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The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle

Nature Microbiology volume 1, Article number: 16163 (2016) Cite this article

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Abstract

Microbial dinitrogen (N2) fixation, the nitrogenase enzyme-catalysed reduction of N2 gas into biologically available ammonia, is the main source of new nitrogen (N) in the ocean. For more than 50 years, oceanic N2 fixation has mainly been attributed to the activity of the colonial cyanobacterium Trichodesmium1,2. Other smaller N2-fixing microorganisms (diazotrophs)—in particular the unicellular cyanobacteria group A (UCYN-A)—are, however, abundant enough to potentially contribute significantly to N2 fixation in the surface waters of the oceans3–6. Despite their abundance, the contribution of UCYN-A to oceanic N2 fixation has so far not been directly quantified. Here, we show that in one of the main areas of oceanic N2 fixation, the tropical North Atlantic7, the symbiotic cyanobacterium UCYN-A contributed to N2 fixation similarly to Trichodesmium. Two types of UCYN-A, UCYN-A1 and -A2, were observed to live in symbioses with specific eukaryotic algae. Single-cell analyses showed that both algae–UCYN-A symbioses actively fixed N2, contributing ∼20% to N2 fixation in the tropical North Atlantic, revealing their significance in this region. These symbioses had growth rates five to ten times higher than Trichodesmium, implying a rapid transfer of UCYN-A-fixed N into the food web that might significantly raise their actual contribution to N2 fixation. Our analysis of global 16S rRNA gene databases showed that UCYN-A occurs in surface waters from the Arctic to the Antarctic Circle and thus probably contributes to N2 fixation in a much larger oceanic area than previously thought. Based on their high rates of N2 fixation and cosmopolitan distribution, we hypothesize that UCYN-A plays a major, but currently overlooked role in the oceanic N cycle.

Trichodesmium is one of the most abundant diazotrophs in the ocean7 and is generally considered the model organism for marine N2 fixation8,9. Field and laboratory experiments with Trichodesmium cultures have been used to derive crucial mathematical parameterization for biogeochemical models of marine productivity10,11. However, nitrogenase (nifH) gene diversity and abundances indicate that other unicellular diazotrophs are present in the ocean and potentially contribute significantly to N2 fixation rates3,4,6. UCYN-A (Candidatus Atelocyanobacterium thalassa12) is globally the most abundant of the unicellular diazotrophs7 as determined by quantitative PCR (qPCR) of the nifH gene, a marker gene for N2 fixation. UCYN-A lacks key genes for CO2 fixation13 and therefore lives in association with a haptophyte, a picoeukaryotic alga from which it receives fixed carbon12,14,15. In return, UCYN-A transfers up to 95% of its recently fixed N to the algal partner12,14,15. Despite its high abundance in the ocean, the contribution of UCYN-A to total N2 fixation has not been quantified.

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Figure 1: N2 fixation rates and the relative contribution of Trichodesmium and UCYN-A to N2 fixation.
Figure 2: Single-cell imaging and cellular activities using nanoSIMS.
Figure 3: Growth rates of UCYN-A associations.
Figure 4: Distribution of UCYN-A in the world's oceans.

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Acknowledgements

The authors thank the captain and crew of R/V Meteor M96 cruise, and G. Klockgether, A. Ellrott, C. Hoffmann, M. Philippi and L. Piepgras for cruise and technical support. The authors thank T. Ferdelman, J. Milucka and H. Marchant for discussions. This research was funded by the Max Planck Society, the Collaborative Research Center 754 (SFB754), the Fundació ‘La Caixa’, the German Academic Exchange Service (DAAD) and a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme.

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Author notes

  1. Carolin R. Löscher & Julie LaRoche

    Present address: † Present addresses: Nordic Center for Earth Evolution, Department of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark (C.R.L.); Department of Biology, Dalhousie University, 1355 Oxford St, PO Box 15000, Halifax, Nova Scotia B3H 4R2, Canada (J.L.).,

Authors and Affiliations

  1. Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany

    Clara Martínez-Pérez, Wiebke Mohr, Julien Dekaezemacker, Sten Littmann, Pelin Yilmaz, Nadine Lehnen, Bernhard M. Fuchs, Gaute Lavik & Marcel M. M. Kuypers

  2. Department of General Microbiology Christian-Albrechts-University Kiel, Christian-Albrechts-University Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany

    Carolin R. Löscher & Ruth A. Schmitz

  3. Department of Biogeochemistry, Helmholtz Centre for Ocean Research (GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany

    Julie LaRoche

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Contributions

M.M.M.K., together with R.A.S., C.M.-P. and J.D., designed the study. C.M.-P., W.M. and J.D. performed the experiments. C.M.-P., W.M., C.R.L., J.D., G.L. and S.L. analysed samples and data. P.Y. analysed and mapped the nifH and next-generation sequencing databases. N.L., B.M.F. and J.L.R. analysed the nifH amplicon sequences and generated the phylogenetic trees. B.M.F. contributed to the CARD–FISH identification of the two different UCYN-A–haptophyte symbioses. J.L.R. contributed unpublished nifH qPCR data. C.M.-P., W.M. and M.M.M.K. wrote the manuscript with the contributions of all co-authors.

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Correspondence to Wiebke Mohr.

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Supplementary information

Supplementary information

Supplementary Figure 1–7, legends for Supplementary Tables 1 and 2, Supplementary Table 3, Supplementary References (PDF 13443 kb)

Supplementary Table 1

Diazotroph abundances, CO2 and N2 fixation rates and nutrient concentrations during the M96 cruise. (XLSX 26 kb)

Supplementary Table 2

Metadata of ICoMM, OSD, and TARA Oceans samples analysed in this study and the descriptive statistics from the SILVAngs pipeline. (XLS 189 kb)

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Martínez-Pérez, C., Mohr, W., Löscher, C. et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat Microbiol 1, 16163 (2016). https://doi.org/10.1038/nmicrobiol.2016.163

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