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. 2020 Feb 22;18(2):128.
doi: 10.3390/md18020128.

Mining the Metabolome and the Agricultural and Pharmaceutical Potential of Sea Foam-Derived Fungi

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Free PMC article

Mining the Metabolome and the Agricultural and Pharmaceutical Potential of Sea Foam-Derived Fungi

Ernest Oppong-Danquah et al. Mar Drugs. .
Free PMC article

Abstract

Sea foam harbors a diverse range of fungal spores with biological and ecological relevance in marine environments. Fungi are known as the producers of secondary metabolites that are used in health and agricultural sectors, however the potentials of sea foam-derived fungi have remained unexplored. In this study, organic extracts of six foam-derived fungal isolates belonging to the genera Penicillium, Cladosporium, Emericellopsis and Plectosphaerella were investigated for their antimicrobial activity against plant and human pathogens and anticancer activity. In parallel, an untargeted metabolomics study using UPLC-QToF-MS/MS-based molecular networking (MN) was performed to unlock their chemical inventory. Penicillium strains were identified as the most prolific producers of compounds with an average of 165 parent ions per strain. In total, 49 known mycotoxins and functional metabolites were annotated to specific and ubiquitous parent ions, revealing considerable chemical diversity. This allowed the identification of putative new derivatives, such as a new analog of the antimicrobial tetrapeptide, fungisporin. Regarding bioactivity, the Penicillium sp. isolate 31.68F1B showed a strong and broad-spectrum activity against seven plant and human pathogens, with the phytopathogen Magnaporthe oryzae and the human pathogen Candida albicans being the most susceptible (IC50 values 2.2 and 6.3 µg/mL, respectively). This is the first study mining the metabolome of the sea foam-derived fungi by MS/MS-based molecular networking, and assessing their biological activities against phytopathogens.

Keywords: antimicrobial activity; marine fungi; metabolomics; molecular network; phytopathogen; sea foam.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Principal component analysis (PCA) scores plot of all six fungal extracts showing discrimination in chemical diversity.
Figure 2
Figure 2
(A) PCA scores plot of the three Penicillium strains (B) PCA loadings plot showing regions (blue: isolate 36.97F1C; orange: isolate 62.72F1A and grey: isolate 31.68F1B) of highly specific features among the Penicillium strains. Three metabolites each, contributing to the discrimination (displayed m/z values) of the three Penicillium strains, are highlighted in the PCA loadings plot and listed in Table 2 as examples. All other discriminatory metabolites annotated are shown in Table S2.
Figure 3
Figure 3
(A) Molecular network (MN) of extracts from three Penicillium strains. Annotated compounds are displayed in Table S2. Nodes represent parent ions detected in the crude extracts of the fungi. Nodes that are highlighted in boxes, also named in the rectangles close to them, indicate representatives of that compound molecular family (B) Venn diagram displaying specific and shared parent ions detected in the culture extracts of three Penicillium strains.
Figure 4
Figure 4
Cyclic tetrapeptides undergo random ring opening at each amide bond to yield linear peptides which fragment to yield nondirect sequence (NDS) ions and direct sequence (DS) ions. The first two fragments from each ring opening point (1, 2, 3 and 4) are annotated, and the sequence of the cyclo-tetrapeptide is consequently predicted. (A) MS/MS spectrum of node m/z 493.2730 annotated as fungisporin. (B) Annotated MS/MS spectrum of the putative new analog of fungisporin m/z 525.2654. V, valine; F, phenylalanine; Y, tyrosine; Y’, putatively identified as N-hydroxyl-tyrosine (as shown in Figure 5B) or β-hydroxyl-tyrosine.
Figure 5
Figure 5
(A) MN of Cladosporium sp. and Emericellopsis sp. highlighting annotated parent ions. Nodes highlighted in boxes, also named in the rectangles close to them, indicate representatives of that compound molecular family (B) Euler diagram generated from the MN showing strain specific ions and shared ions between the two strains.
Figure 6
Figure 6
MN of Plectosphaerella sp. highlighting annotated parent ions. Nodes highlighted in boxes, also named in the rectangles close to them, indicate representatives of that compound MF.

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