Genome-resolved meta-omics unveils rock-hosted lifestyle of enigmatic DPANN archaea

Recent successes in the cultivation of DPANN archaea with their hosts have demonstrated an episymbiotic lifestyle, whereas the lifestyle of DPANN archaea in natural habitats remains controversial. A free-living lifestyle is speculated in oxygen-deprived fluids circulated through rock fractures, where apparent hosts of DPANN archaea are lacking. Alternatively, DPANN archaea may be isolated from their hosts attached to rock surfaces. To understand the ecology of rock-hosted DPANN archaea, rocks rather than fluids should be directly characterized. Here, we show the dominance of Pacearchaeota, one of the widespread and enigmatic lineages of DPANN archaea, in a deep-sea hydrothermal vent chimney. Metagenomic analysis of the rock sample revealed a symbiotic lifestyle of the chimney Pacearchaeota, based on the lack of biosynthetic genes for nucleotides, amino acids, cofactors, and lipids. Genome-resolved metaproteomic analysis clarified the co-occurrence of bacteria actively fixing carbon and nitrogen and thermophilic archaea in the rock habitat. Pacearchaeota has ecological advantages in colonizing the chimney rock interior, because the availability of nutrients and space is limited by silica deposition from hydrothermal fluids. We propose that the diversification of rock-hosted DPANN archaea could be profoundly influenced by coexisting microbes and minerals.