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Phosphonate utilization by the globally important marine diazotroph Trichodesmium

Abstract

The factors that control the growth and nitrogen fixation rates of marine diazotrophs such as Trichodesmium have been intensively studied because of the role that these processes have in the global cycling of carbon and nitrogen, and in the sequestration of carbon to the deep sea. Because the phosphate concentrations of many ocean gyres are low1, the bioavailability of the larger, chemically heterogeneous pool of dissolved organic phosphorus could markedly influence Trichodesmium physiology. Here we describe the induction, by phosphorus stress, of genes from the Trichodesmium erythraeum IMS101 genome that are predicted to encode proteins associated with the high-affinity transport and hydrolysis of phosphonate compounds by a carbon–phosphorus lyase pathway. We show the importance of these genes through expression analyses with T. erythraeum from the Sargasso Sea. Phosphonates are known to be present in oligotrophic marine systems, but have not previously been considered to be bioavailable to marine diazotrophs. The apparent absence of genes encoding a carbon–phosphorus lyase pathway in the other marine cyanobacterial genomes suggests that, relative to other phytoplankton, Trichodesmium is uniquely adapted for scavenging phosphorus from organic sources. This adaptation may help to explain the prevalence of Trichodesmium in low phosphate, oligotrophic systems.

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Figure 1: DNA topology of the phn cluster and phylogenetic analyses of the PhnJ protein.
Figure 2: Expression of phnD and phnJ in cultures and field populations of T. erythraeum.

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Acknowledgements

We thank the captain and crew of the RV Oceanus, I. Ehrenreich and R. Wisniewski for assistance; and V. Edgecomb and F. Valois for suggestions on the manuscript. The T. erythraeum IMS101 genome was produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/). This work was supported by the National Science Foundation Biological Oceanography Program, the Woods Hole Oceanographic Institution and the Princeton Center for BioInorganic Chemistry. Author Contributions S.T.D. and E.A.W. designed the research and wrote the paper; S.T.D., J.W.M and E.A.W performed the field work; P.D.C, S.T.D, S.T.H., E.D.O., J.B.W. and E.A.W. performed the laboratory work; and E.A.W. performed the genome searches and phylogenetic analyses.

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Correspondence to E. A. Webb.

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Competing interests

The sequences of phnJ and phnD from the different Trichodesmium species have been deposited in GenBank with accession numbers DQ176437–DQ176442. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

This is a sequence alignment of phnJ from species of the genus Trichodesmium. (DOC 290 kb)

Supplementary Figure 2

This is a sequence alignment of phnD from species of the genus Trichodesmium. (DOC 136 kb)

Supplementary Table 1

This table lists the % identity between the Trichodemsium Phn orthologs and several different microbes. (DOC 26 kb)

Supplementary Table 2

This table lists analyses and estimates of dissolved inorganic phosphate, and dissolved organic phosphorus at the three field stations in the western North Atlantic along with other field parameters. (DOC 20 kb)

Supplementary Data

This contains the full amino acid sequences. (TXT 9 kb)

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Dyhrman, S., Chappell, P., Haley, S. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71 (2006). https://doi.org/10.1038/nature04203

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