Skip to main content

Thank you for visiting nature.com. 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.

  • Article
  • Published:

Structure elucidation and biosynthetic locus of trinickiabactin from the plant pathogenic bacterium Trinickia caryophylli

The Journal of Antibiotics volume 73, pages 28–34 (2020)Cite this article

Subjects

Abstract

Within the framework of our effort to discover new bioactive metabolites from Gram-negative bacteria, trinickiabactin (1) was isolated from the plant pathogenic strain Trinickia caryophylli DSM 50341. Whole genome sequencing allowed the identification of its biosynthetic gene cluster. The structure of 1 bears a rare diazeniumdiolate ligand system and was elucidated by a combination of NMR- and MS-spectroscopic techniques and bioinformatics. Trinickiabactin was found to be antibacterial toward several Gram-negative bacteria (MIC values ranged from 3.5 to 34.0 µg ml−1).

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Yabuuchi E, Kosako Y, Oyaizu H, Yanu I, Hotta H, Hashimoto Y, et al. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol. 1992;36:1251–75.

    Article  CAS  Google Scholar 

  2. Eberl L, Vandamme P. Members of the genus Burkholderia: good and bad guys. F1000Research. 2016;5:1007.

    Article  Google Scholar 

  3. Kunakom S, Eustáquio AS. Burkholderia as a source of natural products. J Nat Prod. 2019;82:2018–37.

    Article  CAS  Google Scholar 

  4. Liu X, Cheng Y-Q. Genome-guided discovery of diverse natural products from Burkholderia sp. J Ind Microbiol Biotechnol. 2014;41:275–84.

    Article  CAS  Google Scholar 

  5. Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M, Deravel J, et al. Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. MicrobiologyOpen. 2016;5:512–26.

    Article  CAS  Google Scholar 

  6. Cimermancic P, Medema MH, Claesen J, Kurita K, Brown LCW, Mavrommatis K, et al. Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell. 2014;158:412–21.

    Article  CAS  Google Scholar 

  7. Minowa Y, Araki M, Kanehisa M. Comprehensive analysis of distinctive polyketide and nonribosomal peptide structural motifs encoded in microbial genomes. J Mol Biol. 2007;368:1500–17.

    Article  CAS  Google Scholar 

  8. Beukes CW, Palmer M, Manyaka P, Chan WY, Avontuur JR, van Zyl E, et al. Genome data provides high support for generic boundaries in Burkholderia sensu lato. Front Microbiol. 2017;8:1154.

    Article  Google Scholar 

  9. Estrada-de los Santos P, Palmer M, Chávez-Ramirez B, Beukes C, Steenkamp ET, Briscoe L, et al. Whole genome analyses suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazothrophy and nodulation in the Burkholderiaceae. Genes. 2018;9:389.

    Article  Google Scholar 

  10. Mathew A, Jenul C, Carlier AL & Eberl L. The role of siderophores in metal homeostasis of members of the genus Burkholderia. Environ Microbiol Rep. 2016;8:103–9.

  11. Stephan H, Freund S, Meyer J-M, Winkelmann G, Jung G. Structure elucidation of the gallium-ornbactin complex by 2D NMR spectroscopy. Liebigs Ann Chem. 1993;1993:43–8.

    Article  Google Scholar 

  12. Coulon PML, Groleau M-C, Déziel E. Potential of the Burkholderia cepacia complex to produce 4-hydroxy-3-methyl-2-alkyquinolines. Front Cell Infect Microbiol. 2019;9:33.

    Article  Google Scholar 

  13. Dose B, Niehs SP, Scherlach K, Flórez LV Kaltenpoth M & Hertweck C. Unexpected bacterial origin of the antibiotic icosalide: two-tailed depsipeptide assembly in multifarious Burkholderia symbionts. ACS Chem Biol. 2018;13:2412–20.

  14. Barbeau K, Rue EL, Trick CG, Bruland KT, Butler A. Photochemical reactivity of siderophores produced by the marine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding group. Limnol Oceanogr. 2003;48:1069–78.

    Article  CAS  Google Scholar 

  15. Emery T. Exchange of iron by gallium in siderophores. Biochem. 1986;25:4629–33.

    Article  CAS  Google Scholar 

  16. Hermenau R, Ishida K, Gama S, Hoffmann B, Pfeifer-Leeg M, Plass W, et al. Gramibactin is a bacterial siderophore with a diazeniumdiolate ligand system. Nat Chem Biol. 2018;14:841–3.

    Article  CAS  Google Scholar 

  17. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 2019;47:W81–7.

    Article  Google Scholar 

  18. Skinnider MA, Merwin NJ, Johnston CW, Magarvey NA. PRISM: expanded prediction of natural product chemical structures from microbial genomes. Nucleic Acids Res. 2017;45:W49–54.

    Article  CAS  Google Scholar 

  19. Drake EJ, Gulick AM. Structural characterization and high-throughput screening of inhibitors of PvdQ, an NTN hydrolase involved in pyoverdine synthesis. ACS Chem Biol. 2011;6:1277–86.

    Article  CAS  Google Scholar 

  20. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24.

    Article  CAS  Google Scholar 

  21. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Determinantion of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. EUCAST discussion document E. dis 5.1. Clin Microbiol Infect. 2003;9: ix–xv. https://doi.org/10.1046/j.1469-0691.2003.00790.x.

  22. Lepe JA, Domínguez-Herrera J, Pachón J, Aznar J. 2013. Determining accurate vancomycin MIC values for methicillin-resistant Staphylococcus aureus by the microdilution method. J Antimicrob Chemother. 2013;69:1360–80.

    Google Scholar 

Download references

Acknowledgements

JJ and AF gratefully acknowledge the China Scholarship Council (CSC) and the Program for Research and Innovation in Science and Technology (RISET-Pro)/World Bank Loan No. 8245 for a granted Ph.D. scholarship, respectively. Furthermore, we would like to thank Dr. D. Wistuba and her team (Mass Spectrometry Department, Institute for Organic Chemistry, University of Tübingen) for HR-MS measurements and Dr. A. Luqman (Department of Microbial Genetics, IMIT, University of Tübingen) for technical assistance on recording optical density.

Author information

Authors and Affiliations

  1. Pharmaceutical Institute, Department of Pharmaceutical Biology, University of Tübingen, Tübingen, Germany

    Junjing Jiao, Jiayi Du, Andri Frediansyah, Ghazaleh Jahanshah & Harald Gross

  2. Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Sciences (LIPI), Wonosari, 55861, Indonesia

    Andri Frediansyah

Authors
  1. Junjing Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiayi Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andri Frediansyah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ghazaleh Jahanshah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harald Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harald Gross.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

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

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiao, J., Du, J., Frediansyah, A. et al. Structure elucidation and biosynthetic locus of trinickiabactin from the plant pathogenic bacterium Trinickia caryophylli. J Antibiot 73, 28–34 (2020). https://doi.org/10.1038/s41429-019-0246-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-019-0246-0

This article is cited by

Search

Advanced search

Quick links