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

Author(s)
Yao Zhang, Wei Qin, Lei Hou, Emily J Zakem, Xianhui Wan, Zihao Zhao, Li Liu, Kristopher A Hunt, Nianzhi Jiao, Shuh-Ji Kao, Kai Tang, Xiabing Xie, Jiaming Shen, Yufang Li, Mingming Chen, Xiaofeng Dai, Chang Liu, Wenchao Deng, Minhan Dai, Anitra E Ingalls, David A Stahl, Gerhard J Herndl
Abstract

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 × 1013 to ∼2 × 1013 mol of C per year globally through the flux of ∼1 × 1014 to ∼2 × 1014 mol of N per year of the two steps of oxidation throughout the dark ocean.

Organisation(s)
Functional and Evolutionary Ecology
External organisation(s)
Xiamen University, University of Washington, University of Southern California, Royal Netherlands Institute for Sea Research
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN
0027-8424
DOI
https://doi.org/10.1073/pnas.1912367117
Publication date
02-2020
Peer reviewed
Yes
Austrian Fields of Science 2012
Marine biology
Portal url
https://ucris.univie.ac.at/portal/en/publications/nitrifier-adaptation-to-low-energy-flux-controls-inventory-of-reduced-nitrogen-in-the-dark-ocean(9229087a-f3cb-4b21-bfd4-c61f1f6d4345).html