Inactivation of siderophore iron‐chelating moieties by the fungal wheat root symbiont Pyrenophora biseptata

Author:

French Katie S.1,Chukwuma Emmanuel2,Linshitz Ilan3,Namba Kosuke4,Duckworth Owen W.5,Cubeta Marc A.1,Baars Oliver12ORCID

Affiliation:

1. Department of Entomology and Plant Pathology North Carolina State University, Center for Integrated Fungal Research Raleigh North Carolina USA

2. Department of Chemistry North Carolina State University Raleigh North Carolina USA

3. Department of Biology University of Maryland College Park Maryland USA

4. Department of Pharmaceutical Sciences Tokushima University Tokushima Japan

5. Department of Crop and Soil Sciences North Carolina State University Raleigh North Carolina USA

Abstract

AbstractWe investigated the ability of four plant and soil‐associated fungi to modify or degrade siderophore structures leading to reduced siderophore iron‐affinity in iron‐limited and iron‐replete cultures. Pyrenophora biseptata, a melanized fungus from wheat roots, was effective in inactivating siderophore iron‐chelating moieties. In the supernatant solution, the tris‐hydroxamate siderophore desferrioxamine B (DFOB) underwent a stepwise reduction of the three hydroxamate groups in DFOB to amides leading to a progressive loss in iron affinity. A mechanism is suggested based on the formation of transient ferrous iron followed by reduction of the siderophore hydroxamate groups during fungal high‐affinity reductive iron uptake. P. biseptata also produced its own tris‐hydroxamate siderophores (neocoprogen I and II, coprogen and dimerum acid) in iron‐limited media and we observed loss of hydroxamate chelating groups during incubation in a manner analogous to DFOB. A redox‐based reaction was also involved with the tris‐catecholate siderophore protochelin in which oxidation of the catechol groups to quinones was observed. The new siderophore inactivating activity of the wheat symbiont P. biseptata is potentially widespread among fungi with implications for the availability of iron to plants and the surrounding microbiome in siderophore‐rich environments.

Funder

Novo Nordisk Fonden

State of North Carolina

National Science Foundation

Publisher

Wiley

Subject

Agricultural and Biological Sciences (miscellaneous),Ecology, Evolution, Behavior and Systematics

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