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The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite.

ABSTRACT: Acquisition of genes by plastid genomes (plastomes) via horizontal gene transfer (HGT) seems to be a rare phenomenon. Here, we report an interesting case of HGT revealed by sequencing the plastomes of the eustigmatophyte algae Monodopsis sp. MarTras21 and Vischeria sp. CAUP Q 202. These plastomes proved to harbour a unique cluster of six genes, most probably acquired from a bacterium of the phylum Bacteroidetes, with homologues in various bacteria, typically organized in a conserved uncharacterized putative operon. Sequence analyses of the six proteins encoded by the operon yielded the following annotation for them: (i) a novel family without discernible homologues; (ii) a new family within the superfamily of metallo-dependent hydrolases; (iii) a novel subgroup of the UbiA superfamily of prenyl transferases; (iv) a new clade within the sugar phosphate cyclase superfamily; (v) a new family within the xylose isomerase-like superfamily; and (vi) a hydrolase for a phosphate moiety-containing substrate. We suggest that the operon encodes enzymes of a pathway synthesizing an isoprenoid-cyclitol-derived compound, possibly an antimicrobial or other protective substance. To the best of our knowledge, this is the first report of an expansion of the metabolic capacity of a plastid mediated by HGT into the plastid genome.

SUBMITTER: Yurchenko T

PROVIDER: S-EPMC5133447 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite.

Yurchenko Tatiana T Ševčíková Tereza T Strnad Hynek H Butenko Anzhelika A Eliáš Marek M

Open biology 20161101 11

Acquisition of genes by plastid genomes (plastomes) via horizontal gene transfer (HGT) seems to be a rare phenomenon. Here, we report an interesting case of HGT revealed by sequencing the plastomes of the eustigmatophyte algae Monodopsis sp. MarTras21 and Vischeria sp. CAUP Q 202. These plastomes proved to harbour a unique cluster of six genes, most probably acquired from a bacterium of the phylum Bacteroidetes, with homologues in various bacteria, typically organized in a conserved uncharacteri ...[more]

PMID: 27906133

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Project description:Fungal secondary metabolites with antibiotic activities can promote fungal adaptation to diverse environments. Besides the global regulator, individual biosynthetic gene clusters (BGCs) usually contain a pathway-specific transcription factor for the tight regulation of fungal secondary metabolism. Here, we report the chemical biology mediated by a supercluster containing three BGCs in the entomopathogenic fungus Metarhizium robertsii. These clusters are jointly controlled by an embedded transcription factor that orchestrates the collective production of four classes of chemicals: ustilaginoidin, indigotide, pseurotin, and hydroxyl-ovalicin. The ustilaginoidin BGC is implicated as a late-acquired cluster in Metarhizium to produce both the bis-naphtho-γ-pyrones and the monomeric naphtho-γ-pyrone glycosides (i.e., indigotides). We found that the biosynthesis of indigotides additionally requires the functions of paired methylglucosylation genes located outside the supercluster. The pseurotin/ovalicin BGCs are blended and mesosyntenically conserved to the intertwined pseurotin/fumagillin BGCs of Aspergillus fumigatus. However, the former have lost a few genes, including a polyketide synthase gene responsible for the production of a pentaene chain used for assembly with ovalicin to form fumagillin, as observed in A. fumigatus. The collective production of chemical cocktails by this supercluster was dispensable for fungal virulence against insects and could enable the fungus to combat different bacteria better than the metabolite(s) produced by an individual BGC could. Thus, our results unveil a novel strategy employed by fungi to manage chemical ecology against diverse bacteria. IMPORTANCE Fungal chemical ecology is largely mediated by the metabolite(s) produced by individual biosynthetic gene clusters (BGCs) with antibiotic activities. We report a supercluster containing three BGCs that are jointly controlled by an embedded master regulator in the insect pathogen Metarhizium robertsii. Four classes of chemicals, namely, ustilaginoidin, indigotide, pseurotin, and hydroxyl-ovalicin, are collectively produced by these three BGCs along with the contributions of tailoring enzyme genes located outside the supercluster. The production of these metabolites is not required for the fungal infection of insect hosts, but it benefits the fungus to combat diverse bacteria. The findings reveal and advocate a "the-more-the-better" strategy employed by fungi to manage effective adaptations to diverse environments.

Dataset Information

The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite.

Publications

The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite.

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