Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Gramibactin is a bacterial siderophore with a diazeniumdiolate ligand system

This article has been updated


Genome mining and chemical analyses revealed that rhizosphere bacteria (Paraburkholderia graminis) produce a new type of siderophore, gramibactin, a lipodepsipeptide that efficiently binds iron with a logβ value of 27.6. Complexation-induced proton NMR chemical shifts show that the unusual N-nitrosohydroxylamine (diazeniumdiolate) moieties participate in metal binding. Gramibactin biosynthesis genes are conserved in numerous plant-associated bacteria associated with rice, wheat, and maize, which may utilize iron from the complex.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Identification and structure elucidation of gramibactin.
Fig. 2: Characterization of metal-gramibactin complexes.

Change history

  • 06 August 2019

    In the version of this article originally published, compound numbers 4 and 6 were not linked correctly to their respective compound pages. The error has been corrected in the HTML version of this paper.


  1. Hider, R. C. & Kong, X. Nat. Prod. Rep. 27, 637–657 (2010).

    Article  CAS  Google Scholar 

  2. Zhang, R., Vivanco, J. M. & Shen, Q. Curr. Opin. Microbiol. 37, 8–14 (2017).

    Article  Google Scholar 

  3. Jin, C. W., Ye, Y. Q. & Zheng, S. J. Ann. Bot 113, 7–18 (2014).

    Article  CAS  Google Scholar 

  4. Viallard, V. et al. Int. J. Syst. Bacteriol. 48, 549–563 (1998).

    Article  CAS  Google Scholar 

  5. Noinaj, N., Guillier, M., Barnard, T. J. & Buchanan, S. K. Annu. Rev. Microbiol. 64, 43–60 (2010).

    Article  CAS  Google Scholar 

  6. Zuleta, L. F. G. et al. BMC Genom. 15, 535 (2014).

    Article  Google Scholar 

  7. Ohtsubo, Y. et al. Genome Announc. 3, e01283–15 (2015).

    PubMed  PubMed Central  Google Scholar 

  8. Coutinho, B. G., Passos da Silva, D., Previato, J. O., Mendonça-Previato, L. & Venturi, V. Genome Announc. 1, e0022512 (2013).

    Article  Google Scholar 

  9. Franke, J., Ishida, K., Ishida-Ito, M. & Hertweck, C. Angew. Chem. Int. Ed. Engl. 52, 8271–8275 (2013).

    Article  CAS  Google Scholar 

  10. Franke, J., Ishida, K. & Hertweck, C. J. Am. Chem. Soc. 136, 5599–5602 (2014).

    Article  CAS  Google Scholar 

  11. Feigl, F. & Neto, C. C. Anal. Chem. 28, 1311–1312 (1956).

    Article  CAS  Google Scholar 

  12. Hrabie, J. A. & Keefer, L. K. Chem. Rev. 102, 1135–1154 (2002).

    Article  CAS  Google Scholar 

  13. Kobayashi, T. & Nishizawa, N. K. Annu. Rev. Plant Biol. 63, 131–152 (2012).

    Article  CAS  Google Scholar 

  14. Staiger, D. Angew. Chem. Int. Ed. Engl. 41, 2259–2264 (2002).

    Article  CAS  Google Scholar 

  15. Jin, C. W., Li, G. X., Yu, X. H. & Zheng, S. J. Ann. Bot 105, 835–841 (2010).

    Article  CAS  Google Scholar 

  16. Carrillo-Castañeda, G., Munoz, J. J., Peralta-Videa, J. R., Gomez, E. & Gardea-Torresdey, J. L. J. Plant Nutr. 28, 1853–1865 (2005).

    Article  Google Scholar 

  17. Kraepiel, A. M., Bellenger, J. P., Wichard, T. & Morel, F. M. Biometals 22, 573–581 (2009).

    Article  CAS  Google Scholar 

  18. Chen, L. M., Dick, W. A. & Streeter, J. G. J. Plant Nutr. 23, 2047–2060 (2000).

    Article  CAS  Google Scholar 

  19. Vansuyt, G., Robin, A., Briat, J. F., Curie, C. & Lemanceau, P. Mol. Plant Microbe Interact. 20, 441–447 (2007).

    Article  CAS  Google Scholar 

  20. Yehuda, Z., Shenker, M., Hadar, Y. & Chen, Y. J. Plant Nutr. 23, 1991–2006 (2000).

    Article  CAS  Google Scholar 

  21. Radzki, W. et al. Antonie van Leeuwenhoek 104, 321–330 (2013).

    Article  CAS  Google Scholar 

  22. Ishida, K., Lincke, T., Behnken, S. & Hertweck, C. J. Am. Chem. Soc. 132, 13966–13968 (2010).

    Article  CAS  Google Scholar 

  23. Buss, H. L., Lüttge, A. & Brantley, S. L. Chem. Geol. 240, 326–342 (2007).

    Article  CAS  Google Scholar 

  24. Ishida, K., Lincke, T. & Hertweck, C. Angew. Chem. Int. Ed. Engl. 51, 5470–5474 (2012).

    Article  CAS  Google Scholar 

  25. Louden, B. C., Haarmann, D. & Lynne, A. M. J. Microbiol. Biol. Educ. 12, 51–53 (2011).

    Article  Google Scholar 

  26. Bhushan, R. & Brückner, H. Amino Acids 27, 231–247 (2004).

    Article  CAS  Google Scholar 

  27. Fujii, K. et al. Anal. Chem. 69, 3346–3352 (1997).

    Article  CAS  Google Scholar 

  28. Goodlett, D. R. et al. J. Chromatogr. A 707, 233–244 (1995).

    Article  CAS  Google Scholar 

  29. Bretti, C., Cigala, R. M., Lando, G., Milea, D. & Sammartano, S. J. Agric. Food Chem. 60, 8075–8082 (2012).

    Article  CAS  Google Scholar 

  30. Bar-Ness, E., Hadar, Y., Chen, Y., Römheld, V. & Marschner, H. Plant Physiol. 100, 451–456 (1992).

    Article  CAS  Google Scholar 

  31. Graziano, M., Beligni, M. V. & Lamattina, L. Plant Physiol. 130, 1852–1859 (2002).

    Article  CAS  Google Scholar 

  32. Gebhardt, P., Opfermann, T. & Saluz, H. P. Appl. Radiat. Isot. 68, 1057–1059 (2010).

    Article  CAS  Google Scholar 

  33. Wellburn, A. R. J. Plant Physiol. 144, 307–313 (1994).

    Article  CAS  Google Scholar 

Download references


We thank A. Perner for MS analyses and H. Heinecke for NMR measurements. We thank D. Milea for helpful discussion on thermodynamic data and M. Frontauria for potentiometric titrations. We thank the Deutsche Forschungsgemeinschaft for financial support (SFB 1127, ChemBioSys, and Leibniz Award to C.H.).

Author information

Authors and Affiliations



R.H., K.I. and C.H. designed experiments; R.H. conducted cultivation, isolation and structure elucidation experiments, synthesized reference compounds and performed all experiments involving corn plants. K.I. performed genetic experiments; R.H. and K.I. performed bioinformatic analyses and analyzed data. R.H. and M.P.-L. prepared radioisotope complexes. B.H. designed and performed PET–CT experiments and analyzed resulting data. W.P. and S.G. designed thermodynamic studies, R.H. and S.G. performed titrations and S.G. calculated physicochemical constants. J.F.M. performed AAS measurements. T.W. supervised, organized and discussed results concerning iron quantification using AAS. H.-P.S. supervised, organized and discussed results concerning radiochemistry and PET–CT imaging. R.H. and C.H. wrote the manuscript.

Corresponding author

Correspondence to Christian Hertweck.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Text and Figures

Supplementary Tables 1–6, Supplementary Figures 1–14

Reporting Summary

Supplementary Note 1

Synthetic Procedures

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hermenau, R., Ishida, K., Gama, S. et al. Gramibactin is a bacterial siderophore with a diazeniumdiolate ligand system. Nat Chem Biol 14, 841–843 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing