Metagenomic Insights into the Metabolic and Ecological Functions of Abundant Deep-Sea Hydrothermal Vent DPANN Archaea

Abstract

Due to their unique metabolism and important ecological roles, deep-sea hydrothermal archaea have attracted great scientific interests. Among these archaea, DPANN superphylum archaea are widely distributed in hydrothermal vent environments. However, DPANN metabolism and ecology remain largely unknown. In this study, we assembled 20 DPANN genomes among 43 reconstructed genomes obtained from deep-sea hydrothermal vent sediments. Phylogenetic analysis suggests 6 phyla, comprised of Aenigmarchaeota, Diapherotrites, Nanoarchaeota, Pacearchaeota, Woesearchaeota and a new candidate phylum we have designated Kexuearchaeota. These are included in the 20 DPANN archaeal members, indicating their broad diversity in this special environment. Analyses on their metabolism reveal deficiencies due to their reduced genome size, including gluconeogenesis and de novo nucleotide and amino acid biosynthesis. However, DPANN archaea possess alternate strategies to address these deficiencies. DPANN archaea also have potentials to assimilate nitrogen and sulfur compounds, indicating a potentially important ecological role in the hydrothermal vent system. IMPORTANCE DPANN archaea show high distribution in the hydrothermal system though they display small genome size and some incomplete biological processes. Exploring their metabolism is helpful to understand how such small forms of life adapt to this unique environment and what ecological roles they play. In this study, we obtained 20 high quality metagenome-assembled genomes (MAGs) corresponding to 6 phyla of the DPANN group (Aenigmarchaeota, Diapherotrites, Nanoarchaeota, Pacearchaeota, Woesearchaeota and a new candidate phylum designated Kexuearchaeota). Further metagenomic analyses provided insights on the metabolism and ecological functions of DPANN archaea to adapt to deep-sea hydrothermal environments. Our study contributes to gain a deeper understanding of their special lifestyles and should provide clues to cultivate this important archaeal group in the future.