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Published on: February 22, 2017
Virulensome: a transient organelle mediating fungal virulence
Pei-Ji Zhao1, Qian-Yi Hu1, Si-Han Wang1
1State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Key Laboratory of Basic Research and Innovative Application for Green Biological Production, Yunnan University, Kunming, 650091, China.
Abstract:
Fungal pathogens utilize specialized cellular systems to overcome host defenses, yet no dedicated pathogenic organelles have been previously defined in fungi. Here, we describe a transient, membrane-bound vesicle (100-250 nm in diameter) that forms specifically within the infection structures of a nematode-trapping fungus Dactylellina haptotyla, which we term the virulensome. Density-gradient isolation yielded virulensome-enriched fractions that killed 81.6% of Caenorhabditis elegans larvae within 24 h and perforated the nematode cuticle. Quantitative proteomics revealed 486 core components, including 31 peptidases and 23 glycoside hydrolases. Knockout of each of three representative proteins-an α-mannosidase (DHGH1), a metalloendopeptidase (DHMEPE1), and a WSC-domain protein-reduced virulensome abundance by up to 80% and lowered nematode mortality by 4-fold. Conversely, recombinant DHGH1 or DHMEPE1 killed >90% of nematodes in vitro. Live-cell super-resolution imaging showed virulensomes polarizing toward the host interface, disintegrating within infection bulbs, and releasing toxic effector cargos into the nematode body. These findings define the virulensome that packages and delivers destructive enzymes in a targeted manner, revealing a previously unrecognized mechanism of pathogenesis.
Insights
Fungal pathogens use a novel organelle, the virulensome, to deliver destructive enzymes. This membrane-bound vesicle targets nematode hosts, revealing a new mechanism of fungal pathogenesis.
Area of Science:
- Mycology
- Pathogen Biology
- Cell Biology
Background:
- Fungal pathogens employ sophisticated systems to breach host defenses.
- No dedicated pathogenic organelles have been identified in fungi to date.
Purpose of the Study:
- To identify and characterize novel pathogenic organelles in fungi.
- To elucidate the mechanism of pathogenesis in the nematode-trapping fungus *Dactylellina haptotyla*.
Main Methods:
- Density-gradient isolation of fungal vesicles.
- Quantitative proteomics to identify organelle components.
- Gene knockout studies and recombinant protein assays.
- Live-cell super-resolution imaging.
Main Results:
- A transient, membrane-bound vesicle, termed the virulensome, was identified in *D. haptotyla* infection structures.
- Virulensome-enriched fractions demonstrated high lethality against *Caenorhabditis elegans* larvae and cuticle perforation.
- Proteomics revealed 486 core components, including numerous peptidases and glycoside hydrolases.
- Knockout of key virulensome proteins significantly reduced organelle abundance and fungal virulence.
- Recombinant effector proteins showed potent nematode-killing activity in vitro.
- Live imaging demonstrated virulensome polarization, disintegration at the host interface, and targeted release of effectors.
Conclusions:
- The virulensome is a novel pathogenic organelle responsible for packaging and delivering destructive enzymes in fungi.
- This discovery reveals an unrecognized mechanism of fungal pathogenesis involving targeted enzyme delivery.
- The virulensome represents a potential target for novel antifungal strategies against nematode-trapping fungi.
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