Fixed nitrogen (N) often limits the growth of organisms in terrestrial and aquatic biomes1,2, and N availability has been important in controlling the CO2 balance of modern and ancient oceans3,4. The fixation of atmospheric dinitrogen gas (N2) to ammonia is catalysed by nitrogenase and provides a fixed N for N-limited environments2,5. The filamentous cyanobacterium Trichodesmium has been assumed to be the predominant oceanic N2-fixing microorganism since the discovery of N2 fixation in Trichodesmium in 1961 (ref. 6). Attention has recently focused on oceanic N2 fixation because nitrogen availability is generally limiting in many oceans, and attempts to constrain the global atmosphere–ocean fluxes of CO2 are based on basin-scale N balances7,8,9. Biogeochemical studies and models have suggested that total N2-fixation rates may be substantially greater than previously believed7,8 but cannot be reconciled with observed Trichodesmium abundances8,9. It is curious that there are so few known N2-fixing microorganisms in oligotrophic oceans when it is clearly ecologically advantageous. Here we show that there are unicellular cyanobacteria in the open ocean that are expressing nitrogenase, and are abundant enough to potentially have a significant role in N dynamics.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Nature Communications Open Access 10 February 2022
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115 (1991).
Howarth, R. W. & Marino, R. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33, 688–701 (1988).
Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997).
Haug, G. H. et al. Glacial/interglacial variations in production and nitrogen fixation in the Cariaco Basin during the last 580 kyr. Paleoceanography 13, 427–432 (1998).
Paerl, H. W. Physiological ecology and regulation of N2 fixation in natural waters. Adv. Microb. Ecol. 8, 305–344 (1990).
Dugdale, R. C., Menzel, D. W. & Ryther, J. H. Nitrogen fixation in the Sargasso Sea. Deep-Sea Res. 7, 298–300 (1961).
Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem. Cycles 11, 235–266 (1997).
Michaels, A. F. et al. Inputs, losses and transformations of nitrogen and phophorus in the pelagic North Atlantic Ocean. Biogeochemistry 35, 181–226 (1996).
Lipschultz, F. & Owens, N. J. P. An assessment of nitrogen fixation as a source of nitrogen to the North Atlantic Ocean. Biogeochemistry 35, 261–274 (1996).
Zehr, J. P., Mellon, M. T. & Zani, S. New nitrogen fixing microorganisms detected in oligotrophic oceans by the amplification of nitrogenase (nifH) genes. Appl. Environ. Microbiol. 64, 3444–3450 (1998).
Zehr, J. P., Carpenter, E. J. & Villareal, T. A. New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends Microbiol. 8, 68–73 (2000).
Chen, Y. -B., Dominic, B., Mellon, M. T. & Zehr, J. P. Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. Strain IMS 101. J. Bacteriol. 180, 3598–3605 (1998).
Beja, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).
Kolber, Z. S., Van Dover, C. L., Niederman, R. A. & Falkowski, P. G. Bacterial photosynthesis in surface waters of the open ocean. Nature 407, 177–179 (2000).
Reddy, K. J., Haskell, J. B., Sherman, D. M. & Sherman, L. A. Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J. Bacteriol. 175, 1284–1292 (1993).
Waterbury, J. B. & Rippka, R. in Bergey's Manual of Systematic Bacteriology Vol. 3 (ed. Staley, J. T.) 1728–1746 (Williams & Wilkins, Baltimore, 1989).
Neveux, J., Lantoine, F., Vaulot, D., Marie, D. & Blanchot, J. Phycoerythrins in the southern tropical and equatorial Pacific Ocean: evidence for new cyanobacterial types. J. Geophys. Res. 104, 3311–3321 (1999).
Campbell, L., Liu, H., Nolla, H. A. & Vaulot, D. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at station ALOHA during the 1991–1994 ENSO event. Deep-Sea Res. I 44, 167–192 (1997).
Brass, S. et al. Utilization of light for nitrogen fixation by a new Synechocystis strain is extended by its low photosynthetic efficiency. Appl. Environ. Microbiol. 60, 2575–2583 (1994).
Wasmund, N., Voss, M. & Lochte, K. Evidence of nitrogen fixation by non-heterocystous cyanobacteria in the Baltic Sea and re-calculation of a budget of nitrogen fixation. Mar. Ecol. Progr. Ser. 214, 1–14 (2001).
Letelier, R. M. & Karl, D. M. Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar. Ecol. Progr. Ser. 133, 263–273 (1996).
Lin, S., Henze, S. & Carpenter, E. J. Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 64, 3052–3058 (1998).
Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997).
Letelier, R. M. et al. Temporal variability of phytoplankton community structure based on pigment analysis. Limnol. Oceanogr. 38, 1420–1437 (1993).
Hawser, S. P., O'Neil, J. M., Roman, M. R. & Codd, G. A. Toxicity of blooms of the cyanobacterium Trichodesmium to zooplankton. J. Appl. Phys. 4, 79–86 (1992).
Karl, D. Comment: a new source of ‘new’ nitrogen in the sea. Trends Microbiol. 8, 301 (2000).
Zani, S., Mellon, M. T., Collier, J. L. & Zehr, J. P. Expression of nifH genes in natural microbial assemblages in Lake George, NY detected with RT-PCR. Appl. Environ. Microbiol. 66, 3119–3124 (2000).
Van de Peer, Y. & De Wachter, R. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Applic. Biosci. 10, 569–570 (1994).
We thank the crews and participants of the HOT programme, especially L. Tupas and J. Dore for field support. We also thank L. Campbell for providing flow cytometer data. This work was supported by NSF Division of Ocean Sciences grants to J.P.Z., J.P.M. and D.M.K.
About this article
Cite this article
Zehr, J., Waterbury, J., Turner, P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001). https://doi.org/10.1038/35088063
This article is cited by
Molecular mechanisms underlying iron and phosphorus co-limitation responses in the nitrogen-fixing cyanobacterium Crocosphaera
The ISME Journal (2022)
Nature Reviews Microbiology (2022)
Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean
The ISME Journal (2022)
Nature Communications (2022)
Acta Oceanologica Sinica (2022)