespread and account for a significant proportion of methanogens, which might suggest their importance for methane emissions from peatlands. The hydrogen-dependent and methylotrophic order Methanomassiliicoccales is widespread in temperate peatlands, consisting of several phylotypes with a dominant occurrence of the wetland cluster phylotype amplicon sequence variants in the studied peat types.

In the last decades, rewetting of drained peatlands is on the rise worldwide, to restore their significant carbon sink function. Despite the increasing understanding of peat microbiomes, little is known about the seasonal dynamics and network interactions of the microbial communities in these ecosystems, especially in rewetted fens (groundwater-fed peatlands). Here, we investigated the seasonal dynamics in both prokaryotic and eukaryotic microbiomes in three common fen types in Northern Germany. The eukaryotic microbiomes, including fungi, protists and microbial metazoa, showed significant changes in their community structures across the seasons in contrast to largely unaffected prokaryotic microbiomes. Furthermore, our results proved that the dynamics in eukaryotic microbiomes in the rewetted sites differed between fen types, specifically in terms of saprotrophs, arbuscular mycorrhiza and grazers of bacteria. The co-occurrence networks also exhibited strong seasonal dynamics that differed between rewetted and drained sites, and the correlations involving protists and prokaryotes were the major contributors to these dynamics. Our study provides the insight that microbial eukaryotes mainly define the seasonal dynamics of microbiomes in rewetted fen peatlands. Accordingly, future research should unravel the importance of eukaryotes for biogeochemical processes, especially the under-characterized protists and metazoa, in these poorly understood ecosystems.

In the last decades, rewetting of drained peatlands is on the rise worldwide, to restore the significant carbon sink function. Rewetted peatlands differ substantially from their pristine counterparts and can, thus, be considered as novel ecosystems. Despite the increasing understanding of peat microbiomes, little is known about the seasonal dynamics and network interactions of the microbial communities in these novel ecosystems, especially in rewetted groundwater-fed peatlands, i.e. fens. Here, we investigated the seasonal dynamics in both prokaryotic and eukaryotic microbiomes in three common types of fens in Northern Germany, namely percolation fen, alder forest and coastal fen. The eukaryotic microbiomes, including fungi, protists and metazoa, showed significant changes of their community structures across the seasons in contrast to largely unaffected prokaryotic microbiomes. The co-occurrence network in the summer showed a distinct topology compared to networks in the other seasons, which was driven by the increased connections among protists, as well as between protists and the other microbial groups. Our results also indicated that the dynamics in eukaryotic microbiomes differed between fen types, specifically in terms of saprotrophs, arbuscular mycorrhiza and grazers of bacteria. Our study provides the insight that microbial eukaryotes mainly define the seasonal dynamics of microbiomes in rewetted fen peatlands. Accordingly, future research should unravel the importance of eukaryotes for biogeochemical processes, especially the under-characterized protists and metazoa, in these novel yet poorly understood ecosystems. Competing Interest Statement The authors have declared no competing interest. Footnotes * Author list changed

Drained peatlands are significant sources of the greenhouse gas (GHG) carbon dioxide. Rewetting is a proven strategy to protect carbon stocks; however, it can lead to increased emissions of the potent GHG methane. The response to rewetting of soil microbiomes as drivers of these processes is poorly understood, as are biotic and abiotic factors that control community composition. We analyzed the pro- and eukaryotic microbiomes of three contrasting pairs of minerotrophic fens subject to decade-long drainage and subsequent rewetting. Also, abiotic soil properties including moisture, dissolved organic matter, methane fluxes and ecosystem respiration rates. The composition of the microbiomes was fen-type-specific, but all rewetted sites showed higher abundance of anaerobic taxa compared to drained sites. Based on multi-variate statistics and network analyses we identified soil moisture as major driver of community composition. Furthermore, salinity drove the separation between coastal and freshwater fen communities. Methanogens were more than tenfold more abundant in rewetted than in drained sites, while their abundance was lowest in the coastal fen, likely due to competition with sulfate reducers. The microbiome compositions were reflected in methane fluxes from the sites. Our results shed light on the factors that structure fen microbiomes via environmental filtering. Footnotes * Manuscript has been revised, especially greenhouse gas flux measurements have been included, figures and supplementary figures have been updated