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Ammonia-oxidising archaea (AOA) are ubiquitous and abundant in nature and play a major role in nitrogen cycling. AOA have been studied intensively based on the amoA gene (encoding ammonia monooxygenase subunit A), making it the most sequenced functional marker gene. Here, based on extensive phylogenetic and meta-data analyses of 33,378 curated archaeal amoA sequences, we define a highly resolved taxonomy and uncover global environmental patterns that challenge many earlier generalisations. Particularly, we show: (i) the global frequency of AOA is extremely uneven, with few clades dominating AOA diversity in most ecosystems; (ii) characterised AOA do not represent most predominant clades in nature, including soils and oceans; (iii) the functional role of the most prevalent environmental AOA clade remains unclear; and (iv) AOA harbour molecular signatures that possibly reflect phenotypic traits. Our work synthesises information from a decade of research and provides the first integrative framework to study AOA in a global context. Ammonia-oxidising archaea (AOA) were only discovered a little over a decade ago and remain poorly characterized despite their ubiquity and importance for nitrogen cycling. Here, the authors define a taxonomy of AOA based on a resolved amoA phylogeny and describe emergent global patterns in AOA diversity.

Trophic interactions are crucial for carbon cycling in food webs. Traditionally, eukaryotic micropredators are considered the major micropredators of bacteria in soils, although bacteria like myxobacteria and Bdellovibrio are also known bacterivores. Until recently, it was impossible to assess the abundance of prokaryotes and eukaryotes in soil food webs simultaneously. Using metatranscriptomic three-domain community profiling we identified pro- and eukaryotic micropredators in 11 European mineral and organic soils from different climes. Myxobacteria comprised 1.5–9.7% of all obtained SSU rRNA transcripts and more than 60% of all identified potential bacterivores in most soils. The name-giving and well-characterized predatory bacteria affiliated with the Myxococcaceae were barely present, while Haliangiaceae and Polyangiaceae dominated. In predation assays, representatives of the latter showed prey spectra as broad as the Myxococcaceae . 18S rRNA transcripts from eukaryotic micropredators, like amoeba and nematodes, were generally less abundant than myxobacterial 16S rRNA transcripts, especially in mineral soils. Although SSU rRNA does not directly reflect organismic abundance, our findings indicate that myxobacteria could be keystone taxa in the soil microbial food web, with potential impact on prokaryotic community composition. Further, they suggest an overlooked, yet ecologically relevant food web module, independent of eukaryotic micropredators and subject to separate environmental and evolutionary pressures.

Arctic permafrost soils store large amounts of soil organic carbon (SOC) that could be released into the atmosphere as methane (CH ₄) in a future warmer climate. How warming affects the complex microbial network decomposing SOC is not understood. We studied CH ₄ production of Arctic peat soil microbiota in anoxic microcosms over a temperature gradient from 1 to 30 °C, combining metatranscriptomic, metagenomic, and targeted metabolic profiling. The CH ₄ production rate at 4 °C was 25% of that at 25 °C and increased rapidly with temperature, driven by fast adaptations of microbial community structure, metabolic network of SOC decomposition, and trophic interactions. Below 7 °C, syntrophic propionate oxidation was the rate-limiting step for CH ₄ production; above this threshold temperature, polysaccharide hydrolysis became rate limiting. This change was associated with a shift within the functional guild for syntrophic propionate oxidation, with Firmicutes being replaced by Bacteroidetes. Correspondingly, there was a shift from the formate- and H ₂-using Methanobacteriales to Methanomicrobiales and from the acetotrophic Methanosarcinaceae to Methanosaetaceae . Methanogenesis from methylamines, probably stemming from degradation of bacterial cells, became more important with increasing temperature and corresponded with an increased relative abundance of predatory protists of the phylum Cercozoa. We concluded that Arctic peat microbiota responds rapidly to increased temperatures by modulating metabolic and trophic interactions so that CH ₄ is always highly produced: The microbial community adapts through taxonomic shifts, and cascade effects of substrate availability cause replacement of functional guilds and functional changes within taxa. Significance Microorganisms are key players in emissions of the greenhouse gas (GHG) methane from anoxic carbon-rich peat soils of the Arctic permafrost region. Although available data and modeling suggest a significant temperature-induced increase of GHG emissions from these regions by the end of this century, the controls of and interactions within the underlying microbial networks are largely unknown. This temperature-gradient study of an Arctic peat soil using integrated omics techniques reveals critical temperatures at which microbial adaptations cause changes in metabolic bottlenecks of anaerobic carbon-degradation pathways. In particular taxonomic shifts within functional guilds at different levels of the carbon degradation cascade enable a fast adaptation of the microbial system resulting in high methane emissions at all temperatures.

The high numbers and diversity of protists in soil systems have long been presumed, but their true diversity and community composition have remained largely concealed. Traditional cultivation-based methods miss a majority of taxa, whereas molecular barcoding approaches employing PCR introduce significant biases in reported community composition of soil protists. Here, we applied a metatranscriptomic approach to assess the protist community in 12 mineral and organic soil samples from different vegetation types and climatic zones using small subunit ribosomal RNA transcripts as marker. We detected a broad diversity of soil protists spanning across all known eukaryotic supergroups and revealed a strikingly different community composition than shown before. Protist communities differed strongly between sites, with Rhizaria and Amoebozoa dominating in forest and grassland soils, while Alveolata were most abundant in peat soils. The Amoebozoa were comprised of Tubulinea, followed with decreasing abundance by Discosea, Variosea and Mycetozoa. Transcripts of Oomycetes, Apicomplexa and Ichthyosporea suggest soil as reservoir of parasitic protist taxa. Further, Foraminifera and Choanoflagellida were ubiquitously detected, showing that these typically marine and freshwater protists are autochthonous members of the soil microbiota. To the best of our knowledge, this metatranscriptomic study provides the most comprehensive picture of active protist communities in soils to date, which is essential to target the ecological roles of protists in the complex soil system.

A substantial part of the Earths’ soil organic carbon (SOC) is stored in Arctic permafrost peatlands, which represent large potential sources for increased emissions of the greenhouse gases CH4 and CO2 in a warming climate. The microbial communities and their genetic repertoire involved in the breakdown and mineralisation of SOC in these soils are, however, poorly understood. In this study, we applied a combined metagenomic and metatranscriptomic approach on two Arctic peat soils to investigate the identity and the gene pool of the microbiota driving the SOC degradation in the seasonally thawed active layers. A large and diverse set of genes encoding plant polymer-degrading enzymes was found, comparable to microbiotas from temperate and subtropical soils. This indicates that the metabolic potential for SOC degradation in Arctic peat is not different from that of other climatic zones. The majority of these genes were assigned to three bacterial phyla, Actinobacteria, Verrucomicrobia and Bacteroidetes. Anaerobic metabolic pathways and the fraction of methanogenic archaea increased with peat depth, evident for a gradual transition from aerobic to anaerobic lifestyles. A population of CH4-oxidising bacteria closely related to Methylobacter tundripaludum was the dominating active group of methanotrophs. Based on the in-depth characterisation of the microbes and their genes, we conclude that these Arctic peat soils will turn into CO2 sources owing to increased active layer depth and prolonged growing season. However, the extent of future CH4 emissions will critically depend on the response of the methanotrophic bacteria.

Genes of archaea encoding homologues of ammonia monooxygenases have been found on a widespread basis and in large amounts in almost all terrestrial and marine environments, indicating that ammonia oxidizing archaea (AOA) might play a major role in nitrification on Earth. However, only one pure isolate of this group from a marine environment has so far been obtained, demonstrating archaeal ammonia oxidation coupled with autotrophic growth similar to the bacterial counterparts. Here we describe the cultivation and isolation of an AOA from soil. It grows on ammonia or urea as an energy source and is capable of using higher ammonia concentrations than the marine isolate, Nitrosopumilus maritimus. Surprisingly, although it is able to grow chemolithoautotrophically, considerable growth rates of this strain are obtained only upon addition of low amounts of pyruvate or when grown in coculture with bacteria. Our findings expand the recognized metabolic spectrum of AOA and help explain controversial results obtained in the past on the activity and carbon assimilation of these globally distributed organisms.

Biochar production and subsequent soil incorporation could provide carbon farming solutions to global climate change and escalating food demand. There is evidence that biochar amendment causes fundamental changes in soil nutrient cycles, often resulting in marked increases in crop production, particularly in acidic and in infertile soils with low soil organic matter contents, although comparable outcomes in temperate soils are variable. We offer insight into the mechanisms underlying these findings by focusing attention on the soil nitrogen (N) cycle, specifically on hitherto unmeasured processes of organic N cycling in arable soils. We here investigated the impacts of biochar addition on soil organic and inorganic N pools and on gross transformation rates of both pools in a biochar field trial on arable land (Chernozem) in Traismauer, Lower Austria. We found that biochar increased total soil organic carbon but decreased the extractable organic C pool and soil nitrate. While gross rates of organic N transformation processes were reduced by 50-80%, gross N mineralization of organic N was not affected. In contrast, biochar promoted soil ammonia-oxidizer populations (bacterial and archaeal nitrifiers) and accelerated gross nitrification rates more than two-fold. Our findings indicate a de-coupling of the soil organic and inorganic N cycles, with a build-up of organic N, and deceleration of inorganic N release from this pool. The results therefore suggest that addition of inorganic fertilizer-N in combination with biochar could compensate for the reduction in organic N mineralization, with plants and microbes drawing on fertilizer-N for growth, in turn fuelling the belowground build-up of organic N. We conclude that combined addition of biochar with fertilizer-N may increase soil organic N in turn enhancing soil carbon sequestration and thereby could play a fundamental role in future soil management strategies.

Background The planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover in an environment characterised by high primary productivity. Individual clades belonging to the Gammaproteobacteria have shown similar population dynamics to Bacteroidetes species , and are thus assumed to fill competing ecological niches. Previous studies have generated large numbers of metagenome assembled genomes and metaproteomes from these environments, which can be readily mined to identify populations performing potentially important ecosystem functions. In this study we attempt to catalogue these spring bloom-associated Gammaproteobacteria , which have thus far attracted less attention than sympatric Alphaproteobacteria and Bacteroidetes . Methods We annotated 120 non-redundant species-representative gammaproteobacterial metagenome assembled genomes from spring bloom sampling campaigns covering the four years 2010–2012 and 2016 using a combination of Prokka and PfamScan, with further confirmation via BLAST against NCBI-NR. We also matched these gene annotations to 20 previously published metaproteomes covering those sampling periods plus the spring of 2009. Results Metagenome assembled genomes with clear capacity for polysaccharide degradation via dedicated clusters of carbohydrate active enzymes were among the most abundant during blooms. Many genomes lacked gene clusters with clearly identifiable predicted polysaccharide substrates, although abundantly expressed loci for the uptake of large molecules were identified in metaproteomes. While the larger biopolymers, which are the most abundant sources of reduced carbon following algal blooms, are likely the main energy source, some gammaproteobacterial clades were clearly specialised for smaller organic compounds. Their substrates range from amino acids, monosaccharides, and DMSP, to the less expected, such as terpenoids, and aromatics and biphenyls, as well as many ‘unknowns’. In particular we uncover a much greater breadth of apparent methylotrophic capability than heretofore identified, present in several order level clades without cultivated representatives. Conclusions Large numbers of metagenome assembled genomes are today publicly available, containing a wealth of readily accessible information. Here we identified a variety of predicted metabolisms of interest, which include diverse potential heterotrophic niches of spring bloom-associated Gammaproteobacteria . Features such as those identified here could well be fertile ground for future experimental studies.

Rumen methanogens are major sources of anthropogenic methane emissions, and these archaea are targets in strategies aimed at reducing methane emissions. Here we show that the poorly characterised Thermoplasmata archaea in bovine rumen are methylotrophic methanogens and that they are reduced upon dietary supplementation with rapeseed oil in lactating cows. In a metatranscriptomic survey, Thermoplasmata 16S rRNA and methyl-coenzyme M reductase ( mcr ) transcripts decreased concomitantly with mRNAs of enzymes involved in methanogenesis from methylamines that were among the most abundant archaeal transcripts, indicating that these Thermoplasmata degrade methylamines. Their methylotrophic methanogenic lifestyle was corroborated by in vitro incubations, showing enhanced growth of these organisms upon methylamine supplementation paralleled by elevated methane production. The Thermoplasmata have a high potential as target in future strategies to mitigate methane emissions from ruminant livestock. Our findings and the findings of others also indicate a wider distribution of methanogens than previously anticipated. Rumen methanogenic archaea are major sources of methane emissions and potential targets for methane mitigation strategies. Poulsen et al. now show that dietary rapeseed oil (RSO) supplementation can reduce the abundance of methanogenic Thermoplasmata archaea inhabiting the bovine rumen.

Sequencing of taxonomic or phylogenetic markers is becoming a fast and efficient method for studying environmental microbial communities. This has resulted in a steadily growing collection of marker sequences, most notably of the small-subunit (SSU) ribosomal RNA gene, and an increased understanding of microbial phylogeny, diversity and community composition patterns. However, to utilize these large datasets together with new sequencing technologies, a reliable and flexible system for taxonomic classification is critical. We developed CREST (Classification Resources for Environmental Sequence Tags), a set of resources and tools for generating and utilizing custom taxonomies and reference datasets for classification of environmental sequences. CREST uses an alignment-based classification method with the lowest common ancestor algorithm. It also uses explicit rank similarity criteria to reduce false positives and identify novel taxa. We implemented this method in a web server, a command line tool and the graphical user interfaced program MEGAN. Further, we provide the SSU rRNA reference database and taxonomy SilvaMod, derived from the publicly available SILVA SSURef, for classification of sequences from bacteria, archaea and eukaryotes. Using cross-validation and environmental datasets, we compared the performance of CREST and SilvaMod to the RDP Classifier. We also utilized Greengenes as a reference database, both with CREST and the RDP Classifier. These analyses indicate that CREST performs better than alignment-free methods with higher recall rate (sensitivity) as well as precision, and with the ability to accurately identify most sequences from novel taxa. Classification using SilvaMod performed better than with Greengenes, particularly when applied to environmental sequences. CREST is freely available under a GNU General Public License (v3) from http://apps.cbu.uib.no/crest and http://lcaclassifier.googlecode.com.