Abstract
Bacteria and fungi secrete many natural products that inhibit each other’s growth and development. The dynamic changes in secreted metabolites that occur during interactions between bacteria and fungi are complicated. Pyochelin is a siderophore produced by many Pseudomonas and Burkholderia species that induces systemic resistance in plants and has been identified as an antifungal agent. Through imaging mass spectrometry and metabolomics analysis, we found that Phellinus noxius, a plant pathogen, can modify pyochelin and ent-pyochelin to an esterification product, resulting in reduced iron-chelation and loss of antifungal activity. We also observed that dehydroergosterol peroxide, the fungal metabolite, is only accumulated in the presence of pyochelin produced through bacteria–fungi interactions. For the first time, we show the fungal transformation of pyochelin in the microbial interaction. Our findings highlight the importance of understanding the dynamic changes of metabolites in microbial interactions and their influences on microbial communities.
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8:15–25.
Weaver VB, Kolter R. Burkholderia spp. alter Pseudomonas aeruginosa physiology through iron sequestration. J Bacteriol. 2004;186:2376–84.
Linares JF, Gustafsson I, Baquero F, Martinez J. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA. 2006;103:19484–89.
Schiessl KT, Janssen EM-L, Kraemer SM, McNeill K, Ackermann M. Magnitude and mechanism of siderophore-mediated competition at low iron solubility in the Pseudomonas aeruginosa pyochelin system. Front Microbiol. 2017;8:1964.
Weller DM. Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 2007;97:250–56.
Ganeshan G, Manoj Kumar A. Pseudomonas fluorescens, a potential bacterial antagonist to control plant diseases. J Plant Interact. 2005;1:123–34.
Ho Y-N, Chiang H-M, Chao C-P, Su C-C, Hsu H-F, Guo C-T, et al. In planta biocontrol of soilborne Fusarium wilt of banana through a plant endophytic bacterium, Burkholderia cenocepacia 869T2. Plant Soil. 2015;387:295–306.
Ho Y-N, Huang C-C. Draft genome sequence of Burkholderia cenocepacia strain 869T2, a plant-beneficial endophytic bacterium. Genome Announc. 2015;3:e01327–15.
Sahashi N, Akiba M, Ishihara M, Ota Y, Kanzaki N. Brown root rot of trees caused by Phellinus noxius in the Ryukyu Islands, subtropical areas of Japan. Pathol. 2012;42:353–61.
Hoefler BC, Gorzelnik KV, Yang JY, Hendricks N, Dorrestein PC, Straight PD. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc Natl Acad Sci USA. 2012;109:13082–87.
Yang Y-L, Xu Y, Straight P, Dorrestein PC. Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol. 2009;5:885–87.
Ho YN, Shu LJ, Yang YL. Imaging mass spectrometry for metabolites: technical progress, multimodal imaging, and biological interactions. WIRES Syst Biol Med. 2017;9:e1387.
Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotech. 2016;34:828–37.
Cobessi D, Celia H, Pattus F. Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa. J Mol Biol. 2005;352:893–904.
Mislin GLA, Hoegy F, Cobessi D, Poole K, Rognan D, Schalk IJ. Binding related properties of pyochelin and structurally molecules to FptA of Pseudomonas aeruginosa. J Mol Biol. 2006;357:1437–48.
Youard ZA, Wenner N, Reimmann C. Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals. 2011;24:513–22.
Briard B, Mislin GL, Latgé J-P, Beauvais A. Interactions between Aspergillus fumigatus and pulmonary bacteria: current state of the field, new data, and future perspective. J Fungi. 2019;5:48.
Ponce MA, Ramirez JA, Galagovsky LR, Gros EG, Erra-Balsells R. A new look into the reaction between ergosterol and singlet oxygen in vitro. Photoch Photobio Sci. 2002;1:749–56.
Ong KS, Cheow YL, Lee SM. The role of reactive oxygen species in the antimicrobial activity of pyochelin. J Adv Res. 2017;8:393–98.
Ho Y-N, Lee H-J, Hsieh C-T, Peng C-C, Yang Y-L. Chemistry and biology of salicyl-capped siderophores. Stud Nat Prod Chem. 2018;59:431–90.
Acknowledgements
This research was supported by the Ministry of Science and Technology of Taiwan (MOST 104-2321-B-001-060-MY3). LC-MS data were collected in the Metabolomics Core Facility of the Instrument Center, Academia Sinica. NMR data were collected in the High Field Nuclear Magnetic Resonance Center, Academia Sinica. Burkholderia cenocepacia 869T2 was generously provided by Prof. Chieh-Chen Huang’s Lab (National Chung Hsing University, Taiwan) and Phellinus noxius strain 2252 by Prof. Chia-Lin Chung’s Lab (National Taiwan University, Taiwan). 9.11-Dehydroergosterol peroxide and ergosterol peroxide were kindly provided by Dr. Ming-Ren Cheng (Bioresource Collection and Research Center, Taiwan). The molecular docking analysis was supported by Dr. Ying-Ta Wu, Genomics Research Center, Academia Sinica.
Author information
Authors and Affiliations
Corresponding author
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
About this article
Cite this article
Ho, YN., Hoo, S.Y., Wang, BW. et al. Specific inactivation of an antifungal bacterial siderophore by a fungal plant pathogen. ISME J 15, 1858–1861 (2021). https://doi.org/10.1038/s41396-020-00871-0
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/s41396-020-00871-0
This article is cited by
-
Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor
The ISME Journal (2023)
-
Synergistic antagonism mechanism of Bacillus-Pseudomonas consortium against Alternaria solani
European Journal of Plant Pathology (2023)
-
Bacterial-fungal interactions under agricultural settings: from physical to chemical interactions
Stress Biology (2022)
