Deep-sea extreme environments harbor microorganisms with unique adaptive mechanisms. Fungi play significant ecological roles in these ecosystems, yet the regulatory pathways governing their adaptation to extreme conditions remain poorly understood. Here, we investigated the hadal-derived fungus Aspergillus sydowii DM1 as a model strain. Using CRISPR-Cas9 technology, we constructed a sho1 gene knockout mutant to examine its phenotypic and molecular responses to osmotic stress, oxidative stress, and high hydrostatic pressure (HHP). Our results showed that Sho1 contributed to cell wall integrity, was associated with changes in secondary metabolite profiles, and modulated the high-osmolarity glycerol (HOG) responses. Under osmotic stress, deletion of sho1 enhanced colony growth and conidiation under moderate-to-high salinity, and was accompanied by altered asexual developmental progression and HOG-associated gene expression. Under oxidative stress, loss of Sho1 led to increased reactive oxygen species (ROS) accumulation, and reduced spore viability. Under HHP, deletion of sho1 impaired early pressure-responsive signaling, increased ROS accumulation, and reduced spore germination during recovery. Comparative analysis of A. sydowii strains from different ecological niches further suggested that the deep-sea strain may possess a more coordinated pressure-response pattern associated with the Sho1-Hog1 pathway. Together, these findings indicate that Sho1 functions as an important upstream coordinator linking environmental sensing with osmotic adaptation, oxidative homeostasis, developmental regulation, and pressure-associated recovery in a hadal filamentous fungus, offering new insights into fungal signal transduction and adaptive evolution in extreme environments.IMPORTANCEDeep-sea fungi live under extreme conditions, yet the signaling mechanisms that help them survive remain poorly understood. Using a hadal isolate of Aspergillus sydowii, we show that the membrane sensor Sho1 contributes to fungal responses to osmotic stress, oxidative stress, and high hydrostatic pressure. Loss of sho1 altered growth, development, redox balance, and recovery after pressure exposure, indicating that this upstream signaling component coordinates multiple adaptive traits in a deep-sea fungus. These findings extend current knowledge of fungal stress signaling beyond model organisms and suggest that conserved signaling modules can be repurposed for life in the deep ocean. This study provides a useful genetic framework for understanding how fungi adapt to extreme marine environments.
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