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Anaerobic methane oxidizing archaea (ANME) mediate anaerobic oxidation of methane (AOM) in marine sediments and are therefore important for controlling atmospheric methane concentrations in the water column and ultimately the atmosphere. Numerous previous studies have revealed that AOM is coupled to the reduction of different electron acceptors such as sulfate, nitrate/nitrite or Fe(III)/Mn(IV). However, the influence of electron acceptor availability on the in situ ANME community composition in sediments remains largely unknown. Here, we investigated the electron acceptor availability and compared the microbial in situ communities of three methane-rich locations offshore the sub-Antarctic island South Georgia, by Illumina sequencing and qPCR of mcrA genes. The methanic zone (MZ) sediments of Royal Trough and Church Trough comprised high sulfide concentrations of up to 4 and 19 mM, respectively. In contrast, those of the Cumberland Bay fjord accounted for relatively high concentrations of dissolved iron (up to 186 μM). Whereas the ANME community in the sulfidic sites Church Trough and Royal Trough mainly comprised members of the ANME-1 clade, the order-level clade “ANME-1-related” (Lever and Teske, 2015) was most abundant in the iron-rich site in Cumberland Bay fjord, indicating that the availability of electron acceptors has a strong selective effect on the ANME community. This study shows that potential electron acceptors for methane oxidation may serve as environmental filters to select for the ANME community composition and adds to a better understanding of the global importance of AOM.

Functional traits are increasingly used in ecology to link the structure of microbial communities to ecosystem processes. We investigated two important protistan lineages, Cercozoa and Endomyxa (Rhizaria) in soil using Illumina sequencing and analysed their diversity and functional traits along with their responses to environmental factors in grassland and forest across Germany. From 600 soil samples, we obtained 2,101 Operational Taxonomy Units representing ~18 million Illumina reads (region V4, 18S rRNA gene). All major taxonomic and functional groups were present, dominated by small bacterivorous flagellates (Glissomonadida). Endomyxan plant parasites were absent from forest. In grassland, they were promoted by more intensive land use management. Grassland and forest strikingly differed in community composition. Relative abundances of bacterivores and eukaryvores were contrastingly influenced by environmental factors, indicating bottom-up regulation by food resources. These patterns provide new insights into the functional organization of soil biota and indications for a more sustainable land-use management.HighlightsProtistan plant parasites of worldwide importance (Phytomyxea) are absent from forestProtistan plant parasites are enhanced by land use intensification in grasslandOpposite responses of protistan trophic guilds to environmental conditions in forestDrastic differences in protistan community composition between grassland and forest

Spatial and temporal processes shaping microbial communities are inseparably linked but rarely studied together. By Illumina 16S rRNA sequencing, we monitored soil bacteria in 360 stations on a 100 square meter plot distributed across six intra-annual samplings in a rarely managed, temperate grassland. Using a multi-tiered approach, we tested the extent to which stochastic or deterministic processes influenced the composition of local communities. A combination of phylogenetic turnover analysis and null modeling demonstrated that either homogenization by unlimited stochastic dispersal or scenarios, in which neither stochastic processes nor deterministic forces dominated, explained local assembly processes. Thus, the majority of all sampled communities (82%) was rather homogeneous with no significant changes in abundance-weighted composition. However, we detected strong and uniform taxonomic shifts within just nine samples in early summer. Thus, community snapshots sampled from single points in time or space do not necessarily reflect a representative community state. The potential for change despite the overall homogeneity was further demonstrated when the focus shifted to the rare biosphere. Rare OTU turnover, rather than nestedness, characterized abundance-independent β-diversity. Accordingly, boosted generalized additive models encompassing spatial, temporal and environmental variables revealed strong and highly diverse effects of space on OTU abundance, even within the same genus. This pure spatial effect increased with decreasing OTU abundance and frequency, whereas soil moisture – the most important environmental variable – had an opposite effect by impacting abundant OTUs more than the rare ones. These results indicate that – despite considerable oscillation in space and time – the abundant and resident OTUs provide a community backbone that supports much higher β-diversity of a dynamic rare biosphere. Our findings reveal complex interactions among space, time, and environmental filters within bacterial communities in a long-established temperate grassland.

Marine fungi are an important component of pelagic planktonic communities. However, it is not yet clear how individual fungal taxa are integrated in marine processes of the microbial loop and food webs. Most likely, biotic interactions play a major role in shaping the fungal community structure. Thus, the aim of our work was to identify possible biotic interactions of mycoplankton with phytoplankton and zooplankton groups and among fungi, and to investigate whether there is coherence between interactions and the dynamics, abundance and temporal occurrence of individual fungal OTUs. Marine surface water was sampled weekly over the course of 1 year, in the vicinity of the island of Helgoland in the German Bight (North Sea). The mycoplankton community was analyzed using 18S rRNA gene tag-sequencing and the identified dynamics were correlated to environmental data including phytoplankton, zooplankton, and abiotic factors. Finally, co-occurrence patterns of fungal taxa were detected with network analyses based on weighted topological overlaps (wTO). Of all abundant and persistent OTUs, 77% showed no biotic relations suggesting a saprotrophic lifestyle. Of all other fungal OTUs, nearly the half (44%) had at least one significant negative relationship, especially with zooplankton and other fungi, or to a lesser extent with phytoplankton. These findings suggest that mycoplankton OTUs are embedded into marine food web chains via highly complex and manifold relationships such as parasitism, predation, grazing, or allelopathy. Furthermore, about one third of all rare OTUs were part of a dense fungal co-occurrence network probably stabilizing the fungal community against environmental changes and acting as functional guilds or being involved in fungal cross-feeding. Placed in an ecological context, strong antagonistic relationships of the mycoplankton community with other components of the plankton suggest that: (i) there is a top-down control by fungi on zooplankton and phytoplankton; (ii) fungi serve as a food source for zooplankton and thereby transfer nutrients and organic material; (iii) the dynamics of fungi harmful to other plankton groups are controlled by antagonistic fungal taxa.

The flux of methane, a potent greenhouse gas, from the seabed is largely controlled by anaerobic oxidation of methane (AOM) coupled to sulfate reduction (S-AOM) in the sulfate methane transition (SMT). S-AOM is estimated to oxidize 90% of the methane produced in marine sediments and is mediated by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria. An additional methane sink, i.e., iron oxide coupled AOM (Fe-AOM), has been suggested to be active in the methanic zone of marine sediments. Geochemical signatures below the SMT such as high dissolved iron, low to undetectable sulfate and high methane concentrations, together with the presence of iron oxides are taken as prerequisites for this process. So far, Fe-AOM has neither been proven in marine sediments nor have the governing key microorganisms been identified. Here, using a multidisciplinary approach, we show that Fe-AOM occurs in iron oxide-rich methanic sediments of the Helgoland Mud Area (North Sea). When sulfate reduction was inhibited, different iron oxides facilitated AOM in long-term sediment slurry incubations but manganese oxide did not. Especially magnetite triggered substantial Fe-AOM activity and caused an enrichment of ANME-2a archaea. Methane oxidation rates of 0.095 ± 0.03 nmol cm–3 d–1 attributable to Fe-AOM were obtained in short-term radiotracer experiments. The decoupling of AOM from sulfate reduction in the methanic zone further corroborated that AOM was iron oxide-driven below the SMT. Thus, our findings prove that Fe-AOM occurs in methanic marine sediments containing mineral-bound ferric iron and is a previously overlooked but likely important component in the global methane budget. This process has the potential to sustain microbial life in the deep biosphere.

Soil protists are increasingly appreciated as essential components of soil foodwebs; however, there is a dearth of information on the factors structuring their communities. Here we investigate the importance of different biotic and abiotic factors as key drivers of spatial and seasonal distribution of protistan communities. We conducted an intensive survey of a 10m2 grassland plot in Germany, focusing on a major group of protists, the Cercozoa. From 177 soil samples, collected from April to November, we obtained 694 Operational Taxonomy Units representing >6 million Illumina reads. All major cercozoan taxonomic and functional groups were present, dominated by the small flagellates of the Glissomonadida. We found evidence of environmental selection structuring the cercozoan communities both spatially and seasonally. Spatial analyses indicated that communities were correlated within a range of 3.5 meters. Seasonal variations in the abundance of bacterivores and bacteria, followed by that of omnivores suggested a dynamic prey-predator succession. The most influential edaphic properties were moisture and clay content, which differentially affected each functional group. Our study is based on an intense sampling of protists at a small scale, thus providing a detailed description of the biodiversity of different taxa/functional groups and the ecological processes involved in shaping their distribution.

Microorganisms can use crystalline iron minerals for iron reduction linked to organic matter degradation or as conduits for direct interspecies electron transfer (mDIET) to syntrophic partners, e.g., methanogens. The environmental conditions that lead either to reduction or conduit use are so far unknown. We investigated microbial community shifts and interactions with crystalline iron minerals (hematite and magnetite) in methanic ferruginous marine sediment incubations during organic matter (glucose) degradation at varying temperatures. Iron reduction rates increased with decreasing temperature from 30°C to 4°C. Both hematite and magnetite facilitated iron reduction at 4°C, demonstrating that microorganisms in the methanic zone of marine sediments can reduce crystalline iron oxides under psychrophilic conditions. Methanogenesis occurred, however, at higher rates with increasing temperature. At 30°C, both hematite and magnetite accelerated methanogenesis onset and maximum process rates. At lower temperatures (10°C and 4°C), hematite could still facilitate methanogenesis but magnetite served more as an electron acceptor for iron reduction than as a conduit. Different temperatures selected for different key microorganisms: at 30°C, members of genus Orenia, Halobacteroidaceae, at 10°C, Photobacterium and the order Clostridiales, and at 4°C Photobacterium and Psychromonas were enriched. Members of the order Desulfuromonadales harboring known dissimilatory iron reducers were also enriched at all temperatures. Our results show that crystalline iron oxides predominant in some natural environments can facilitate electron transfer between microbial communities at psychrophilic temperatures. Furthermore, temperature has a critical role in determining the pathway of crystalline iron oxide utilization in marine sediment shifting from conduction at 30°C to predominantly iron reduction at lower temperatures.

Interrelated successive transformation steps of nitrification are performed by distinct microbial groups – the ammonia-oxidizers, comprising ammonia-oxidizing archaea (AOA) and bacteria (AOB), and nitrite-oxidizers such as Nitrobacter and Nitrospira, which are the dominant genera in the investigated soils. Hence, not only their presence and activity in the investigated habitat is required for nitrification, but also their temporal and spatial interactions. To demonstrate the interdependence of both groups and to address factors promoting putative niche differentiation within each group, temporal and spatial changes in nitrifying organisms were monitored in an unfertilized grassland site over an entire vegetation period at the plot scale of 10 m2. Nitrifying organisms were assessed by measuring the abundance of marker genes (amoA for AOA and AOB, nxrA for Nitrobacter, 16S rRNA gene for Nitrospira) selected for the respective sub-processes. A positive correlation between numerically dominant AOA and Nitrospira, and their co-occurrence at the same spatial scale in August and October, suggests that the nitrification process is predominantly performed by these groups and is restricted to a limited timeframe. Amongst nitrite-oxidizers, niche differentiation was evident in observed seasonally varying patterns of co-occurrence and spatial separation. While their distributions were most likely driven by substrate concentrations, oxygen availability may also have played a role under substrate-limited conditions. Phylogenetic analysis revealed temporal shifts in Nitrospira community composition with an increasing relative abundance of OTU03 assigned to sublineage V from August onward, indicating its important role in nitrite oxidation.