Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Ocean warming alleviates iron limitation of marine nitrogen fixation

Nature Climate Change volume 8, pages 709–712 (2018)Cite this article

Subjects

Abstract

The cyanobacterium Trichodesmium fixes as much as half of the nitrogen (N2) that supports tropical open-ocean biomes, but its growth is frequently limited by iron (Fe) availability1,2. How future ocean warming may interact with this globally widespread Fe limitation of Trichodesmium N2 fixation is unclear3. Here, we show that the optimum growth temperature of Fe-limited Trichodesmium is ~5 °C higher than for Fe-replete cells, which results in large increases in growth and N2 fixation under the projected warmer Fe-deplete sea surface conditions. Concurrently, the cellular Fe content decreases as temperature rises. Together, these two trends result in thermally driven increases of ~470% in Fe-limited cellular iron use efficiencies (IUEs), defined as the molar quantity of N2 fixed by Trichodesmium per unit time per mole of cellular Fe (mol N2 fixed h–1 mol Fe–1), which enables Trichodesmium to much more efficiently leverage the scarce available Fe supplies to support N2 fixation. Modelling these results in the context of the IPCC representative concentration pathway (RCP) 8.5 global warming scenario4 predicts that IUEs of N2 fixers could increase by ~76% by 2100, and largely alleviate the prevailing Fe limitation across broad expanses of the tropical Pacific and Indian Oceans. Thermally enhanced cyanobacterial IUEs could increase future global marine N2 fixation by ~22% over the next century, and thus profoundly alter the biology and biogeochemistry of open-ocean ecosystems.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Trichodesmium growth responses to Fe availability and warming interactions.
Fig. 2: Responses of Trichodesmium N2 fixation, CO2 fixation and IUEs to Fe availability and warming.
Fig. 3: Modelled consequences of Fe and warming interactions for future changes in global IUE and N2 fixation.

Similar content being viewed by others

References

  1. Capone, D. G., Zehr, J. P., Paerl, H. W., Bergman, B. & Carpenter, E. J. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221–1229 (1997).

    Article  CAS  Google Scholar 

  2. Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9, 499–508 (2011).

    Article  CAS  Google Scholar 

  3. Hutchins, D. A. & Boyd, P. Marine phytoplankton and the changing ocean iron cycle. Nat. Clim. Change 6, 1072–1079 (2016).

    Article  CAS  Google Scholar 

  4. IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

  5. Breitbarth, E., Oschilles, A. & LaRoche, J. L. Physiological constraints on the global distribution of Trichodesmium—effect of temperature on diazotrophy. Biogeosciences 4, 53–61 (2007).

  6. Fu, F.-X. et al. Differing responses of marine N2-fixers to warming and consequences for future diazotroph community structure. Aquat. Microb. Ecol. 72, 33–46 (2014).

    Article  Google Scholar 

  7. Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476 (2012).

    Article  CAS  Google Scholar 

  8. Fu, F. X., Warner, M. E., Zhang, Y., Feng, Y. & Hutchins, D. A. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43, 485–496 (2007).

  9. Sunda, W. G. & Huntsman, S. A. Interactive effects of light and temperature on iron limitation in a marine diatom: implications for marine productivity and carbon cycling. Limnol. Oceanogr. 56, 1475–1488 (2011).

    Article  CAS  Google Scholar 

  10. Boyd, P. et al. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nat. Clim. Change 6, 207–213 (2016).

    Article  Google Scholar 

  11. Kustka, A., Sañudo-Wilhelmy, S. A., Carpenter, E. J., Capone, D. G. & Raven, J. A. A revised estimate of the iron use efficiency of nitrogen fixation, with special reference to the marine cyanobacterium Trichodesmium (Cyanophyta). J. Phycol. 39, 12–25 (2003).

    Article  CAS  Google Scholar 

  12. Sañudo-Wilhelmy, S. A. et al. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66–69 (2001).

    Article  Google Scholar 

  13. Walworth, N. G. et al. Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat. Commun. 7, 12081 (2016).

    Article  CAS  Google Scholar 

  14. Xu, K., Fu, F.-X. & Hutchins, D. A. Comparative responses of two dominant Antarctic phytoplankton taxa to interactions between ocean acidification, warming, irradiance, and iron availability. Limnol. Oceanogr. 59, 919–931 (2014).

    Article  Google Scholar 

  15. Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat. Clim. Change 3, 979–984 (2013).

    Article  CAS  Google Scholar 

  16. Fasham, M. J. R., Ducklow, H. W. & McKelvie, S. M. A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J. Mar. Res. 48, 591–639 (1990).

    Article  CAS  Google Scholar 

  17. Geider, R. J., MacIntyre, H. L. & Kana, T. M. Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Mar. Ecol. Progr. Ser. 148, 187–200 (1997).

  18. Moore, J. K., Lindsay, K., Doney, S. C., Long, M. C. & Misumi, K. Marine ecosystem dynamics and biogeochemical cycling in the Community Earth System Model [CESM1(BGC)]: comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 scenarios. J. Clim. 26, 9291–9312 (2013).

  19. Behrenfeld, M. J. & Kolber, Z. S. Widespread iron limitation of phytoplankton in the South Pacific. Ocean. Sci. 283, 840–843 (1999).

    CAS  Google Scholar 

  20. Dutkiewicz, S., Ward, B. A., Monteiro, F. M. & Follows, M. J. Interconnection of nitrogen fixers and iron in the Pacific Ocean: theory and numerical simulations. Glob. Biogeochem. Cycles 26, GB1012 (2012).

    Article  Google Scholar 

  21. Carpenter, E. J. and Capone, D. G. in Nitrogen in the Marine Environment 2nd edn (eds Capone, D. G. et al.) Ch. 4 (Academic, London, 2008).

  22. Hutchins, D. A., Fu, F.-X., Webb, E. A., Walworth, N. & Tagliabue, A. Taxon-specific responses of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat. Geosci. 6, 790–795 (2013).

    Article  CAS  Google Scholar 

  23. Hutchins, D. A. et al. Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nat. Commun. 6, 8155 (2015).

    Article  Google Scholar 

  24. Fu, F.-X. et al. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 53, 2472–2484 (2008).

    Article  CAS  Google Scholar 

  25. Doney, S. C. et al. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4, 11–37 (2012).

    Article  Google Scholar 

  26. Boyce, D. G., Lewis, M. R., M. R. & Worm, M. R. Global phytoplankton decline over the past century. Nature 466, 591–596 (2010).

    Article  CAS  Google Scholar 

  27. Behrenfeld, M. J. et al. Revaluating ocean warming impacts on global phytoplankton. Nat. Clim. Change 6, 323–330 (2016).

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by US National Science Foundation grants OCE 1657757, OCE 1638804, OCE 1538525, OCE 1260233 and OCE 1260490 and National Natural Science Foundation of China grants 31470171 and 31770033.

Author information

Authors and Affiliations

  1. Central China Normal University, Wuhan, Hubei, China

    Hai-Bo Jiang

  2. University of Southern California, Los Angeles, CA, USA

    Fei-Xue Fu, Sara Rivero-Calle, Naomi M. Levine, Sergio A. Sañudo-Wilhelmy, Ping-Ping Qu, Paulina Pinedo-Gonzalez & David A. Hutchins

  3. Xiamen University, Xiamen, Fujian, China

    Xin-Wei Wang

  4. Shanghai Jiao Tong University, Minhang District, Shanghai, China

    Zhu Zhu

Authors
  1. Hai-Bo Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei-Xue Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sara Rivero-Calle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naomi M. Levine
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sergio A. Sañudo-Wilhelmy
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping-Ping Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xin-Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paulina Pinedo-Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhu Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. David A. Hutchins
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H.B.J., D.A.H. and F.-X.F. contributed to conceiving and planning the experiments, H.B.J., F.-X.F., P.P.Q., X.-W.W. and Z.Z. performed the lab experiments, P.P.G. and S.A.S.-W. contributed analytical work, S.-R.C. and N.M.L. contributed modelling work, H.B.J. and D.A.H. contributed to writing the paper and all of the authors contributed comments, revisions and editing.

Corresponding author

Correspondence to David A. Hutchins.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods and Supplementary Methods’s References, Supplementary Figures 1–15, Supplementary Tables 1–6

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, HB., Fu, FX., Rivero-Calle, S. et al. Ocean warming alleviates iron limitation of marine nitrogen fixation. Nature Clim Change 8, 709–712 (2018). https://doi.org/10.1038/s41558-018-0216-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41558-018-0216-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology