Metagenomic discovery ofCandidatusParvarchaeales related lineages sheds light on the adaptation and diversification from neutral-thermal to acidic-mesothermal environments

Abstract

Candidatus Parvarchaeales, 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, 28 Parvarchaeales-associated metagenome-assembled genomes (MAGs) representing two orders and five genera were recovered. Among them, we identified three new genera and proposed the names Candidatus Jingweiarchaeum, Candidatus Haiyanarchaeum, and Candidatus Rehaiarchaeum with the former two belonging to a new order Candidatus Jingweiarchaeales. 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 and Parvarchaeales are 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 as rgy. 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.