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High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean

Abstract

The availability of nitrogen is important in regulating biological productivity in marine environments. Deepwater nitrate has long been considered the major source of new nitrogen supporting primary production in oligotrophic regions of the open ocean, but recent studies have showed that biological N2 fixation has a critical role in supporting oceanic new production1,2,3,4,5,6,7. Large colonial cyanobacteria in the genus Trichodesmium and the heterocystous endosymbiont Richelia have traditionally been considered the dominant marine N2 fixers, but unicellular diazotrophic cyanobacteria and bacterioplankton have recently been found in the picoplankton and nanoplankton community of the North Pacific central gyre, and a variety of molecular and isotopic evidence suggests that these unicells could make a major contribution to the oceanic N budget8. Here we report rates of N2 fixation by these small, previously overlooked diazotrophs that, although spatially variable, can equal or exceed the rate of N2 fixation reported for larger, more obvious organisms. Direct measurements of 15N2 fixation by small diazotrophs in various parts of the Pacific Ocean, including the waters off Hawaii where the unicellular diazotrophs were first characterized, show that N2 fixation by unicellular diazotrophs can support a significant fraction of total new production in oligotrophic waters.

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Figure 1: Volumetric rate of N2 fixation by unicellular organisms in the North Pacific Ocean and near Australia.
Figure 2: Time course of N2 fixation in incubations under simulated in situ conditions.
Figure 3: Summary of rate measurements as a function of depth at stations along a transect in the eastern subtropical Pacific from Hawaii to San Diego (cruise Cook-25).

References

  1. 1

    Carpenter, E. J. & Romans, K. Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science 254, 1356–1358 (1991)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997)

    ADS  CAS  Article  Google Scholar 

  3. 3

    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)

    CAS  Article  Google Scholar 

  4. 4

    Michaels, A. F. et al. Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochemistry 35, 181–226 (1996)

    CAS  Article  Google Scholar 

  5. 5

    Karl, D. et al. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533–538 (1997)

    ADS  CAS  Article  Google Scholar 

  6. 6

    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)

    CAS  Article  Google Scholar 

  7. 7

    Montoya, J. P., Carpenter, E. J. & Capone, D. G. Nitrogen-fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic. Limnol. Oceanogr. 47, 1617–1628 (2002)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Zehr, J. P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Montoya, J. P., Voss, M., Kaehler, P. & Capone, D. G. A simple, high precision, high sensitivity tracer assay for dinitrogen fixation. Appl. Environ. Microbiol. 62, 986–993 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Dore, J. E., Brum, J. R., Tupas, L. & Karl, D. M. Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical North Pacific Ocean. Limnol. Oceanogr. 47, 1595–1607 (2002)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Falcon, L. I., Carpenter, E. J., Cipriano, F., Bergman, B. & Capone, D. G. N2 fixation by unicellular bacterioplankton from the Atlantic and Pacific Oceans: Phylogeny and in situ rates. Appl. Environ. Microbiol. 70, 765–770 (2004)

    CAS  Article  Google Scholar 

  12. 12

    Capone, D. G., O'Neil, J. M., Zehr, J. & Carpenter, E. J. Basis for diel variation in nitrogenase activity in the marine planktonic cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 56, 3532–3536 (1990)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Chen, Y.-B., Zehr, J. P. & Mellon, M. T. Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS101 in defined media: evidence for a circadian rhythm. J. Phycol. 32, 916–923 (1996)

    Article  Google Scholar 

  14. 14

    Lee, K., Karl, D. M., Wanninkhof, R. H. & Zhang, J. Z. Global estimates of net carbon production in the nitrate-depleted tropical and subtropical oceans. Geophys. Res. Lett. 29 (2002) doi: 10.1029/2001GLO14198

  15. 15

    Allen, C. B., Kanda, J. & Laws, E. A. New production and photosynthetic rates within and outside a cyclonic mesoscale eddy in the North Pacific subtropical gyre. Deep-Sea Res. I 43, 917–936 (1996)

    CAS  Article  Google Scholar 

  16. 16

    Aufdenkampe, A. K. et al. Biogeochemical controls on new production in the tropical Pacific. Deep-Sea Res. II 49, 2619–2648 (2002)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Carpenter, E. J., Subramaniam, A. & Capone, D. G. Biomass and productivity of the cyanobacterium, Trichodesmium spp. in the tropical North Atlantic Ocean. Deep-Sea Res. I 51, 173–203 (2004)

    CAS  Article  Google Scholar 

  18. 18

    Tillett, D. & Neilan, B. A. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. 36, 251–258 (2004)

    Article  Google Scholar 

  19. 19

    Zehr, J. P. & Turner, P. J. in Methods in Marine Microbiology (ed. Paul, J. H.) 271–286 (Academic, San Diego, 2001)

    Book  Google Scholar 

  20. 20

    Zehr, J. P. & McReynolds, L. A. Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 55, 2522–2526 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Wessel, P. & Smith, W. H. F. New, improved version of Generic Mapping Tools released. Eos 79, 579 (1998)

    ADS  Article  Google Scholar 

  22. 22

    Goering, J. J., Dugdale, R. C. & Menzel, D. W. Estimate of in situ rates of nitrogen uptake by Trichodesmium sp. in the Tropical Atlantic Ocean. Limnol. Oceanogr. 11, 614–620 (1966)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Carpenter, E. J. & Price, C. C. Nitrogen fixation, distribution and production of Oscillatoria (Trichodesmium) spp. in the western Sargasso and Caribbean Seas. Limnol. Oceanogr. 22, 60–72 (1977)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Orcutt, K. M. et al. A seasonal study of the significance of N2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-series Study (BATS) site. Deep-Sea Res. II 48, 1583–1608 (2001)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Gundersen, K. R. et al. Structure and biological dynamics of the oligotrophic ocean photic zone off the Hawaiian Islands. Pacif. Sci. 30, 45–68 (1976)

    CAS  Google Scholar 

  26. 26

    Saino, T. Biological Nitrogen Fixation in the Ocean with Emphasis on the Nitrogen Fixing Blue-Green Alga, Trichodesmium, and its Significance in the Nitrogen Cycle in the Low Latitude Sea Areas (Univ. Tokyo, Tokyo, 1977)

    Google Scholar 

  27. 27

    Capone, D. G. et al. An extensive bloom of the N2-fixing cyanobacterium, Trichodesmium erythraeum, in the central Arabian Sea. Mar. Ecol. Prog. Ser. 172, 281–292 (1998)

    ADS  Article  Google Scholar 

  28. 28

    Carpenter, E. J. et al. Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Mar. Ecol. Prog. Ser. 185, 273–283 (1999)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Deutsch, C. et al. Denitrification and N2 fixation in the Pacific Ocean. Glob. Biogeochem. Cycles 15, 483–506 (2001)

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank D. Karl and the entire HOT team for support in Hawaii; A. Gibson for collecting samples for molecular characterization on cruise Cook-25; C. Payne, K. Rathbun, S. Patel, K. Ghanouni, P. Davoodi and G. Stewart for their assistance in the laboratory analyses; and the captains and crews of the RV Ewing and RV Melville for their assistance at sea. This research was supported by grants from the National Science Foundation.

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Correspondence to Joseph P. Montoya.

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Montoya, J., Holl, C., Zehr, J. et al. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027–1031 (2004). https://doi.org/10.1038/nature02824

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