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A microbial source of phosphonates in oligotrophic marine systems

Abstract

Phosphonates, compounds with a carbon–phosphorus bond, are a key component of the marine dissolved organic phosphorus pool1. These compounds serve as a phosphorus source for primary producers, including the nitrogen-fixing cyanobacteria Trichodesmium2. Phosphonates can therefore support marine primary production, as well as climate-driven increases in marine nitrogen fixation3, carbon sequestration4 and possibly methane production, through the breakdown of methylphosphonate5. Despite their importance, the source of phosphonates to the open ocean has remained uncertain. Here, we use solid-state nuclear magnetic resonance spectroscopy to screen for the presence of phosphonates in cultured strains of Trichodesmium erythraeum. We show that phosphonates comprise an average of 10% of the cellular particulate phosphorus pool in this species. We therefore suggest that these cyanobacteria produce phosphonates, and might be a significant source of these compounds in the ocean, particularly in nutrient-poor regions, where Trichodesmium blooms occur. Given that Trichodesmium also thrives in a warm, carbon-dioxide-rich environment3, phosphonate production may increase in the future. This, in turn, might select for a microbial community that can use phosphonate, and could have implications for nitrogen fixation, carbon sequestration and greenhouse-gas production.

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Figure 1: 31P NMR spectra from cultures and field populations of N2-fixing cyanobacteria denoting phosphorus (P) bond classes.
Figure 2: A plot of particulate phosphonate and particulate phosphorus content in cultures of Trichodesmium erythraeum IMS101.

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References

  1. Clark, L. L., Ingall, E. D. & Benner, R. Marine phosphorus is selectively remineralized. Nature 393, 426 (1998).

    Article  Google Scholar 

  2. Dyhrman, S. T. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71 (2006).

    Article  Google Scholar 

  3. Hutchins, D. A. et al. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293–1304 (2007).

    Article  Google Scholar 

  4. Karl, D. M. & Letelier, R. M. Nitrogen fixation-enhanced carbon sequestration in low nitrate, low chlorophyll seascapes. Mar. Ecol. Prog. Ser. 364, 257–268 (2008).

    Article  Google Scholar 

  5. Karl, D. M. et al. Aerobic production of methane in the sea. Nature Geosci. 1, 473–478 (2008).

    Article  Google Scholar 

  6. Alego, T. J. & Ingall, E. D. Sedimentary Corg:P ratios, paleocean ventilation and phanerozoic atmospheric pO2. Paloegeogr. Palaeoclimatol. Palaeoecol. 256, 130–155 (2007).

    Article  Google Scholar 

  7. Wu, J., Sunda, W. G., Boyle, E. A. & Karl, D. M. Phosphate depletion in the western North Atlantic Ocean. Science 289, 759–762 (2000).

    Article  Google Scholar 

  8. Mather, R. L. et al. Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres. Nature Geosci. 1, 439–443 (2008).

    Article  Google Scholar 

  9. Ilikchyan, I. N. et al. Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environ. Microbiol. 11, 1314–1324 (2009).

    Article  Google Scholar 

  10. Kittredge, J. S. & Roberts, E. A. A carbon–phosphorus bond in nature. Science 164, 37–42 (1969).

    Article  Google Scholar 

  11. Quin, L. D. The presence of compounds with a carbon–phosphorus bond in some marine invertebrates. Biochemistry 4, 324–330 (1965).

    Article  Google Scholar 

  12. Kittredge, J. S., Horiguchi, M. & Williams, P. M. Aminophosphonic acids: Biosynthesis by marine phytoplankton. Comp. Biochem. Physiol. 29, 859–863 (1969).

    Article  Google Scholar 

  13. Kononova, S. V. & Nesmeyanova, M. A. Phosphonates and their degradation by microorganisms. Biochemistry (Moscow) 67, 184–195 (2002).

    Article  Google Scholar 

  14. Sannigrahi, P., Ingall, E. D. & Benner, R. Nature and dynamics of phosphorus-containing components of marine dissolved and particulate organic matter. Geochim. Cosmochim. Acta 70, 5868–5882 (2006).

    Article  Google Scholar 

  15. Clark, L. L., Ingall, E. D. & Benner, R. Marine organic phosphorus cycling: Novel insights from nuclear magnetic resonance. Am. J. Sci. 299, 724–737 (1999).

    Article  Google Scholar 

  16. Antia, N. J., Harrison, P. J. & Oliveira, L. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia 30, 1–89 (1991).

    Article  Google Scholar 

  17. Karl, D. M. & Björkman, K. M. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. & Carlson, C.) 249–366 (Elsevier Science, 2002).

    Book  Google Scholar 

  18. Paytan, A., Cade-Menun, B., McLaughlin, K. & Faul, K. Selective phosphorus regeneration of sinking marine particles: Evidence from 31P-NMR. Mar. Chem. 82, 55–70 (2003).

    Article  Google Scholar 

  19. Benitez-Nelson, C. R. et al. Phosphonates and particulate organic phosphorus cycling in an anoxic marine basin. Limnol. Oceanogr. 49, 1593–1604 (2004).

    Article  Google Scholar 

  20. Orcutt, K. M. et al. Characterization of Trichodesmium spp. by genetic techniques. Appl. Environ. Microbiol. 68, 2236–2245 (2002).

    Article  Google Scholar 

  21. Van Mooy, B. A. S. et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009).

    Article  Google Scholar 

  22. Capone, D. G. et al. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221–1229 (1997).

    Article  Google Scholar 

  23. Davis, C. S. & McGillicuddy, D. J. Transatlantic abundance of the N2-fixing colonial cyanobacterium Trichodesmium. Science 312, 1517–1520 (2006).

    Article  Google Scholar 

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

    Google Scholar 

  25. 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. 48, 1583–1608 (2001).

    Article  Google Scholar 

  26. Karl, D. M., Bidigare, R. R. & Letelier, R. M. in Phytoplankton Productivity and Carbon Assimilation in Marine and Freshwater Ecosystems (eds Williams, P. J. le B., Thomas, D. R. & Reynolds, C. S.) 222–264 (Blackwell, 2002).

    Google Scholar 

  27. Ingall, E. D. Oceanography: Making methane. Nature Geosci. 1, 419–420 (2008).

    Article  Google Scholar 

  28. Webb, E. A., Moffett, J. W. & Waterbury, J. B. Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): Identification of the IdiA protein. Appl. Environ. Microbiol. 67, 5444–5452 (2001).

    Article  Google Scholar 

  29. Sherr, B. F., Sherr, E. B. & del Georgio, P. in Methods in Microbiology (ed. Paul, J. H.) 129–159 (Academic, 2001).

    Google Scholar 

  30. McGeorge, G., Alderman, D. W. & Grant, D. M. Resolution enhancement in 13C and 15N magic angle turning experiments with TPPM decoupling. J. Magn. Reson. 137, 138–143 (1999).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Science Foundation Biological and Chemical Oceanography Programs, the Center for Microbial Oceanography: Research and Education, and the Woods Hole Oceanographic Institution. The authors thank B. A. S. Van Mooy and E. Ingall for their helpful discussions, J. Waterbury for access to cultures and the participants of the ATP-3 project for assistance at sea.

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S.T.D. and C.R.B.-N. conceived of the study, processed samples and wrote the manuscript. E.D.O. and S.T.H. carried out the culture studies and P.J.P. did the 31P NMR spectroscopy.

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Correspondence to Sonya T. Dyhrman.

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Dyhrman, S., Benitez-Nelson, C., Orchard, E. et al. A microbial source of phosphonates in oligotrophic marine systems. Nature Geosci 2, 696–699 (2009). https://doi.org/10.1038/ngeo639

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