Fruiting body-associated Pseudomonas contact triggers ROS-mediated perylenequinone biosynthesis in Shiraia mycelium culture

Summary

Scientists discovered that a beneficial bacteria living inside medicinal mushroom fruiting bodies can trigger the production of powerful healing compounds called perylenequinones. These compounds are used to treat various cancers and infections. The key finding is that the bacteria must make physical contact with the mushroom to activate this production through a process involving reactive oxygen species. By understanding this interaction, researchers developed a better way to grow these medicinal compounds in the laboratory.

Background

Perylenequinones (PQs) from Shiraia fruiting bodies are potent photosensitizers for anticancer and antimicrobial photodynamic therapy. Shiraia fruiting bodies harbor diverse endophytic bacterial communities, particularly Pseudomonas species, but their interactions with the host fungus and effects on secondary metabolism remain poorly understood.

Objective

This study investigated the interaction between Shiraia sp. S9 and endophytic Pseudomonas isolates to determine whether direct physical contact is necessary for eliciting fungal perylenequinone production and to elucidate the underlying molecular mechanisms.

Results

Direct physical contact with P. fulva SB1 at 400 cells/mL was essential for eliciting fungal PQ production and extracellular secretion, resulting in a total PQ yield of 362.2 mg/L (2.4-fold increase). RNA-seq identified 646 differentially expressed genes enriched in oxidative stress defense and carbohydrate metabolism. Bacterial contact induced ROS generation (O₂·⁻ and H₂O₂) that mediated increased membrane permeability and enhanced hypocrellin A production through upregulation of polyketide synthase and major facilitator superfamily transporter genes.

Conclusion

This work provides the first evidence that contact-dependent ROS signaling by endophytes regulates fungal secondary metabolism and perylenequinone biosynthesis. These findings establish an effective co-culture strategy for enhanced production of bioactive PQs and offer novel insights into bacterial-fungal interactions in fruiting bodies.
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