Hua, Zheng-Shuang

AbstractIn the ongoing debates about eukaryogenesis—the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors—members of the Asgard archaea play a key part as the closest archaeal relatives of eukaryotes1. However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved2–4. Here we analyse distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea and as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree and species tree reconciliation approaches, we show that analogous to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared with other archaea. Finally, we infer that the last common ancestor of Asgard archaea was probably a thermophilic chemolithotroph and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and a platform for better understanding the emergence of cellular complexity in eukaryotic cells.

“ 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.

AbstractCandidate bacterial phylum Omnitrophota has not been isolated and is poorly understood. We analysed 72 newly sequenced and 349 existing Omnitrophota genomes representing 6 classes and 276 species, along with Earth Microbiome Project data to evaluate habitat, metabolic traits and lifestyles. We applied fluorescence-activated cell sorting and differential size filtration, and showed that most Omnitrophota are ultra-small (~0.2 μm) cells that are found in water, sediments and soils. Omnitrophota genomes in 6 classes are reduced, but maintain major biosynthetic and energy conservation pathways, including acetogenesis (with or without the Wood-Ljungdahl pathway) and diverse respirations. At least 64% of Omnitrophota genomes encode gene clusters typical of bacterial symbionts, suggesting host-associated lifestyles. We repurposed quantitative stable-isotope probing data from soils dominated by andesite, basalt or granite weathering and identified 3 families with high isotope uptake consistent with obligate bacterial predators. We propose that most Omnitrophota inhabit various ecosystems as predators or parasites.

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.

AbstractTrace metals have been an important ingredient for life throughout Earth’s history. Here, we describe the genome-guided cultivation of a member of the elusive archaeal lineage Caldarchaeales (syn. Aigarchaeota), Wolframiiraptor gerlachensis, and its growth dependence on tungsten. A metagenome-assembled genome (MAG) of W. gerlachensis encodes putative tungsten membrane transport systems, as well as pathways for anaerobic oxidation of sugars probably mediated by tungsten-dependent ferredoxin oxidoreductases that are expressed during growth. Catalyzed reporter deposition-fluorescence in-situ hybridization (CARD-FISH) and nanoscale secondary ion mass spectrometry (nanoSIMS) show that W. gerlachensis preferentially assimilates xylose. Phylogenetic analyses of 78 high-quality Wolframiiraptoraceae MAGs from terrestrial and marine hydrothermal systems suggest that tungsten-associated enzymes were present in the last common ancestor of extant Wolframiiraptoraceae. Our observations imply a crucial role for tungsten-dependent metabolism in the origin and evolution of this lineage, and hint at a relic metabolic dependence on this trace metal in early anaerobic thermophiles.

Recent advances in sequencing technology promoted the blowout discovery of super tiny microbes in the Diapherotrites , Parvarchaeota , Aenigmarchaeota , Nanoarchaeota , and Nanohaloarchaeota (DPANN) superphylum. However, the unculturable properties of the majority of microbes impeded our investigation of their behavior and symbiotic lifestyle in the corresponding community.

Ca . Bathyarchaeia MAGs from terrestrial hot spring habitats are poorly revealed, though they have been studied extensively in marine ecosystems.

“Candidatus Nitrosocaldaceae” are globally distributed in neutral or slightly alkaline hot springs and geothermally heated soils. Despite their essential role in the nitrogen cycle in high-temperature ecosystems, they remain poorly understood because they have never been isolated in pure culture, and very few genomes are available. In the present study, a metagenomics approach was employed to obtain “Ca. Nitrosocaldaceae” metagenomic-assembled genomes (MAGs) from hot spring samples collected from India and China. Phylogenomic analysis placed these MAGs within “Ca. Nitrosocaldaceae.” Average nucleotide identity and average amino acid identity analysis suggested the new MAGs represent two novel species of “Candidatus Nitrosocaldus” and a novel genus, herein proposed as “Candidatus Nitrosothermus.” Key genes responsible for chemolithotrophic ammonia oxidation and a thaumarchaeal 3HP/4HB cycle were detected in all MAGs. Furthermore, genes coding for urea degradation were only present in “Ca. Nitrosocaldus,” while biosynthesis of the vitamins, biotin, cobalamin, and riboflavin were detected in almost all MAGs. Comparison of “Ca. Nitrosocaldales/Nitrosocaldaceae” with other AOA revealed 526 specific orthogroups. This included genes related to thermal adaptation (cyclic 2,3-diphosphoglycerate, and S-adenosylmethionine decarboxylase), indicating their importance for life at high temperature. In addition, these MAGs acquired genes from members from archaea (Crenarchaeota) and bacteria (Firmicutes), mainly involved in metabolism and stress responses, which might play a role to allow this group to adapt to thermal habitats.

Abstract Background: ‘Ca. Aenigmarchaeota’ represents an evolutionary branch within the DPANN superphylum. However, their ecological roles and potential host-symbiont interactions are poorly understood.Results: Here, we analyze eight metagenomic-assembled genomes from hot spring habitats and reveal their functional potentials. Although they have limited metabolic capacities, they harbor substantial carbohydrate metabolizing abilities. Further investigation suggests that horizontal gene transfer might be the main driver that endows these abilities to ‘Ca. Aenigmarchaeota’, including enzymes involved in glycolysis. Additionally, members from the TACK superphylum and Euryarchaeota contribute substantially to the niche expansion of ‘Ca. Aenigmarchaeota’, especially genes related to carbohydrate metabolism and stress responses. Based on co-occurrence network analysis, we conjecture that ‘Ca. Aenigmarchaeota’ may be symbionts associated with TACK archaea and Euryarchaeota, though host-specificity might be wide and variable across different ‘Ca. Aenigmarchaeota’ genomes. Conclusion: This study provides significant insights into possible host-symbiont interactions and ecological roles of ‘Ca. Aenigmarchaeota’.