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Critical thresholds of 1-Octen-3-ol shape inter-species Aspergillus interactions modulating the growth and secondary metabolism.

ABSTRACT: In fungi, contactless interactions are mediated via the exchange of volatile organic compounds (VOCs). As these pair-wise interactions are fundamental to complex ecosystem, we examined the effects of inter-species VOCs trade-offs in Aspergillus flavus development. First, we exposed A. flavus to the A. oryzae volatilome (Treatment-1) with highest relative abundance of 1-Octen-3-ol (~ 4.53 folds) among the C-8 VOCs. Further, we examined the effects of gradient titers of 1-Octen-3-ol (Treatment-2: 100-400 ppm/day) in a range that elicits natural interactions. On 7-day, VOC-treated A. flavus displayed significantly reduced growth and sclerotial counts (p < 0.01) coupled with higher conidial density (T2_{100-200 ppm/day}, p < 0.01) and α-amylase secretion (T2_200 ppm/day, p < 0.01), compared to the untreated sets. Similar phenotypic trends except for α-amylases were evident for 9-day incubated A. flavus in T2. The corresponding metabolomics data displayed a clustered pattern of secondary metabolite profiles for VOC-treated A. flavus (PC1-18.03%; PC2-10.67%). Notably, a higher relative abundance of aflatoxin B1 with lower levels of most anthraquinones, indole-terpenoids, and oxylipins was evident in VOC-treated A. flavus. The observed correlations among the VOC-treatments, phenotypes, and altered metabolomes altogether suggest that the distant exposure to the gradient titers of 1-Octen-3-ol elicits an attenuated developmental response in A. flavus characterized by heightened virulence.

SUBMITTER: Singh D

PROVIDER: S-EPMC7338521 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Critical thresholds of 1-Octen-3-ol shape inter-species Aspergillus interactions modulating the growth and secondary metabolism.

Singh Digar D Son Su Young SY Lee Choong Hwan CH

Scientific reports 20200706 1

In fungi, contactless interactions are mediated via the exchange of volatile organic compounds (VOCs). As these pair-wise interactions are fundamental to complex ecosystem, we examined the effects of inter-species VOCs trade-offs in Aspergillus flavus development. First, we exposed A. flavus to the A. oryzae volatilome (Treatment-1) with highest relative abundance of 1-Octen-3-ol (~ 4.53 folds) among the C-8 VOCs. Further, we examined the effects of gradient titers of 1-Octen-3-ol (Treatment-2: ...[more]

PMID: 32632328

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Project description:The filamentous fungus Aspergillus nidulans has been a primary workhorse used to understand fungal genetics. Much of this work has focused on elucidating the genetics of biosynthetic gene clusters (BGCs) and the secondary metabolites (SMs) they produce. SMs are both niche defining in fungi and of great economic importance to humans. Despite the focus on A. nidulans, very little is known about the natural diversity in secondary metabolism within this species. We determined the BGC content and looked for evolutionary patterns in BGCs from whole-genome sequences of two clinical isolates and the A4 reference genome of A. nidulans Differences in BGC content were used to explain SM profiles determined using liquid chromatography-high-resolution mass spectrometry. We found that in addition to genetic variation of BGCs contained by all isolates, nine BGCs varied by presence/absence. We discovered the viridicatumtoxin BGC in A. nidulans and suggest that this BGC has undergone a horizontal gene transfer from the Aspergillus section Nigri lineage into Penicillium sometime after the sections Nigri and Nidulantes diverged. We identified the production of viridicatumtoxin and several other compounds previously not known to be produced by A. nidulans One isolate showed a lack of sterigmatocystin production even though it contained an apparently intact sterigmatocystin BGC, raising questions about other genes and processes known to regulate this BGC. Altogether, our work uncovers a large degree of intraspecies diversity in BGC and SM production in this genetic model species and offers new avenues to understand the evolution and regulation of secondary metabolism.IMPORTANCE Much of what we know about the genetics underlying secondary metabolite (SM) production and the function of SMs in the model fungus Aspergillus nidulans comes from a single reference genome. A growing body of research indicates the importance of biosynthetic gene cluster (BGC) and SM diversity within a species. However, there is no information about the natural diversity of secondary metabolism in A. nidulans We discovered six novel clusters that contribute to the considerable variation in both BGC content and SM production within A. nidulans We characterize a diverse set of mutations and emphasize how findings of single nucleotide polymorphisms (SNPs), deletions, and differences in evolutionary history encompass much of the variation observed in nonmodel systems. Our results emphasize that A. nidulans may also be a strong model to use within-species diversity to elucidate regulatory cross talk, fungal ecology, and drug discovery systems.

Project description:Diverse expression patterns for secondary metabolism gene clusters from Aspergillus flavus under different environmental conditions and in genetic mutants: Insights into regulation of cyclopiazonic acid along with aflatoxin Species of Aspergillus produce a diverse array of secondary metabolites, and recent genomic analysis predicts that these species have the capacity to synthesize many more compounds. It has been possible to infer the presence of 55 gene clusters associated with secondary metabolism in A. flavus. Presumably, secondary metabolites play important roles in the ecology of the producing species, but functions for most secondary metabolites remain unknown. Only three metabolic pathways have been associated with the predicted clusters in A. flavus. These include aflatoxin, cyclopiazonic acid (CPA), and aflatrem. To gain insight into the regulation of, and infer ecological significance for the 55 secondary metabolite gene clusters predicted in A. flavus, we examined their expression over 28 diverse conditions. Variables included culture media and temperature, fungal development, colonization of developing maize seeds, and misexpression of laeA, the global regulator of secondary metabolism. Hierarchical clustering analysis of expression profiles allowed us to categorize the gene clusters into four distinct clades. Gene clusters for the production of aflatoxins, CPA, and seven other unknown compound(s) were identified as belonging to one clade. To further explore the relationships found by gene expression analysis, aflatoxin and CPA production were quantified under five different cell culture environments known to be conducive or non-conducive for aflatoxin biosynthesis and during colonization of developing maize seeds. Results from these studies showed that secondary metabolism gene clusters have distinctive gene expression profiles. Aflatoxin and CPA were found to have unique regulation but similar enough that they would be expected to co-occur in commodities colonized with A. flavus.

Dataset Information

Critical thresholds of 1-Octen-3-ol shape inter-species Aspergillus interactions modulating the growth and secondary metabolism.

Publications

Critical thresholds of 1-Octen-3-ol shape inter-species Aspergillus interactions modulating the growth and secondary metabolism.

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