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New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods

The ISME Journal volume 14, pages2514–2526(2020)Cite this article

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Abstract

Nitrogen availability limits marine productivity across large ocean regions. Diazotrophs can supply new nitrogen to the marine environment via nitrogen (N2) fixation, relieving nitrogen limitation. The distributions of diazotrophs and N2 fixation have been hypothesized to be generally controlled by temperature, phosphorus, and iron availability in the global ocean. However, even in the North Atlantic where most research on diazotrophs and N2 fixation has taken place, environmental controls remain contentious. Here we measure diazotroph composition, abundance, and activity at high resolution using newly developed underway sampling and sensing techniques. We capture a diazotrophic community shift from Trichodesmium to UCYN-A between the oligotrophic, warm (25–29 °C) Sargasso Sea and relatively nutrient-enriched, cold (13–24 °C) subpolar and eastern American coastal waters. Meanwhile, N2 fixation rates measured in this study are among the highest ever recorded globally and show significant increase with phosphorus availability across the transition from the Gulf Stream into subpolar and coastal waters despite colder temperatures and higher nitrate concentrations. Transcriptional patterns in both Trichodesmium and UCYN-A indicate phosphorus stress in the subtropical gyre. Over this iron-replete transect spanning the western North Atlantic, our results suggest that temperature is the major factor controlling the diazotrophic community structure while phosphorous drives N2 fixation rates. Overall, the occurrence of record-high UCYN-A abundance and peak N2 fixation rates in the cold coastal region where nitrate concentrations are highest (~200 nM) challenges current paradigms on what drives the distribution of diazotrophs and N2 fixation.

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Fig. 1: N2 fixation rates and molecular sampling sites.
Fig. 2: Contribution of N2 fixation (NF) to marine production.
Fig. 3: Relative abundance of nifH OTUs recovered from community DNA in discrete samples collected near noon daily shown in Fig. 1b.
Fig. 4: Environmental properties, N2 fixation rates, diazotroph abundances, and nifH transcription patterns along the transect.
Fig. 5: Spearman’s rank correlation analyses between surface daily N2 fixation rates and environmental properties.
Fig. 6: Relations between quantitative diazotroph nifH gene abundances and various environmental properties.
Fig. 7: Evidence suggesting phosphorus limitation in diazotrophs.

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Acknowledgements

We thank the marine technicians and crew of the R/V Atlantic Explorer for their invaluable help during the cruise. We appreciate discussions with M. Susan Lozier (Duke University) on the analysis of physical supply of phosphorus. We would also like to thank NASA and NOAA for processing and distributing the Ocean Color, and World Ocean Atlas and ETOPO1 bathymetry data, respectively. This study has been conducted using E.U. Copernicus Marine Service Information (geostrophic velocity). WT would like to thank Yajuan Lin (Duke University) for suggestions on the analysis of nifH sequences. WT’s visit to National Oceanography Centre (Southampton) was funded by the Duke Graduate School and Duke Interdisciplinary Studies through The Dissertation Research Travel Award: International and the Graduate Student Training Enhancement Grant (GSTEG), respectively. NC, WT, and SW were supported by the NSF-CAREER grant (#1350710). NC, HP and HW were also funded by the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19) and co-funded by a grant from the French government under the program “Investissements d’Avenir”. JR, MM and RoCSI development costs were supported by NERC grant NE/N006496/1 and AtlantOS (Horizon 2020).

Author information

Author notes

  1. Weiyi Tang

    Present address: Department of Geosciences, Princeton University, Princeton, NJ, 08544, USA

  2. Hannah Whitby

    Present address: Department of Earth, Ocean and Ecological Sciences, School of Environmental Sciences, University of Liverpool, Liverpool, L69 3GP, UK

Affiliations

  1. Division of Earth and Ocean Sciences, Nicholas School of the Environment, Duke University, Durham, NC, 27708, USA

    Weiyi Tang, Seaver Wang & Nicolas Cassar

  2. Department of Ocean and Earth Sciences, National Oceanography Centre, University of Southampton, European Way, SO14 3ZH, Southampton, UK

    Elena Cerdán-García, Despo Polyviou & Alison Baylay

  3. CNRS, Univ Brest, IRD, Ifremer, LEMAR, F-29280 Plouzané, France

    Hugo Berthelot, Hannah Whitby, Hélène Planquette & Nicolas Cassar

  4. Ocean Technology and Engineering Group, National Oceanography Centre, European Way, SO14 3ZH, Southampton, UK

    Matthew Mowlem & Julie Robidart

Authors
  1. Weiyi Tang
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  2. Elena Cerdán-García
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  3. Hugo Berthelot
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  4. Despo Polyviou
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  5. Seaver Wang
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  6. Alison Baylay
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  7. Hannah Whitby
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  8. Hélène Planquette
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  9. Matthew Mowlem
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  10. Julie Robidart
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  11. Nicolas Cassar
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Corresponding authors

Correspondence to Julie Robidart or Nicolas Cassar.

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Tang, W., Cerdán-García, E., Berthelot, H. et al. New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods. ISME J 14, 2514–2526 (2020). https://doi.org/10.1038/s41396-020-0703-6

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