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

Wei Qin; Yue Zheng; Feng Zhao; Yulin Wang; Hidetoshi Urakawa; Willm Martens-Habbena; Haodong Liu; Xiaowu Huang; Xinxu Zhang; Tatsunori Nakagawa; Daniel R. Mende; Annette Bollmann; Baozhan Wang; Yao Zhang; Shady A. Amin; Jeppe L. Nielsen; Koji Mori; Reiji Takahashi; E. Virginia Armbrust; Mari K.H. Winkler; Edward F. DeLong; Meng Li; Po Heng Lee; Jizhong Zhou; Chuanlun Zhang; Tong Zhang; David A. Stahl; Anitra E. Ingalls

doi:10.1038/s41396-020-0710-7

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

Wei Qin^*, Yue Zheng, Feng Zhao^*, Yulin Wang, Hidetoshi Urakawa, Willm Martens-Habbena, Haodong Liu, Xiaowu Huang, Xinxu Zhang, Tatsunori Nakagawa, Daniel R. Mende, Annette Bollmann, Baozhan Wang, Yao Zhang, Shady A. Amin, Jeppe L. Nielsen, Koji Mori, Reiji Takahashi, E. Virginia Armbrust, Mari K.H. WinklerEdward F. DeLong, Meng Li, Po Heng Lee, Jizhong Zhou, Chuanlun Zhang, Tong Zhang, David A. Stahl, Anitra E. Ingalls^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

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.

Original language	English
Pages (from-to)	2595-2609
Number of pages	15
Journal	ISME Journal
Volume	14
Issue number	10
DOIs	https://doi.org/10.1038/s41396-020-0710-7
State	Published - 1 Oct 2020
Externally published	Yes

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Qin, W., Zheng, Y., Zhao, F., Wang, Y., Urakawa, H., Martens-Habbena, W., Liu, H., Huang, X., Zhang, X., Nakagawa, T., Mende, D. R., Bollmann, A., Wang, B., Zhang, Y., Amin, S. A., Nielsen, J. L., Mori, K., Takahashi, R., Virginia Armbrust, E., ... Ingalls, A. E. (2020). Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea. ISME Journal, 14(10), 2595-2609. https://doi.org/10.1038/s41396-020-0710-7

@article{1d3153fd51e74cc2ba6e5b3b5f6b893c,

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

abstract = "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.",

author = "Wei Qin and Yue Zheng and Feng Zhao and Yulin Wang and Hidetoshi Urakawa and Willm Martens-Habbena and Haodong Liu and Xiaowu Huang and Xinxu Zhang and Tatsunori Nakagawa and Mende, {Daniel R.} and Annette Bollmann and Baozhan Wang and Yao Zhang and Amin, {Shady A.} and Nielsen, {Jeppe L.} and Koji Mori and Reiji Takahashi and {Virginia Armbrust}, E. and Winkler, {Mari K.H.} and DeLong, {Edward F.} and Meng Li and Lee, {Po Heng} and Jizhong Zhou and Chuanlun Zhang and Tong Zhang and Stahl, {David A.} and Ingalls, {Anitra E.}",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = oct,

day = "1",

doi = "10.1038/s41396-020-0710-7",

language = "英语",

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Qin, W, Zheng, Y, Zhao, F, Wang, Y, Urakawa, H, Martens-Habbena, W, Liu, H, Huang, X, Zhang, X, Nakagawa, T, Mende, DR, Bollmann, A, Wang, B, Zhang, Y, Amin, SA, Nielsen, JL, Mori, K, Takahashi, R, Virginia Armbrust, E, Winkler, MKH, DeLong, EF, Li, M, Lee, PH, Zhou, J, Zhang, C, Zhang, T, Stahl, DA & Ingalls, AE 2020, 'Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea', ISME Journal, vol. 14, no. 10, pp. 2595-2609. https://doi.org/10.1038/s41396-020-0710-7

TY - JOUR

T1 - Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea

AU - Qin, Wei

AU - Zheng, Yue

AU - Zhao, Feng

AU - Wang, Yulin

AU - Urakawa, Hidetoshi

AU - Martens-Habbena, Willm

AU - Liu, Haodong

AU - Huang, Xiaowu

AU - Zhang, Xinxu

AU - Nakagawa, Tatsunori

AU - Mende, Daniel R.

AU - Bollmann, Annette

AU - Wang, Baozhan

AU - Zhang, Yao

AU - Amin, Shady A.

AU - Nielsen, Jeppe L.

AU - Mori, Koji

AU - Takahashi, Reiji

AU - Virginia Armbrust, E.

AU - Winkler, Mari K.H.

AU - DeLong, Edward F.

AU - Li, Meng

AU - Lee, Po Heng

AU - Zhou, Jizhong

AU - Zhang, Chuanlun

AU - Zhang, Tong

AU - Stahl, David A.

AU - Ingalls, Anitra E.

PY - 2020/10/1

Y1 - 2020/10/1

N2 - 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.

AB - 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.

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DO - 10.1038/s41396-020-0710-7

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AN - SCOPUS:85087614263

SN - 1751-7362

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JF - ISME Journal

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ER -

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

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