Targeted induction of a silent fungal gene cluster encoding the bacteria-specific germination inhibitor fumigermin

Stroe, Maria C.; Netzker, Tina; Scherlach, Kirstin; Krüger, Thomas; Hertweck, Christian; Valiante, Vito; Brakhage, Axel A.

doi:10.7554/elife.52541

Cited by 59 publications

(80 citation statements)

References 71 publications

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“…The resultant compound was a potent fungal metabolite that in turn inhibited the spore-germination of S. rapamycinicus [38]. Therefore, the secondary metabolite gene clusters confer a competitive advantage to the fungi over the bacteria residing in the same environment.…”

Section: Discussionmentioning

confidence: 99%

A fungal member of theArabidopsis thalianaphyllosphere antagonizesAlbugo laibachiivia a secreted lysozyme

Eitzen

Sengupta

Kroll

et al. 2020

Preprint

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In natural habitats, plants are challenged by pathogenic organisms, while they are extensively colonized by microbes, which establish a network of interactions with the plant and amongst each other. Therefore, plant immunity might not only be shaped by the co-evolutionary arms race between plants and pathogens, but also be a result from interactions within the microbiota and the host. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii has been identified as main driver of the phyllosphere microbiota. In this study, we describe the epiphytic yeast Moesziomyces albugensis and its antagonistic role in the microbial phyllosphere of Arabidopsis thaliana. M. albugensis, a close relative to pathogenic smut fungi, antagonizes several leaf-colonizing microbes. In particular, it prevents infection of A. thaliana by A. laibachii. Combination of transcriptomics and reverse genetics identified a gene of M. albugensis encoding a GH25 hydrolase as major factor of this microbial antagonism. Findings in this study provide identify a potential factor of oomycete biocontrol, provide mechanistic insight in microbial antagonism shaping leaf microbiota and provide new insights in the evolution of epiphytic basidiomycete yeasts. Recent research has focused largely on the importance of rhizoshpere microbiota in nutrient acquisition, pathogenic protection, and boosting overall plant growth and development [1-3]. However, the above ground parts of the plant including the phyllosphere are colonized by diverse groups of microbes that assist in plant protection and immunity [4,5] . The environment has a greater impact on the microbial community on the leaf surface, ultimately influencing the host-microbe interactions [6]. Scale-free network analysis was performed with the leaf microbial population of Arabidopsis thaliana [7]. Majority of the interactions existing in the network were found to be negative, consistent with the fact that it is rather the antagonistic interactions that stabilizes a microbial community [8]. Phyllosphere network analysis 3 of A. thaliana revealed a small number of microbes as hub organisms that have severe effect on the community structure. The major hub microbe in the A. thaliana phyllosphere is the oomycete Albugo laibachii, which is a biotrophic pathogen of Arabidopsis. This pathogen has been shown to significantly reduce the bacterial diversity of epiphytic and endophytic leaf habitats. Since bacteria generally comprises a large proportion of the phyllosphere microbiome, [9]; phylogenetic profiling of A. thaliana was also directed towards identifying a small group of bacteria that frequently colonize A. thaliana leaves. The analysis helped to develop a synthetic community of bacteria for gnotobiotic experiments. Along with bacteria and oomycetes, a broad range of fungi are colonizers of the A. thaliana leaf. Among those fungi, basidiomycete yeasts are frequently found and the most frequent ones is the epiphytic basidiomycete genus Dioszegia, as well as an anamorphic yeast classifie...

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Section: Discussionmentioning

confidence: 99%

A fungal member of theArabidopsis thalianaphyllosphere antagonizesAlbugo laibachiivia a secreted lysozyme

Eitzen

Sengupta

Kroll

et al. 2020

Preprint

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“…In contrast, only 3 of 11 species-specific SM core genes had been characterized. The most recently identified gene, Afu1g01010 , is involved in fumigermin biosynthesis in strain ATCC 46645, but not in strain Af293 owing to multiple SNPs inside the ORF (13). On the basis of the results, we hypothesized that SC BGCs are transcriptionally more active and functional than species-specific BGCs, enabling us to easily access and preferentially characterize the metabolites derived from the SC BGCs under laboratory conditions.…”

Section: Discussionmentioning

confidence: 99%

“…This may occur because of the loss of transcriptional ability owing to the diversification of machinery regulating SM gene clusters. Although many researchers have attempted to verify this hypothesis (13,14,16,17), whether the SM gene clusters in their genomes are “alive” from an evolutionary perspective has been poorly studied.…”

Section: Introductionmentioning

confidence: 99%

Comparative genome and transcriptome analyses revealing interspecies variations in the expression of fungal biosynthetic gene clusters

Takahashi

Umemura

Shimizu

et al. 2020

Preprint

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33Filamentous fungi produce various bioactive compounds that are biosynthesized by a 34 set of proteins encoded in biosynthetic gene clusters (BGCs). For an unknown reason, 35 large parts of the BGCs are transcriptionally silent under laboratory conditions, which 36 has hampered the discovery of novel fungal compounds. The transcriptional regulation 37 of fungal secondary metabolism is not fully understood from an evolutionary viewpoint. 38To address this issue, we conducted comparative genomic and transcriptomic analyses 39 using five closely related species of the Aspergillus section Fumigati: Aspergillus 40 fumigatus, Aspergillus lentulus, Aspergillus udagawae, Aspergillus pseudoviridinutans, 41and Neosartorya fischeri. From their genomes, 298 secondary metabolite (SM) core 42 genes were identified, with 27.4% to 41.5% being unique to a species. Compared with 43 the species-specific genes, a set of section-conserved SM core genes was expressed 44 at a higher rate and greater magnitude, suggesting that their expression tendency is 45 correlated with the BGC distribution pattern. However, the section-conserved BGCs 46 showed diverse expression patterns across the Fumigati species. Thus, not all common 47BGCs across species appear to be regulated in an identical manner. A consensus motif 48 was sought in the promoter region of each gene in the 15 section-conserved BGCs 49 among the Fumigati species. A conserved motif was detected in only two BGCs including 50 the gli cluster. The comparative transcriptomic and in silico analyses provided insights 51 into how the fungal SM gene cluster diversified at a transcriptional level, in addition to 52 genomic rearrangements and cluster gains and losses. This information increases our 53 understanding of the evolutionary processes associated with fungal secondary 54 metabolism. 55 56 KEY WORDS: comparative genomics, comparative transcriptomics, secondary 57 metabolism, biosynthetic gene cluster, Aspergillus 58 59 Author summary 61 Filamentous fungi provide a wide variety of bioactive compounds that contribute to public 62 health. The ability of filamentous fungi to produce bioactive compounds has been 63 underestimated, and fungal resources can be developed into new drugs. However, most 64 biosynthetic genes encoding bioactive compounds are not expressed under laboratory 65 conditions, which hampers the use of fungi in drug discovery. The mechanisms 66 underlying silent metabolite production are poorly understood. Here, we attempted to 67 show the diversity in fungal transcriptional regulation from an evolutionary viewpoint. To 68 meet this goal, the secondary metabolisms, at genomic and transcriptomic levels, of the 69 most phylogenetically closely related species in Aspergillus section Fumigati were 70 compared. The conserved biosynthetic gene clusters across five Aspergillus species 71were identified. The expression levels of the well-conserved gene clusters tended to be 72 more active than the species-specific, which were not well-conserved, gene clusters. 73Despite hig...

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“…A general mechanism for this purpose is the formation of volatile or diffusible toxins that include secondary metabolites (SMs) or peptides (Hiscox and Boddy, 2017). For example, the fumigermin produced by Aspergillus fumigatus (Eurotiales, Ascomycota) can inhibit the spore germination of actinobacterium Streptomyces rapamycinicus , conferring advantage for A. fumigatus to defend for environmental resources (Stroe et al ., 2020). Another mechanism is the involvement of the formation of reactive oxygen species (ROS).…”

Section: Introductionmentioning

confidence: 99%

Azaphilones biosynthesis complements the defence mechanism of Trichoderma guizhouense against oxidative stress

Pang

Sun

et al. 2020

Environmental Microbiology

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Summary Filamentous fungi are known as producers of a large array of diverse secondary metabolites (SMs) that aid in securing their environmental niche. Here, we demonstrated that the SMs have an additional role in fungal defence against other fungi: Trichoderma guizhouense, a mycoparasite, is able to antagonize Fusarium oxysporum f. sp. cubense race 4 (Foc4) by forming aerial hyphae that kill the host with hydrogen peroxide. At the same time, a gene cluster comprising two polyketide synthases is strongly expressed. Using functional genetics, we characterized this cluster and identified its products as azaphilones (termed as trigazaphilones). The trigazaphilones were found lacking of antifungal toxicity but exhibited high radical scavenging activities. The antioxidant property of trigazaphilones was in vivo functional under various tested conditions of oxidative stress. Thus, we conclude that the biosynthesis of trigazaphilones serves as a complementary antioxidant mechanism and defends T. guizhouense against the hydrogen peroxide that it produces to combat other fungi like Foc4.

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Targeted induction of a silent fungal gene cluster encoding the bacteria-specific germination inhibitor fumigermin

Cited by 59 publications

References 71 publications

A fungal member of theArabidopsis thalianaphyllosphere antagonizesAlbugo laibachiivia a secreted lysozyme

A fungal member of theArabidopsis thalianaphyllosphere antagonizesAlbugo laibachiivia a secreted lysozyme

Comparative genome and transcriptome analyses revealing interspecies variations in the expression of fungal biosynthetic gene clusters

Azaphilones biosynthesis complements the defence mechanism of Trichoderma guizhouense against oxidative stress

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