“
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.
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.
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.
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’.
Abstract
Several recent studies have shown the presence of genes for the key enzyme associated with archaeal methane/alkane metabolism, methyl-coenzyme M reductase (Mcr), in metagenome-assembled genomes (MAGs) divergent to existing archaeal lineages. Here, we study the mcr-containing archaeal MAGs from several hot springs, which reveal further expansion in the diversity of archaeal organisms performing methane/alkane metabolism. Significantly, an MAG basal to organisms from the phylum Thaumarchaeota that contains mcr genes, but not those for ammonia oxidation or aerobic metabolism, is identified. Together, our phylogenetic analyses and ancestral state reconstructions suggest a mostly vertical evolution of mcrABG genes among methanogens and methanotrophs, along with frequent horizontal gene transfer of mcr genes between alkanotrophs. Analysis of all mcr-containing archaeal MAGs/genomes suggests a hydrothermal origin for these microorganisms based on optimal growth temperature predictions. These results also suggest methane/alkane oxidation or methanogenesis at high temperature likely existed in a common archaeal ancestor.