Abstract
Marine sediments represent a vast habitat for complex microbiomes. Among these, ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are one of the most common, yet little explored, inhabitants, which seem extraordinarily well adapted to the harsh conditions of the subsurface biosphere. We present 11 metagenome-assembled genomes of the most abundant AOA clades from sediment cores obtained from the Atlantic Mid-Ocean ridge flanks and Pacific abyssal plains. Their phylogenomic placement reveals three independently evolved clades within the order Nitrosopumilales, of which no cultured representative is known yet. In addition to the gene sets for ammonia oxidation and carbon fixation known from other AOA, all genomes encode an extended capacity for the conversion of fermentation products that can be channeled into the central carbon metabolism, as well as uptake of amino acids probably for protein maintenance or as an ammonia source. Two lineages encode an additional (V-type) ATPase and a large repertoire of DNA repair systems that may allow to overcome the challenges of high hydrostatic pressure. We suggest that the adaptive radiation of AOA into marine sediments occurred more than once in evolution and resulted in three distinct lineages with particular adaptations to this extremely energy-limiting and high-pressure environment.
Highlights
Ammonia oxidizing archaea (AOA) comprise one of the most successful archaeal phyla having colonized almost every imaginable oxic environment of the planet where they emerge as key players in the nitrogen cycle [1,2,3,4,5,6]
Our comparative and phylogenomic analyses using 11 sediment-derived metagenome-assembled genomes (MAGs) reported in this study, together with a large collection of ammonia oxidizing archaea (AOA) genomes with a broad phylogenetic and ecological distribution, allowed us to study the evolution, diversification, and adaptation mechanisms of AOA into deep marine environments
Based on phylogenomic analyses and different from earlier scenarios [29], we conclude that AOA from deep marine sediments evolved independently within three lineages
Summary
Ammonia oxidizing archaea (AOA) comprise one of the most successful archaeal phyla having colonized almost every imaginable oxic environment of the planet where they emerge as key players in the nitrogen cycle [1,2,3,4,5,6] This includes the marine environment where they dominate archaeal communities associated with oxic sediments ranging from shallow estuaries to the open ocean [7,8,9,10,11,12], and from the surface layers all the way into the deep oceanic crust [13,14,15]. The abundance and distribution of amoA-NP-theta and -delta in the energy-starved subsurface suggest that they have adapted and evolved differently than their pelagic counterparts These clades represent a yet unexplored diversity within NP, and so far have no cultivated or genomic representatives [28]
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