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

View ORCID ProfileMelina Kerou, Rafael I. Ponce-Toledo, Rui Zhao, Sophie S. Abby, Miho Hirai, Hidetaka Nomaki, Yoshihiro Takaki, Takuro Nunoura, Steffen L. Jørgensen, Christa Schleper
doi: https://doi.org/10.1101/2020.06.24.168906
Melina Kerou
1Department of Functional and Evolutionary Ecology, Archaea Biology and Ecogenomics Unit, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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  • ORCID record for Melina Kerou
Rafael I. Ponce-Toledo
1Department of Functional and Evolutionary Ecology, Archaea Biology and Ecogenomics Unit, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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Rui Zhao
2Department of Earth Science, K.G. Jebsen Centre for Deep Sea Research, University of Bergen, Bergen, Norway
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Sophie S. Abby
1Department of Functional and Evolutionary Ecology, Archaea Biology and Ecogenomics Unit, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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Miho Hirai
4Super-cutting-edge Grand and Advanced Research (SUGAR) Program, X-star, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan
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Hidetaka Nomaki
4Super-cutting-edge Grand and Advanced Research (SUGAR) Program, X-star, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan
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Yoshihiro Takaki
4Super-cutting-edge Grand and Advanced Research (SUGAR) Program, X-star, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan
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Takuro Nunoura
3Research Center for Bioscience and Nanoscience (CeBN), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan
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Steffen L. Jørgensen
2Department of Earth Science, K.G. Jebsen Centre for Deep Sea Research, University of Bergen, Bergen, Norway
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Christa Schleper
1Department of Functional and Evolutionary Ecology, Archaea Biology and Ecogenomics Unit, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
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  • For correspondence: christa.schleper@univie.ac.at
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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, that 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 Ca. 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 gene repair systems that may allow to overcome 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.

Competing Interest Statement

The authors have declared no competing interest.

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Posted June 24, 2020.
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Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages
Melina Kerou, Rafael I. Ponce-Toledo, Rui Zhao, Sophie S. Abby, Miho Hirai, Hidetaka Nomaki, Yoshihiro Takaki, Takuro Nunoura, Steffen L. Jørgensen, Christa Schleper
bioRxiv 2020.06.24.168906; doi: https://doi.org/10.1101/2020.06.24.168906
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Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages
Melina Kerou, Rafael I. Ponce-Toledo, Rui Zhao, Sophie S. Abby, Miho Hirai, Hidetaka Nomaki, Yoshihiro Takaki, Takuro Nunoura, Steffen L. Jørgensen, Christa Schleper
bioRxiv 2020.06.24.168906; doi: https://doi.org/10.1101/2020.06.24.168906

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