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Published on: February 9, 2019
Differential Biosynthesis and Roles of Two Ferrichrome-Type Siderophores, ASP2397/AS2488053 and Ferricrocin, in
Yoshiki Asai1, Tomoshige Hiratsuka1,2, Miyu Ueda1
1Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan.
Abstract:
Ferrichromes are a family of fungal siderophores with cyclic hexapeptide structures. Most fungi produce one or two ferrichrome-type siderophores. Acremonium persicinum MF-347833 produces ferrichrome-like potent Trojan horse antifungal antibiotics ASP2397 and AS2488053, the aluminum- and iron-chelating forms of AS2488059, respectively. Here, we show by gene sequencing followed by gene deletion experiments that A. persicinum MF-347833 possesses two nonribosomal peptide synthetase genes responsible for AS2488059 and ferricrocin assembly. AS2488059 was produced under iron starvation conditions and excreted into the media to serve as a defense metabolite and probably an iron courier. In contrast, ferricrocin was produced under iron-replete conditions and retained inside the cells, likely serving as an iron-sequestering molecule. Notably, the phylogenetic analyses suggest the different evolutionary origin of AS2488059 from that of conventional ferrichrome-type siderophores. Harnessing two ferrichrome-type siderophores with distinct biological properties may give A. persicinum a competitive advantage for surviving the natural environment.
Insights
Acremonium persicinum produces two distinct siderophores, AS2488059 and ferricrocin, using separate gene pathways. These compounds have different roles in iron management and cellular defense, suggesting unique evolutionary origins and survival advantages.
Area of Science:
- Mycology
- Biochemistry
- Evolutionary Biology
Background:
- Ferrichromes are cyclic hexapeptide siderophores produced by fungi for iron acquisition.
- Most fungi synthesize one or two types of ferrichrome siderophores.
- Acremonium persicinum produces unique antifungal compounds, ASP2397 and AS2488053, related to siderophores.
Purpose of the Study:
- To identify the genes responsible for the synthesis of siderophores AS2488059 and ferricrocin in Acremonium persicinum.
- To elucidate the distinct biological roles and regulation of these two siderophores.
- To investigate the evolutionary relationship of AS2488059 with conventional ferrichromes.
Main Methods:
- Gene sequencing to identify nonribosomal peptide synthetase (NRPS) genes.
- Gene deletion experiments to confirm gene function in siderophore production.
- Analysis of siderophore production under different iron conditions (starvation vs. replete).
- Phylogenetic analysis to determine evolutionary origins.
Main Results:
- Two nonribosomal peptide synthetase genes in A. persicinum were identified as responsible for AS2488059 and ferricrocin synthesis.
- AS2488059 is produced under iron starvation, excreted, and functions as a defense metabolite and iron courier.
- Ferricrocin is produced under iron-replete conditions, retained intracellularly, and acts as an iron-sequestering molecule.
- Phylogenetic analysis indicates AS2488059 has a distinct evolutionary origin compared to typical ferrichromes.
Conclusions:
- Acremonium persicinum utilizes two distinct gene clusters for the production of siderophores with contrasting functions.
- The differential production and localization of AS2488059 and ferricrocin highlight their specialized roles in iron homeostasis and cellular defense.
- The unique evolutionary trajectory of AS2488059 suggests adaptive radiation within fungal siderophore biosynthesis.
- The ability to produce and utilize two distinct ferrichrome-type siderophores may confer a significant survival advantage to A. persicinum in diverse environmental conditions.
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