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Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages.

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.

SUBMITTER: Kerou M

PROVIDER: S-EPMC8397731 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Metagenomics of marine sediments has uncovered a broad diversity of new uncultured taxa and provided insights into their metabolic capabilities. Here, we detected microbial lineages from a sediment core near the Jiulong methane reef of the northern South China Sea (at 1,100-m depth). Assembly and binning of the metagenomes resulted in 11 genomes (>85% complete) that represented nine distinct phyla, including candidate phyla TA06 and LCP-89, Lokiarchaeota, Heimdallarchaeota, and a newly described globally distributed phylum (B38). The genome of LCP-89 has pathways for nitrate, selenate, and sulfate reduction, suggesting that they may be involved in mediating these important processes. B38 are able to participate in the cycling of hydrogen and selenocompounds. Many of these uncultured microbes may also be capable of autotrophic CO2 fixation, as exemplified by identification of the Wood-Ljungdahl (W-L) pathway. Genes encoding carbohydrate degradation, W-L pathway, Rnf-dependent energy conservation, and Ni/Fe hydrogenases were detected in the transcriptomes of these novel members. Characterization of these new lineages provides insight to the undescribed branches in the tree of life.IMPORTANCE Sedimentary microorganisms in the South China Sea (SCS) remain largely unknown due to the complexity of sediment communities impacted by continent rifting and extension. Distinct geochemical environments may breed special microbial communities including microbes that are still enigmatic. Functional inference of their metabolisms and transcriptional activity provides insight in the ecological roles and substrate-based interactivity of these uncultured Archaea and Bacteria These microorganisms play different roles in utilizing inorganic carbon and scavenging diverse organic compounds involved in the deep-sea carbon cycle. The genomes recovered here contributed undescribed species to the tree of life and laid the foundation for future study on these novel phyla persisting in marginal sediments of the SCS.

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Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages.

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