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Biological nitrogen fixation detected under Antarctic sea ice

Nature Geoscience volume 13, pages 729–732 (2020)Cite this article

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Matters Arising to this article was published on 11 January 2022

Abstract

Nitrogen fixation is the primary source of reactive nitrogen in the ocean. Most ecological models do not predict nitrogen fixation in the Antarctic Ocean because of the low availability of iron and high abundance of nitrogen. Here we extensively examined nitrogen fixation in the Antarctic Ocean, and found substantial nitrogen fixation (maximum: 44.4 nmol N l−1 d−1) near the Antarctic coast, especially around ice-covered regions. The nitrogenase gene (nifH) was detected at all coastal stations, including stations where no nitrogen fixation was found. At the stations where nitrogen fixation was detected, the nitrogen-fixing cyanobacterium UCYN-A (Candidatus ‘Atelocyanobacterium thalassa’) dominated nifH gene expression, and the nifH sequence was identical to that of the major oligotype in tropical and subtropical oceans. Our results suggest that marine nitrogen fixation is a ubiquitous process in the global ocean, and that UCYN-A is the keystone species for making it possible.

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Fig. 1: Sampling stations, maximum nitrogen fixation and diazotroph community composition in the Antarctic Ocean.
Fig. 2: Nitrogen fixation and UCYN-A abundance in the world ocean.

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Data availability

The sequence datasets generated for this study can be obtained from the DNA Data Bank of Japan Sequence Read Archive (number DRA009504). Background satellite-derived data are available in the UTokyo Repository (http://hdl.handle.net/2261/00079465). Source data are provided with this paper.

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Acknowledgements

We thank the captain, crew and participants of the 60th Japanese Antarctic Research Expedition (JARE-60) for their cooperation at sea and on land. We also thank H. Endo and C. Deutsch for helpful discussions, N. Takeda for help with the nutrient analyses and K. Turk-Kubo for providing the sequence data for UCYN-A. This research was supported financially by JSPS KAKENHI grant numbers JP19H04263 (T.S.), 20H04985 (T.S.), 17H01852 (F.H.) and JP15H05712 (N.H.) and the Simons Foundation (Simons Postdoctoral Fellowship in Marine Microbial Ecology) under award number 544338 (K.I.).

Author information

Authors and Affiliations

  1. Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan

    Takuhei Shiozaki

  2. Earth Surface System Research Center, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan

    Takuhei Shiozaki & Naomi Harada

  3. Institute of Arctic Climate and Environment Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan

    Amane Fujiwara

  4. School of Oceanography, University of Washington, Seattle, WA, USA

    Keisuke Inomura

  5. Department of Applied Chemistry and Life Science, Toyohashi University of Technology, Toyohashi, Japan

    Yuu Hirose

  6. Department of Ocean Sciences, Tokyo University of Marine Science and Technology, Minato-ku, Tokyo, Japan

    Fuminori Hashihama

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Contributions

T.S. and N.H. designed the research and collected the samples. T.S. conducted the measurements of the nitrogen fixation rate. A.F. conducted the satellite data analyses and visualized the data. T.S. and Y.H. supervised the molecular analyses. F.H. oversaw the nutrient analyses. T.S. and K.I. wrote the manuscript, with contributions from all co-authors.

Corresponding author

Correspondence to Takuhei Shiozaki.

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Peer review information Primary Handling Editor: Clare Davis.

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Extended data

Extended Data Fig. 1 Spatial distribution of environmental variables and UCYN-A1 abundance in the Antarctic Ocean.

(a) surface nitrate. (b) the surface total inorganic nitrogen/phosphate ratio in the surface water. (c) the maximum abundance of UCYN-A1. The details regarding the background contours and lines are described in Fig. 1.

Source data

Extended Data Fig. 2 Nonmetric multidimensional scaling (nMDS) plot derived from a Bray–Curtis distance matrix of the diazotroph community at each sampling station.

Beach (Sta. N and T), fast-ice (Sta. A–C), ice-edge (Sta. D, E, and EL), and ice-free (Sta. BP, CD0, and CD1) areas are shown in yellow, red, green, and blue, respectively.

Source data

Extended Data Fig. 3 Maximum-likelihood tree of diazotrophs constructed from nifH gene sequences.

The major phylotypes in the Southern Ocean (≥10% of total reads for each sample) are shown in red. The nifH sequences from isolated culture are shown in bold. Bootstrap values (> 50%) determined from 1,000 iterations are shown as purple circles, with the area proportional to the value.

Source data

Extended Data Fig. 4 Global map of the maximum abundance of UCYN-A.

Details of the dataset used in this study are written in Methods. Black circles indicate that UCYN-A was not detectable. Background contour lines indicate surface nitrate concentrations, obtained from the World Ocean Atlas 201834.

Source data

Source data

Source Data Fig. 1

Sampling locations, nitrogen fixation, diazotroph community composition and satellite data in the Antarctic Ocean. Background satellite-derived data are available in the UTokyo Repository (http://hdl.handle.net/2261/00079465).

Source Data Fig. 2

The depth-integrated rate of nitrogen fixation and maximum abundance of UCYN-A in the world ocean.

Source Data Extended Data Fig. 1

Nitrate, total inorganic nitrogen/phosphate ratio and UCYN-A in the Antarctic Ocean.

Source Data Extended Data Fig. 2

Sequence variant table used for the nMDS analysis.

Source Data Extended Data Fig. 3

Sequence data used to construct the phylogenetic tree.

Source Data Extended Data Fig. 4

Maximum abundance of UCYN-A in the world ocean.

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Shiozaki, T., Fujiwara, A., Inomura, K. et al. Biological nitrogen fixation detected under Antarctic sea ice. Nat. Geosci. 13, 729–732 (2020). https://doi.org/10.1038/s41561-020-00651-7

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