Publications

3780

A novel sulphur-reducing bacterium was isolated from a pyrite-forming enrichment culture inoculated with sewage sludge from a wastewater treatment plant. Based on phylogenetic data, strain J.5.4.2-T.3.5.2T could be affiliated with the phylum Synergistota . Among type strains of species with validly published names, the highest 16S rRNA gene sequence identity value was found with Aminiphilus circumscriptus ILE-2T (89.2 %). Cells of the new isolate were Gram-negative, non-spore-forming, straight to slightly curved rods with tapered ends. Motility was conferred by lateral flagella. True branching of cells was frequently observed. The strain had a strictly anaerobic, asaccharolytic, fermentative metabolism with peptides and amino acids as preferred substrates. Sulphur was required as an external electron acceptor during fermentative growth and was reduced to sulphide, whereas it was dispensable during syntrophic growth with a Methanospirillum species. Major fermentation products were acetate and propionate. The cellular fatty acid composition was dominated by unsaturated and branched fatty acids, especially iso-C15 : 0. Its major polar lipids were phosphatidylglycerol, phosphatidylethanolamine and distinct unidentified polar lipids. Respiratory lipoquinones were not detected. Based on the obtained data we propose the novel species and genus Aminithiophilus ramosus, represented by the type strain J.5.4.2-T.3.5.2T (=DSM 107166T=NBRC 114655T) and the novel family Aminithiophilaceae fam. nov. to accommodate the genus Aminithiophilus. In addition, we suggest reclassifying certain members of the Synergistaceae into new families to comply with current standards for the classification of higher taxa. Based on phylogenomic data, the novel families Acetomicrobiaceae fam. nov., Aminiphilaceae fam. nov., Aminobacteriaceae fam. nov., Dethiosulfovibrionaceae fam. nov. and Thermovirgaceae fam. nov. are proposed.

AbstractThe roles of Asgard archaea in eukaryogenesis and marine biogeochemical cycles are well studied, yet their contributions in soil ecosystems are unknown. Of particular interest are Asgard archaeal contributions to methane cycling in wetland soils. To investigate this, we reconstructed two complete genomes for soil-associated Atabeyarchaeia, a new Asgard lineage, and the first complete genome of Freyarchaeia, and defined their metabolismin situ. Metatranscriptomics highlights high expression of [NiFe]-hydrogenases, pyruvate oxidation and carbon fixation via the Wood-Ljungdahl pathway genes. Also highly expressed are genes encoding enzymes for amino acid metabolism, anaerobic aldehyde oxidation, hydrogen peroxide detoxification and glycerol and carbohydrate breakdown to acetate and formate. Overall, soil-associated Asgard archaea are predicted to be non-methanogenic acetogens, likely impacting reservoirs of substrates for methane production in terrestrial ecosystems.One-Sentence SummaryComplete genomes of Asgard archaea, coupled with metatranscriptomic data, indicate roles in production and consumption of carbon compounds that are known to serve as substrates for methane production in wetlands.

Abstract Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

“ Candidatus Parvarchaeales” microbes may represent a lineage uniquely distributed in extreme environments such as AMD and hot springs. However, little is known about the strategies and processes of how they adapted to these extreme environments.

AbstractAn enormous diversity of previously unknown bacteria and archaea has been discovered recently, yet their functional capacities and distributions in the terrestrial subsurface remain uncertain. Here, we continually sampled a CO2-driven geyser (Colorado Plateau, Utah, USA) over its 5-day eruption cycle to test the hypothesis that stratified, sandstone-hosted aquifers sampled over three phases of the eruption cycle have microbial communities that differ both in membership and function. Genome-resolved metagenomics, single-cell genomics and geochemical analyses confirmed this hypothesis and linked microorganisms to groundwater compositions from different depths. Autotrophic Candidatus “Altiarchaeum sp.” and phylogenetically deep-branching nanoarchaea dominate the deepest groundwater. A nanoarchaeon with limited metabolic capacity is inferred to be a potential symbiont of the Ca. “Altiarchaeum”. Candidate Phyla Radiation bacteria are also present in the deepest groundwater and they are relatively abundant in water from intermediate depths. During the recovery phase of the geyser, microaerophilic Fe- and S-oxidizers have high in situ genome replication rates. Autotrophic Sulfurimonas sustained by aerobic sulfide oxidation and with the capacity for N2 fixation dominate the shallow aquifer. Overall, 104 different phylum-level lineages are present in water from these subsurface environments, with uncultivated archaea and bacteria partitioned to the deeper subsurface.

AbstractCandidatusParvarchaeales, representing a DPANN archaeal group with limited metabolic potentials and reliance on hosts for their growth, were initially found in acid mine drainage (AMD). Due to the lack of representatives, however, their ecological roles and adaptation to extreme habitats such as AMD, as well as how they diverge across the lineage remain largely unexplored. By applying genome-resolved metagenomics, 28Parvarchaeales-associated metagenome-assembled genomes (MAGs) representing two orders and five genera were recovered. Among them, we identified three new genera and proposed the namesCandidatusJingweiarchaeum,CandidatusHaiyanarchaeum, andCandidatusRehaiarchaeum with the former two belonging to a new orderCandidatusJingweiarchaeales. Further analyses of metabolic potentials revealed substantial niche differentiation between Jingweiarchaeales and Parvarchaeales. Jingweiarchaeales may rely on fermentation, salvage pathways, partial glycolysis, and pentose phosphate pathway (PPP) for energy reservation, while the metabolic potentials of Parvarchaeales might be more versatile. Comparative genomic analyses suggested that Jingweiarchaeales are more favorable to habitats with higher temperatures andParvarchaealesare better adapted to acidic environments. We further revealed that the thermal adaptation of these lineages especially for Haiyanarchaeum might rely on innate genomic features such as the usage of specific amino acids, genome streamlining, and hyperthermal featured genes such asrgy. Notably, the acidic adaptation of Parvarchaeales was possibly driven by horizontal gene transfer (HGT). Reconstruction of ancestral states demonstrated that both may originate from thermal and neutral environments and later spread to mesothermal and acidic environments. These evolutionary processes may also be accompanied by adaptation toward oxygen-rich environments via HGT.ImportanceCandidatusParvarchaeales may represent a lineage uniquely distributed in extreme environments such as AMD and hot springs. However, little is known about the strategies and processes of how they adapted to these extreme environments. By the discovery of potential new order-level lineages - Jingweiarchaeales and in-depth comparative genomic analysis, we unveiled the functional differentiation of these lineages. Further, we show that the adaptation to high-temperature and acidic environments of these lineages was driven by different strategies, with the prior relying more on innate genomic characteristics and the latter more on the acquisition of genes associated with acid tolerance. Finally, by reconstruction of ancestral states of OGT andpI, we showed the potential evolutionary process of Parvarchaeales-related lineages with regard to the shift from a high-temperature environment of their common ancestors to low-temperature (potentially acidic) environments.

AbstractMarine sediments comprise one of the largest environments on the planet, and their microbial inhabitants are significant players in global carbon and nutrient cycles. Recent studies using metagenomic techniques have shown the complexity of these communities and identified novel microorganisms from the ocean floor. Here, we obtained 77 metagenome-assembled genomes (MAGs) from the bacterial phylum Armatimonadota in the Guaymas Basin, Gulf of California, and the Bohai Sea, China. These MAGs comprise two previously undescribed classes within Armatimonadota, which we propose naming Hebobacteria and Zipacnadia. They are globally distributed in hypoxic and anoxic environments and are dominant members of deep-sea sediments (up to 1.95% of metagenomic raw reads). The classes described here also have unique metabolic capabilities, possessing pathways to reduce carbon dioxide to acetate via the Wood-Ljungdahl pathway (WLP) and generating energy through the oxidative branch of glycolysis using carbon dioxide as an electron sink, maintaining the redox balance using the WLP. Hebobacteria may also be autotrophic, not previously identified in Armatimonadota. Furthermore, these Armatimonadota may play a role in sulfur and nitrogen cycling, using the intermediate compounds hydroxylamine and sulfite. Description of these MAGs enhances our understanding of diversity and metabolic potential within anoxic habitats worldwide.

AbstractOur knowledge of archaeal diversity and evolution has expanded rapidly in the past decade. However, hardly any genomes of the phylum Korarchaeota have been obtained due to the difficulty in accessing their natural habitats and – possibly – their limited abundance. As a result, many aspects of Korarchaeota biology, physiology and evolution remain enigmatic. Here, we expand this phylum with five high-quality metagenome-assembled genomes. This improved taxon sampling combined with sophisticated phylogenomic analyses robustly places Korarchaeota at the base of TACK and Asgard clades, revisiting the phylum’s long-assumed position. Furthermore, we observe a clear split between terrestrial and marine thermal clades. Gene tree-aware ancestral reconstructions suggest that the last Korarchaeota common ancestor was a thermophilic autotroph. In contrast, Korarchaeaceae, the lineage where environmental transitions occurred, shifted towards a heterotrophic lifestyle. Terrestrial Korarchaeota gained manycasand CARF genes indicating they may need to manage viral infections. Together, our study provides new insights into these early diverging Archaea and suggests that gradual gene gain and loss shaped their adaptation to different thermal environments.ImportanceKorarchaeota are an ancient group of archaea, but their biology, physiology and evolution have remained obscure. Analysis of five novel Korarchaeota MAGs, and publicly available reference data provides robust phylogenomic evidence that Korarchaeota are placed at the base of Asgard archaea and TACK, revisiting the phylum’s long-assumed position. Gene content reconstruction suggests a versatile thermophilic and autotrophic last Korarchaeota common ancestor. Environmental distribution surveying of public databases places all Korarchaeota in thermophilic environments and indicates that their habitat is limited to hydrothermal vents and hot springs. Our modeling indicates at least two transitions linked to habitat switching between these environments in the evolutionary history of Korarchaeota. Both are linked to a significant alteration of the inferred ancestral gene content, including a shift towards a heterotrophic and potential scavenging lifestyle. Furthermore, hot spring Korarchaeota acquired various genes participating in resistance to viruses, suggesting they may need to manage frequent viral threats.