The origin and cellular complexity of eukaryotes represent a major enigma in biology. Current data support scenarios in which an archaeal host cell and an alphaproteobacterial (mitochondrial) endosymbiont merged together, resulting in the first eukaryotic cell. The host cell is related to Lokiarchaeota, an archaeal phylum with many eukaryotic features. The emergence of the structural complexity that characterizes eukaryotic cells remains unclear. Here we describe the 'Asgard' superphylum, a group of uncultivated archaea that, as well as Lokiarchaeota, includes Thor-, Odin- and Heimdallarchaeota. Asgard archaea affiliate with eukaryotes in phylogenomic analyses, and their genomes are enriched for proteins formerly considered specific to eukaryotes. Notably, thorarchaeal genomes encode several homologues of eukaryotic membrane-trafficking machinery components, including Sec23/24 and TRAPP domains. Furthermore, we identify thorarchaeal proteins with similar features to eukaryotic coat proteins involved in vesicle biogenesis. Our results expand the known repertoire of 'eukaryote-specific' proteins in Archaea, indicating that the archaeal host cell already contained many key components that govern eukaryotic cellular complexity.

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Large reservoirs of natural gas in the oceanic subsurface sustain complex communities of anaerobic microbes, including archaeal lineages with potential to mediate oxidation of hydrocarbons such as methane and butane. Here we describe a previously unknown archaeal phylum, Helarchaeota, belonging to the Asgard superphylum and with the potential for hydrocarbon oxidation. We reconstruct Helarchaeota genomes from metagenomic data derived from hydrothermal deep-sea sediments in the hydrocarbon-rich Guaymas Basin. The genomes encode methyl-CoM reductase-like enzymes that are similar to those found in butane-oxidizing archaea, as well as several enzymes potentially involved in alkyl-CoA oxidation and the Wood-Ljungdahl pathway. We suggest that members of the Helarchaeota have the potential to activate and subsequently anaerobically oxidize hydrothermally generated short-chain hydrocarbons.

Investigations of the biogeochemical roles of benthic Archaea in marine sediments are hampered by the scarcity of cultured representatives. In order to determine their metabolic capacity, we reconstructed the genomic content of four widespread uncultured benthic Archaea recovered from estuary sediments at 48% to 95% completeness. Four genomic bins were found to belong to different subgroups of the former Miscellaneous Crenarcheota Group (MCG) now called Bathyarchaeota: MCG-6, MCG-1, MCG-7/17 and MCG-15. Metabolic predictions based on gene content of the different genome bins indicate that subgroup 6 has the ability to hydrolyse extracellular plant-derived carbohydrates, and that all four subgroups can degrade detrital proteins. Genes encoding enzymes involved in acetate production as well as in the reductive acetyl-CoA pathway were detected in all four genomes inferring that these Archaea are organo-heterotrophic and autotrophic acetogens. Genes involved in nitrite reduction were detected in all Bathyarchaeota subgroups and indicate a potential for dissimilatory nitrite reduction to ammonium. Comparing the genome content of the different Bathyarchaeota subgroups indicated preferences for distinct types of carbohydrate substrates and implicitly, for different niches within the sedimentary environment.

Marine and estuary sediments contain a variety of uncultured archaea whose metabolic and ecological roles are unknown. De novo assembly and binning of high-throughput metagenomic sequences from the sulfate-methane transition zone in estuary sediments resulted in the reconstruction of three partial to near-complete (2.4-3.9 Mb) genomes belonging to a previously unrecognized archaeal group. Phylogenetic analyses of ribosomal RNA genes and ribosomal proteins revealed that this group is distinct from any previously characterized archaea. For this group, found in the White Oak River estuary, and previously registered in sedimentary samples, we propose the name 'Thorarchaeota'. The Thorarchaeota appear to be capable of acetate production from the degradation of proteins. Interestingly, they also have elemental sulfur and thiosulfate reduction genes suggesting they have an important role in intermediate sulfur cycling. The reconstruction of these genomes from a deeply branched, widespread group expands our understanding of sediment biogeochemistry and the evolutionary history of Archaea.

BackgroundDeep-sea hydrothermal vents are hotspots for productivity and biodiversity. Thermal pyrolysis and circulation produce fluids rich in hydrocarbons and reduced compounds that stimulate microbial activity in surrounding sediments. Several studies have characterized the diversity of Guaymas Basin (Gulf of California) sediment-inhabiting microorganisms; however, many of the identified taxa lack cultures or genomic representations. Here, we resolved the metabolic potential and community-level interactions of these diverse communities by reconstructing and analyzing microbial genomes from metagenomic sequencing data.ResultsWe reconstructed 115 microbial metagenome-assembled genomes comprising 27 distinct archaeal and bacterial phyla. The archaea included members of the DPANN and TACK superphyla, Bathyarchaeota, novel Methanosarcinales (GoM-Arc1), and anaerobic methane-oxidizing lineages (ANME-1). Among the bacterial phyla, members of the Bacteroidetes, Chloroflexi, and Deltaproteobacteria were metabolically versatile and harbored potential pathways for hydrocarbon and lipid degradation and a variety of respiratory processes. Genes encoding enzymes that activate anaerobic hydrocarbons for degradation were detected in Bacteroidetes, Chloroflexi, Latescibacteria, and KSB1 phyla, while the reconstructed genomes for most candidate bacteria phyla (Aminicenantes, Atribacteria, Omnitrophica, and Stahlbacteria) indicated a fermentative metabolism. Newly obtained GoM-Arc1 archaeal genomes encoded novel pathways for short-chain hydrocarbon oxidation by alkyl-coenzyme M formation. We propose metabolic linkages among different functional groups, such as fermentative community members sharing substrate-level interdependencies with sulfur- and nitrogen-cycling microbes.ConclusionsOverall, inferring the physiologies of archaea and bacteria from metagenome-assembled genomes in hydrothermal deep-sea sediments has revealed potential mechanisms of carbon cycling in deep-sea sediments. Our results further suggest a network of biogeochemical interdependencies in organic matter utilization, hydrocarbon degradation, and respiratory sulfur cycling among deep-sea-inhabiting microbial communities.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0322-2) contains supplementary material, which is available to authorized users.

The Deepwater Horizon blowout in the Gulf of Mexico in 2010, one of the largest marine oil spills(1), changed bacterial communities in the water column and sediment as they responded to complex hydrocarbon mixtures(2-4). Shifts in community composition have been correlated to the microbial degradation and use of hydrocarbons(2,5,6), but the full genetic potential and taxon-specific metabolisms of bacterial hydrocarbon degraders remain unresolved. Here, we have reconstructed draft genomes of marine bacteria enriched from sea surface and deep plume waters of the spill that assimilate alkane and polycyclic aromatic hydrocarbons during stable-isotope probing experiments, and we identify genes of hydrocarbon degradation pathways. Alkane degradation genes were ubiquitous in the assembled genomes. Marinobacter was enriched with n-hexadecane, and uncultured Alpha- and Gammaproteobacteria populations were enriched in the polycyclic-aromatic-hydrocarbon-degrading communities and contained a broad gene set for degrading phenanthrene and naphthalene. The repertoire of polycyclic aromatic hydrocarbon use varied among different bacterial taxa and the combined capabilities of the microbial community exceeded those of its individual components, indicating that the degradation of complex hydrocarbon mixtures requires the non-redundant capabilities of a complex oil-degrading community.

Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the continental shelf of the northern Gulf of Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration and strong seasonal stratification. Previous research in this dead zone revealed the presence of multiple cosmopolitan bacterioplankton lineages that have eluded cultivation, and thus their metabolic roles in this ecosystem remain unknown. We used a coupled shotgun metagenomic and metatranscriptomic approach to determine the metabolic potential of Marine Group II Euryarchaeota, SAR406, and SAR202. We recovered multiple high-quality, nearly complete genomes from all three groups as well as candidate phyla usually associated with anoxic environments—Parcubacteria (OD1) and Peregrinibacteria. Two additional groups with putative assignments to ACD39 and PAUC34f supplement the metabolic contributions by uncultivated taxa. Our results indicate active metabolism in all groups, including prevalent aerobic respiration, with concurrent expression of genes for nitrate reduction in SAR406 and SAR202, and dissimilatory nitrite reduction to ammonia and sulfur reduction by SAR406. We also report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f. Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter.