Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea

• Published in: The ISME Journal Vol. 14; no. 10; pp. 2595 - 2609
• Main Authors: Qin, Wei, Zheng, Yue, Zhao, Feng, Wang, Yulin, Urakawa, Hidetoshi, Martens-Habbena, Willm, Liu, Haodong, Huang, Xiaowu, Zhang, Xinxu, Nakagawa, Tatsunori, Mende, Daniel R., Bollmann, Annette, Wang, Baozhan, Zhang, Yao, Amin, Shady A., Nielsen, Jeppe L., Mori, Koji, Takahashi, Reiji, Virginia Armbrust, E., Winkler, Mari-K.H., DeLong, Edward F., Li, Meng, Lee, Po-Heng, Zhou, Jizhong, Zhang, Chuanlun, Zhang, Tong, Stahl, David A., Ingalls, Anitra E.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.10.2020; Nature Publishing Group
• Subjects: 45; 45/23; 45/47; 631/326/171/1878; 631/326/2565/855; 96; Adaptive radiation; Ammonia; Aquatic habitats; Archaea; Archaea - genetics; BASIC BIOLOGICAL SCIENCES; Biogeography; Biomedical and Life Sciences; Comparative analysis; Ecology; Energy conservation; Evolutionary Biology; Genomes; Geographical locations; Hydrostatic pressure; Life Sciences; Metagenomics; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microorganisms; Nitrification; Nitrogen oxides; Nutrients; Oxidation; Oxidation-Reduction; Phosphorus; Photochemicals; Phylogeny; Physiology
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-020-0710-7

Ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms in the ocean, exerting primary control on nitrification and nitrogen oxides emission. Although united by a common physiology of chemoautotrophic growth on ammonia, a corresponding high genomic and habitat variability suggests tremendous adaptive capacity. Here, we compared 44 diverse AOA genomes, 37 from species cultivated from samples collected across diverse geographic locations and seven assembled from metagenomic sequences from the mesopelagic to hadopelagic zones of the deep ocean. Comparative analysis identified seven major marine AOA genotypic groups having gene content correlated with their distinctive biogeographies. Phosphorus and ammonia availabilities as well as hydrostatic pressure were identified as selective forces driving marine AOA genotypic and gene content variability in different oceanic regions. Notably, AOA methylphosphonate biosynthetic genes span diverse oceanic provinces, reinforcing their importance for methane production in the ocean. Together, our combined comparative physiological, genomic, and metagenomic analyses provide a comprehensive view of the biogeography of globally abundant AOA and their adaptive radiation into a vast range of marine and terrestrial habitats.