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A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.).

ABSTRACT: Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

SUBMITTER: Rinke C

PROVIDER: S-EPMC6461757 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Project description:Due to their unique metabolism and important ecological roles, deep-sea hydrothermal archaea have attracted great scientific interest. 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 of 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 the potential to assimilate nitrogen and sulfur compounds, indicating an important ecological role in the hydrothermal vent system.IMPORTANCE DPANN archaea show high distribution in the hydrothermal system, although 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 a deeper understanding of their special lifestyles and should provide clues to cultivate this important archaeal group in the future.

Dataset Information

A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.).

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