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Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans

Abstract

Whereas the non-heterocystous cyanobacteria Trichodesmium spp. are the dominant N2-fixing organisms in the tropical oceans1, heterocystous species dominate N2 fixation in freshwater lakes and brackish environments such as the Baltic Sea2. So far no satisfactory explanation for the absence of heterocystous cyanobacteria in the pelagic of the tropical oceans has been given, even though heterocysts would seem to represent an ideal strategy for protecting nitrogenase from being inactivated by O2, thereby enabling cyanobacteria to fix N2 and to perform photosynthesis simultaneously. Trichodesmium is capable of N2 fixation, apparently without needing to differentiate heterocysts3. Here we show that differences in the temperature dependence of O2 flux, respiration and N2 fixation activity explain how Trichodesmium performs better than heterocystous species at higher temperatures. Our results also explain why Trichodesmium is not successful in temperate or cold seas. The absence of heterocystous cyanobacteria in the pelagic zone of temperate and cold seas, however, requires another explanation.

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Figure 1: Relationship of nitrogenase activity versus temperature measured at 20% O2.
Figure 2: Theoretical enzyme activity curves with a Q10* of 2 (unbroken line) and a Q10* of 1.16 (broken line).
Figure 3: Changes in the ratio of Ntot to Nd with temperature.

References

  1. Karl, D. et al. Dinitrogen fixation in the world's oceans. Biogeochemistry 57/58, 47–98 (2002)

    CAS  Article  Google Scholar 

  2. Laamanen, M. Environmental factors affecting the occurrence of different morphological forms of cyanoprokaryotes in the northern Baltic Sea. J. Plankt. Res. 19, 1385–1403 (1997)

    Article  Google Scholar 

  3. Berman-Frank, I. et al. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294, 1534–1537 (2001)

    ADS  CAS  Article  Google Scholar 

  4. Berman-Frank, I., Cullen, J. T., Shaked, Y., Sherrell, R. M. & Falkowski, P. G. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol. Oceanogr. 46, 1249–1260 (2001)

    ADS  CAS  Article  Google Scholar 

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

    ADS  Article  Google Scholar 

  6. Carpenter, E. J. & Janson, S. Anabaena gerdii sp. nov., a new planktonic filamentous cyanobacterium from the South Pacific Ocean and Arabian Sea. Phycologia 40, 105–110 (2001)

    Google Scholar 

  7. Bergman, B., Gallon, J. R., Rai, A. N. & Stal, L. J. N2 fixation by non-heterocystus cyanobacteria. FEMS Microb. Rev. 19, 139–185 (1997)

    CAS  Article  Google Scholar 

  8. Walsby, A. E. The permeability of heterocysts to the gases nitrogen and oxygen. Proc. R. Soc. Lond. B 226, 345–366 (1985)

    ADS  CAS  Article  Google Scholar 

  9. Wolk, C. P., Ernst, A. & Elhai, J. in The Molecular Biology of Cyanobacteria (ed. Bryant, D. A.) 770–823 (Kluwer Academic, Dordrecht, 1994)

    Google Scholar 

  10. Hoffmann, L. Marine cyanobacteria in tropical regions: diversity and ecology. Eur. J. Phycol. 34, 371–379 (1999)

    Article  Google Scholar 

  11. Kana, T. M. Rapid oxygen cycling in Trichodesmium thieboutii. Limnol. Oceanogr. 38, 18–24 (1993)

    ADS  CAS  Article  Google Scholar 

  12. Staal, M., te Lintel Hekkert, S., Herman, P. & Stal, L. J. Comparison of models describing light dependency of N2 fixation in heterocystous cyanobacteria. Appl. Environ. Microbiol. 68, 4679–4683 (2002)

    CAS  Article  Google Scholar 

  13. Stal, L. J. & Walsby, A. E. Photosynthesis and nitrogen fixation in a cyanobacterial bloom in the Baltic Sea. Eur. J. Phycol. 35, 97–108 (2000)

    Article  Google Scholar 

  14. Davison, I. R. Environmental effects on algal photosynthesis: temperature. J. Phycol. 27, 2–8 (1991)

    Article  Google Scholar 

  15. Kangatharalingam, N., Dodds, W. K., Priscu, J. C. & Paerl, H. W. Nitrogenase activity, photosynthesis, and the degree of heterocyst aggregation in the cyanobacterium Anabaena flos-aquae. J. Phycol. 27, 680–686 (1991)

    CAS  Article  Google Scholar 

  16. Murry, M. A. & Wolk, C. P. Evidence that the barrier to the penetration of oxygen to heterocysts depends upon two layers of the cell envelope. Arch. Microbiol. 151, 469–474 (1989)

    CAS  Article  Google Scholar 

  17. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1–61 (1979)

    Google Scholar 

  18. Chen, Y. B., Zehr, J. P. & Mellon, M. Growth and nitrogen fixation of the diazotrophic filamentous non-heterocystous cyanobacterium Trichodesmium sp. IMS 101 in defined media: evidence for a circadian rhythm. J. Phycol. 32, 916–923 (1996)

    Article  Google Scholar 

  19. Staal, M., te Lintel-Hekkert, S., Harren, F. & Stal, L. J. Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay: a comparison between batch incubation and on-line monitoring. Environ. Microbiol. 3, 343–351 (2001)

    CAS  Article  Google Scholar 

  20. Talling, J. F. Photosynthetic characteristics of some freshwater plankton diatoms in relation to underwater radiation. New Phytol. 56, 29–50 (1957)

    Article  Google Scholar 

Download references

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Correspondence to Marc Staal.

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Supplementary information

41586_2003_BFnature01999_MOESM1_ESM.doc

Supplementary Appendix A: Mathematical derivation of a general N2-fixing cell model describing a spherical diffusion system with a diffusion resistant layer resembling a heterocyst (spherical geometry) (DOC 170 kb)

41586_2003_BFnature01999_MOESM2_ESM.doc

Supplementary Appendix B: Mathematical derivation of a general N2-fixing cell model describing a cylindrical diffusion system resembling a cluster of diazocyte cells (cylindrical geometry) (DOC 118 kb)

41586_2003_BFnature01999_MOESM3_ESM.doc

Supplementary Appendix C: O2 optima for nitrogenase activity (acetylene reduction) for Nodularia spumigena (strain CCY 9414), Anabaena sp. (strain CCY 9901) and Trichodesmium sp. (strain IMS101) (DOC 31 kb)

Supplementary Appendix D: Heterocystous cyanobacteria from which Ntot/Nd ratios were determined. (DOC 37 kb)

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Staal, M., Meysman, F. & Stal, L. Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans. Nature 425, 504–507 (2003). https://doi.org/10.1038/nature01999

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