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Asgard archaea are considered to be the closest known relatives of eukaryotes. Their genomes contain hundreds of eukaryotic signature proteins (ESPs), which inspired hypotheses on the evolution of the eukaryotic cell 1 – 3 . A role of ESPs in the formation of an elaborate cytoskeleton and complex cellular structures has been postulated 4 – 6 , but never visualized. Here we describe a highly enriched culture of ‘ Candidatus Lokiarchaeum ossiferum’, a member of the Asgard phylum, which thrives anaerobically at 20 °C on organic carbon sources. It divides every 7–14 days, reaches cell densities of up to 5 × 10 7 cells per ml and has a significantly larger genome compared with the single previously cultivated Asgard strain 7 . ESPs represent 5% of its protein-coding genes, including four actin homologues. We imaged the enrichment culture using cryo-electron tomography, identifying ‘ Ca . L. ossiferum’ cells on the basis of characteristic expansion segments of their ribosomes. Cells exhibited coccoid cell bodies and a network of branched protrusions with frequent constrictions. The cell envelope consists of a single membrane and complex surface structures. A long-range cytoskeleton extends throughout the cell bodies, protrusions and constrictions. The twisted double-stranded architecture of the filaments is consistent with F-actin. Immunostaining indicates that the filaments comprise Lokiactin—one of the most highly conserved ESPs in Asgard archaea. We propose that a complex actin-based cytoskeleton predated the emergence of the first eukaryotes and was a crucial feature in the evolution of the Asgard phylum by scaffolding elaborate cellular structures. Culture and analysis of ‘ Candidatus  Lokiarchaeum ossiferum’—a member of the Asgard phylum—reveals an elaborate cell architecture with extensive membranous protrusions.

Chemolithotrophic ammonia-oxidizing bacteria and Thaumarchaeota are central players in the global nitrogen cycle. Obligate ammonia chemolithotrophy has been characterized for bacteria; however, large gaps remain in the Thaumarchaeotal pathway. Using batch growth experiments and instantaneous microrespirometry measurements of resting biomass, we show that the terrestrial Thaumarchaeon Nitrososphaera viennensis EN76 T exhibits tight control over production and consumption of nitric oxide (NO) during ammonia catabolism, unlike the ammonia-oxidizing bacterium Nitrosospira multiformis ATCC 25196 T . In particular, pulses of hydroxylamine into a microelectrode chamber as the sole substrate for N. viennensis resulted in iterative production and consumption of NO followed by conversion of hydroxylamine to nitrite. In support of these observations, oxidation of ammonia in growing cultures of N. viennensis , but not of N. multiformis , was inhibited by the NO-scavenger PTIO. When based on the marginal nitrous oxide (N 2 O) levels detected in cell-free media controls, the higher levels produced by N. multiformis were explained by enzyme activity, whereas N 2 O in N. viennensis cultures was attributed to abiotic reactions of released N-oxide intermediates with media components. Our results are conceptualized in a pathway for ammonia-dependent chemolithotrophy in Thaumarchaea, which identifies NO as an essential intermediate in the pathway and implements known biochemistry to be executed by a proposed but still elusive copper enzyme. Taken together, this work identifies differences in ammonia-dependent chemolithotrophy between bacteria and the Thaumarchaeota, advances a central catabolic role of NO only in the Thaumarchaeotal pathway and reveals stark differences in how the two microbial cohorts contribute to N 2 O emissions.

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.

Background: Soil ecosystems harbor the most complex prokaryotic and eukaryotic microbial communities on Earth. Experimental approaches studying these systems usually focus on either the soil community’s taxonomic structure or its functional characteristics. Many methods target DNA as marker molecule and use PCR for amplification. Methodology/Principal Findings: Here we apply an RNA-centered meta-transcriptomic approach to simultaneously obtain information on both structure and function of a soil community. Total community RNA is random reversely transcribed into cDNA without any PCR or cloning step. Direct pyrosequencing produces large numbers of cDNA rRNA-tags; these are taxonomically profiled in a binning approach using the MEGAN software and two specifically compiled rRNA reference databases containing small and large subunit rRNA sequences. The pyrosequencing also produces mRNA-tags; these provide a sequence-based transcriptome of the community. One soil dataset of 258,411 RNA-tags of ~98 bp length contained 193,219 rRNA-tags with valid taxonomic information, together with 21,133 mRNA-tags. Quantitative information about the relative abundance of organisms from all three domains of life and from different trophic levels was obtained in a single experiment. Less frequent taxa, such as soil Crenarchaeota, were well represented in the data set. These were identified by more than 2,000 rRNA-tags; furthermore, their activity in situ was revealed through the presence of mRNA-tags specific for enzymes involved in ammonia oxidation and CO² fixation. Conclusions/Significance: This approach could be widely applied in microbial ecology by efficiently linking community structure and function in a single experiment while avoiding biases inherent in other methods.

Soil emissions are largely responsible for the increase of the potent greenhouse gas nitrous oxide (N 2 O) in the atmosphere and are generally attributed to the activity of nitrifying and denitrifying bacteria. However, the contribution of the recently discovered ammonia-oxidizing archaea (AOA) to N 2 O production from soil is unclear as is the mechanism by which they produce it. Here we investigate the potential of Nitrososphaera viennensis , the first pure culture of AOA from soil, to produce N 2 O and compare its activity with that of a marine AOA and an ammonia-oxidizing bacterium (AOB) from soil . N. viennensis produced N 2 O at a maximum yield of 0.09% N 2 O per molecule of nitrite under oxic growth conditions. N 2 O production rates of 4.6±0.6 amol N 2 O cell −1  h −1 and nitrification rates of 2.6±0.5 fmol NO 2 − cell −1  h −1 were in the same range as those of the AOB Nitrosospira multiformis and the marine AOA Nitrosopumilus maritimus grown under comparable conditions. In contrast to AOB, however, N 2 O production of the two archaeal strains did not increase when the oxygen concentration was reduced, suggesting that they are not capable of denitrification. In 15 N-labeling experiments we provide evidence that both ammonium and nitrite contribute equally via hybrid N 2 O formation to the N 2 O produced by N. viennensis under all conditions tested. Our results suggest that archaea may contribute to N 2 O production in terrestrial ecosystems, however, they are not capable of nitrifier-denitrification and thus do not produce increasing amounts of the greenhouse gas when oxygen becomes limiting.

Unlike all other archaeal lineages, ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread and abundant in all moderate and oxic environments on Earth. The evolutionary adaptations that led to such unprecedented ecological success of a microbial clade characterized by highly conserved energy and carbon metabolisms have, however, remained underexplored. Here, we reconstructed the genomic content and growth temperature of the ancestor of all AOA, as well as the ancestors of the marine and soil lineages, based on 39 available complete or nearly complete genomes of AOA. Unlike all other archaeal lineages, ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread and abundant in all moderate and oxic environments on Earth. The evolutionary adaptations that led to such unprecedented ecological success of a microbial clade characterized by highly conserved energy and carbon metabolisms have, however, remained underexplored. Here, we reconstructed the genomic content and growth temperature of the ancestor of all AOA, as well as the ancestors of the marine and soil lineages, based on 39 available complete or nearly complete genomes of AOA. Our evolutionary scenario depicts an extremely thermophilic, autotrophic, aerobic ancestor from which three independent lineages of a marine and two terrestrial groups radiated into moderate environments. Their emergence was paralleled by (i) a continuous acquisition of an extensive collection of stress tolerance genes mostly involved in redox maintenance and oxygen detoxification, (ii) an expansion of regulatory capacities in transcription and central metabolic functions, and (iii) an extended repertoire of cell appendages and modifications related to adherence and interactions with the environment. Our analysis provides insights into the evolutionary transitions and key processes that enabled the conquest of the diverse environments in which contemporary AOA are found.

Marine Crenarchaeota represent an abundant component of oceanic microbiota with potential to significantly influence biogeochemical cycling in marine ecosystems. Prior studies using specific archaeal lipid biomarkers and isotopic analyses indicated that planktonic Crenarchaeota have the capacity for autotrophic growth, and more recent cultivation studies support an ammonia-based chemolithoautotrophic energy metabolism. We report here analysis of fosmid sequences derived from the uncultivated marine crenarchaeote, Cenarchaeum symbiosum, focused on the reconstruction of carbon and energy metabolism. Genes predicted to encode multiple components of a modified 3-hydroxypropionate cycle of autotrophic carbon assimilation were identified, consistent with utilization of carbon dioxide as a carbon source. Additionally, genes predicted to encode a near complete oxidative tricarboxylic acid cycle were also identified, consistent with the consumption of organic carbon and in the production of intermediates for amino acid and cofactor biosynthesis. Therefore, C. symbiosum has the potential to function either as a strict autotroph, or as a mixotroph utilizing both carbon dioxide and organic material as carbon sources. From the standpoint of energy metabolism, genes predicted to encode ammonia monooxygenase subunits, ammonia permease, urease, and urea transporters were identified, consistent with the use of reduced nitrogen compounds as energy sources fueling autotrophic metabolism. Homologues of these genes, recovered from ocean waters worldwide, demonstrate the conservation and ubiquity of crenarchaeal pathways for carbon assimilation and ammonia oxidation. These findings further substantiate the likely global metabolic importance of Crenarchaeota with respect to key steps in the biogeochemical transformation of carbon and nitrogen in marine ecosystems.

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.

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.

The detection of silica-rich dust particles, as an indication for ongoing hydrothermal activity, and the presence of water and organic molecules in the plume of Enceladus, have made Saturn’s icy moon a hot spot in the search for potential extraterrestrial life. Methanogenic archaea are among the organisms that could potentially thrive under the predicted conditions on Enceladus, considering that both molecular hydrogen (H 2 ) and methane (CH 4 ) have been detected in the plume. Here we show that a methanogenic archaeon, Methanothermococcus okinawensis , can produce CH 4 under physicochemical conditions extrapolated for Enceladus. Up to 72% carbon dioxide to CH 4 conversion is reached at 50 bar in the presence of potential inhibitors. Furthermore, kinetic and thermodynamic computations of low-temperature serpentinization indicate that there may be sufficient H 2 gas production to serve as a substrate for CH 4 production on Enceladus. We conclude that some of the CH 4 detected in the plume of Enceladus might, in principle, be produced by methanogens. Many methanogenic archaea use H 2 and CO 2 to produce methane. Here, Taubner et al. show that Methanothermococcus okinawensis produces methane under conditions extrapolated for Saturn’s icy moon, Enceladus, and estimate that serpentinization may produce sufficient H 2 for biological methane production.