Nitrifier adaptation to low energy flux controls inventory of reduced nitrogen in the dark ocean.

carbon fixation dark ocean homeostasis nitrification nitrogen flux

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
03 03 2020
Historique:
pubmed: 20 2 2020
medline: 20 2 2020
entrez: 20 2 2020
Statut: ppublish

Résumé

Ammonia oxidation to nitrite and its subsequent oxidation to nitrate provides energy to the two populations of nitrifying chemoautotrophs in the energy-starved dark ocean, driving a coupling between reduced inorganic nitrogen (N) pools and production of new organic carbon (C) in the dark ocean. However, the relationship between the flux of new C production and the fluxes of N of the two steps of oxidation remains unclear. Here, we show that, despite orders-of-magnitude difference in cell abundances between ammonia oxidizers and nitrite oxidizers, the two populations sustain similar bulk N-oxidation rates throughout the deep waters with similarly high affinities for ammonia and nitrite under increasing substrate limitation, thus maintaining overall homeostasis in the oceanic nitrification pathway. Our observations confirm the theoretical predictions of a redox-informed ecosystem model. Using balances from this model, we suggest that consistently low ammonia and nitrite concentrations are maintained when the two populations have similarly high substrate affinities and their loss rates are proportional to their maximum growth rates. The stoichiometric relations between the fluxes of C and N indicate a threefold to fourfold higher C-fixation efficiency per mole of N oxidized by ammonia oxidizers compared to nitrite oxidizers due to nearly identical apparent energetic requirements for C fixation of the two populations. We estimate that the rate of chemoautotrophic C fixation amounts to ∼1 × 10

Identifiants

pubmed: 32071230
pii: 1912367117
doi: 10.1073/pnas.1912367117
pmc: PMC7060736
doi:

Banques de données

GENBANK
['GGEF00000000']

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

4823-4830

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Yao Zhang (Y)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China; yaozhang@xmu.edu.cn.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Wei Qin (W)

School of Oceanography, University of Washington, Seattle, WA 98195.

Lei Hou (L)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Emily J Zakem (EJ)

Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.

Xianhui Wan (X)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.

Zihao Zhao (Z)

Department of Limnology and Bio-Oceanography, Center of Functional Ecology, University of Vienna, A-1090 Vienna, Austria.

Li Liu (L)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Kristopher A Hunt (KA)

Department of Civil and Environmental Engineering, University of Washington, Seattle, WA 98195.

Nianzhi Jiao (N)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Shuh-Ji Kao (SJ)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Kai Tang (K)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Xiabing Xie (X)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.

Jiaming Shen (J)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Yufang Li (Y)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Mingming Chen (M)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Xiaofeng Dai (X)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Chang Liu (C)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Wenchao Deng (W)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.

Minhan Dai (M)

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361101 Xiamen, China.
College of Ocean and Earth Sciences, Xiamen University, 361101 Xiamen, China.

Anitra E Ingalls (AE)

School of Oceanography, University of Washington, Seattle, WA 98195.

David A Stahl (DA)

Department of Civil and Environmental Engineering, University of Washington, Seattle, WA 98195.

Gerhard J Herndl (GJ)

Department of Limnology and Bio-Oceanography, Center of Functional Ecology, University of Vienna, A-1090 Vienna, Austria.
Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Utrecht University, 1790 AB Den Burg, The Netherlands.

Classifications MeSH