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Cyclodepsipeptide Biosynthesis in Hypocreales Fungi and Sequence Divergence of The Non-Ribosomal Peptide Synthase Genes.

ABSTRACT: Fungi from the Hypocreales order synthesize a range of toxic non-ribosomal cyclic peptides with antimicrobial, insecticidal and cytotoxic activities. Entomopathogenic Beauveria, Isaria and Cordyceps as well as phytopathogenic Fusarium spp. are known producers of beauvericins (BEAs), beauvenniatins (BEAEs) or enniatins (ENNs). The compounds are synthesized by beauvericin/enniatin synthase (BEAS/ESYN1), which shows significant sequence divergence among Hypocreales members. We investigated ENN, BEA and BEAE production among entomopathogenic (Beauveria, Cordyceps, Isaria) and phytopathogenic (Fusarium) fungi; BEA and ENNs were quantified using an LC-MS/MS method. Phylogenetic analysis of partial sequences of putative BEAS/ESYN1 amplicons was also made. Nineteen fungal strains were identified based on sequence analysis of amplified ITS and tef-1? regions. BEA was produced by all investigated fungi, with F. proliferatum and F. concentricum being the most efficient producers. ENNs were synthesized mostly by F. acuminatum, F. avenaceum and C. confragosa. The phylogeny reconstruction suggests that ancestral BEA biosynthesis independently diverged into biosynthesis of other compounds. The divergent positioning of three Fusarium isolates raises the possibility of parallel acquisition of cyclic depsipeptide synthases in ancient complexes within Fusarium genus. Different fungi have independently evolved NRPS genes involved in depsipeptide biosynthesis, with functional adaptation towards biosynthesis of overlapping yet diversified metabolite profiles.

SUBMITTER: Urbaniak M

PROVIDER: S-EPMC7400199 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Publications

Cyclodepsipeptide Biosynthesis in Hypocreales Fungi and Sequence Divergence of The Non-Ribosomal Peptide Synthase Genes.

Urbaniak Monika M Waśkiewicz Agnieszka A Trzebny Artur A Koczyk Grzegorz G Stępień Łukasz Ł

Pathogens (Basel, Switzerland) 20200709 7

Fungi from the Hypocreales order synthesize a range of toxic non-ribosomal cyclic peptides with antimicrobial, insecticidal and cytotoxic activities. Entomopathogenic Beauveria, Isaria and Cordyceps as well as phytopathogenic Fusarium spp. are known producers of beauvericins (BEAs), beauvenniatins (BEAEs) or enniatins (ENNs). The compounds are synthesized by beauvericin/enniatin synthase (BEAS/ESYN1), which shows significant sequence divergence among Hypocre ...[more]

PMID: 32660015

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Project description:BACKGROUND: Horizontal gene transfer, also called lateral gene transfer, frequently occurs among prokaryotic organisms, and is considered an important force in their evolution. However, there are relatively few reports of transfer to or from fungi, with some notable exceptions in the acquisition of prokaryotic genes. Some fungal species have been found to contain sequences resembling those of bacterial genes, and with such sequences absent in other fungal species, this has been interpreted as horizontal gene transfer. Similarly, a few fungi have been found to contain genes absent in close relatives but present in more distantly related taxa, and horizontal gene transfer has been invoked as a parsimonious explanation. There is a paucity of direct experimental evidence demonstrating the occurrence of horizontal gene transfer in fungi. RESULTS: We found a fungal field isolate from rice (Oryzae sativa) that contains ribosomal DNA sequences from two species of fungal rice pathogens (Thanatephorus cucumeris and Ceratobasidium oryzae-sativae). This field isolate has four types of ribosomal DNA internal transcribed spacers (ITS), namely pure ITS of C. oryzae-sativae, which was dominant in this field isolate, pure ITS of T. cucumeris, and two chimeric ITS, with ITS1 derived from C. oryzae-sativae and ITS2 from T. cucumeris, or ITS1 from T. cucumeris and ITS2 from C. oryzae-sativae. The presence of chimeric forms indicates that the intergeneric hybrid was not merely composed of nuclei from the parental species, but that nuclear fusion and crossing over had taken place. CONCLUSION: Hyphae of T. cucumeris and C. oryzae-sativae are vegetatively incompatible, and do not successfully anastomose. However, they parasitize the same host, and perhaps under the influence of host enzymes targeted to weaken pathogen cells or in dying host plant tissue, the fungal hyphae lost their integrity, and normal vegetative incompatibility mechanisms were overcome, allowing the hyphae to fuse. Based on the presence of other similarly anomalous isolates from the field, we speculate that these types of intergeneric hybridization events and occurrences of horizontal gene transfer may not be so rare in the field.

Dataset Information

Cyclodepsipeptide Biosynthesis in Hypocreales Fungi and Sequence Divergence of The Non-Ribosomal Peptide Synthase Genes.

Publications

Cyclodepsipeptide Biosynthesis in <i>Hypocreales</i> Fungi and Sequence Divergence of The <b>Non-Ribosomal Peptide Synthase Genes</b>.

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