Results 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.
Abstract
ABSTRACT 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. IMPORTANCE Deep-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. Deep-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.
Virulence factor genes (VFGs) in soil microbiomes pose potential health risks, yet how environmental stressors drive their enrichment remains poorly understood. We integrated metagenomic and metatranscriptomic analyses with a time series microcosm experiment (6 h to 60 days) to investigate VFG responses to arsenic (As) stress in paddy soils. High-As stress (150 mg kg–1) reduced overall microbial alpha diversity at the DNA level but paradoxically drove co-occurrence networks of potential pathogens toward a highly interconnected architecture dominated by positive associations (98.50%), with global transitivity increasing to 0.874. This restructuring was accompanied by significant enrichment of VFGs, particularly those involved in adherence, motility, and biofilm formation, with As(III) identified as the primary driver of VFG expression. VFGs showed strong transcriptional coupling with mobile genetic elements, and 35 high-quality metagenome-assembled genomes carrying VFG-MGE pairs provided direct genomic evidence of horizontal transfer potential. Notably, VFG upregulation reflected a community-level stress tolerance strategy rather than a direct shift toward pathogenicity, yet the unintended consequence was sustained time-dependent enrichment of opportunistic pathogens, including ESKAPE pathogens, with 53 potential pathogens transcriptionally active by day 60. Our findings establish that As-contaminated paddy soils serve as hidden reservoirs for VFGs and opportunistic pathogens, with implications for food safety and One Health risk assessment.
Zi-Teng Liu, Jia-qi Li, Xin-Di Zhao et al.· Environment & Health· 0 citations
Findings underscore a significant role for VdOMO in siderophore-associated iron acquisition, fungal development, stress adaptation, and the early stages of host colonization in V. dahliae.
Yusha Du, Lixinyu Sun, Kang-Wei Xie et al.· Frontiers in Plant Science· 0 citations
Oxidative stress poses significant challenges for fungi inhabiting extreme environments. Elevated salinity frequently induces the excessive production of reactive oxygen species (ROS), which can damage cellular components and impair growth. In response, fungi—common inhabitants of extreme environments—activate coordinated adaptive mechanisms, including antioxidant defense systems and other stress-related pathways. In the present study, a newly isolated strain, Trichoderma afroharzianum B2.2, obtained from the poorly studied saline habitat of Atanasovsko Lake (Bulgaria), was investigated. The cellular response of this moderately halotolerant strain to increased salinity was characterized. Biomarkers of oxidative stress were evaluated, and the involvement of key enzymes from glycolysis and the pentose phosphate pathway in the strain’s adaptation to elevated salinity was examined. Understanding adaptations to salt environments is crucial not only for elucidating fungal survival mechanisms under extreme conditions but also for their potential applications in biotechnology, ecology, and food safety, particularly in the context of increasing ecosystem salinization and climate change.
L. Yovchevska, G. Stoyancheva, V. Dishliyska et al.· Stresses· 0 citations
Fungi live in diverse environments requiring tolerance against abiotic and biotic stress and changing atmospheric conditions. Studies with white rot and brown rot species of Polyporales Basidiomycota have demonstrated that aerobic wood decay fungi may adapt to low oxygen and even anoxic conditions, which they undoubtedly encounter in their deadwood habitat. In the white rot fungus Phlebia radiata, oxygen depletion on lignocellulose substrates leads to hypoxia and fermentative metabolism. In this study, we elaborated the atmospheric effect further by subjecting the fungus to oxidative stress on wood substrate under aerobic and low oxygen conditions, with the aim to examine changes in gene expression and metabolic pathways as consequences of the oxidative treatment. Overall, 762 genes were significantly differentially expressed (DEGs with absolute Log2FoldChange > 1) 18 h after treatment with hydrogen peroxide according to RNA-Seq data. Half of these (348 genes) were downregulated in low oxygen (< 10% O2) cultures, with 185 genes unique to the condition but one third (121 genes) of unknown function. In aerobic cultures, a different response was observed with less DEGs showing downregulation (236 genes) while a higher number were upregulated (267 genes) and 153 of the upregulated genes were unique to the condition. Among DEGs upregulated under both conditions, small secreted proteins (SSPs) were the most abundant, followed by short-chain dehydrogenase/reductases, aldo-keto reductases, GNAT family acetyltransferases and CAZy carbohydrate active enzymes. Among downregulated DEGs, numerous SSP and CAZy classes, and genes encoding heat-shock proteins and MFS transporters were identified. Closer examination of carbon metabolism genes showed that under both conditions, oxidative treatment led to suppression of pentose catabolic pathway, glycerol metabolism, and formation of ethanol and acetate. Oxidative stress caused a substantial change in fungal gene expression, but with different responses depending on the culture atmosphere. This may be explained by contrasting fungal metabolic states before the shock as was observed in extracellular enzyme, aromatic metabolite and redox activity profiles. Surprisingly, oxidative shock caused downregulation of a few heat-shock proteins whereas small secreted proteins were either up- or downregulated, suggesting both sensing and regulative roles for these, functionally yet unknown, diverse fungal proteins.
Janina Österman-Udd, Eero A. Kiviniemi, A. Simojoki et al.· Fungal Biology and Biotechno...· 0 citations
Transcriptional analysis revealed that compared to neutral conditions, osmotic stress-related genes were significantly upregulated in the ΔliaS strain under acidic conditions, indicating that LiaS modulates acid tolerance through transcriptional regulation.
Yong-Shu Wu, Jiali Xu, Yifan Wang et al.· Virulence· 0 citations
The biology of the pathogenic fungus Aspergillus fumigatus remains largely unexplored, in part due to the large number of hypothetical and uncharacterized proteins. In this study, we focused on the protein encoded by the Afu4g10610 gene, which is consistently up-regulated across multiple stress-related transcriptomic datasets, including both in vitro and in vivo infection models. Functional characterization through the generation of mutant strains revealed that deletion of Afu4g10610 compromises the response to cell wall stress induced by Congo Red and Calcofluor White, correlating with the downregulation of key cell wall integrity (CWI) pathway sensors (wsc1 and midA). In addition, the mutant exhibits enhanced resistance to osmotic stress, consistent with altered expression of the high-osmolarity glycerol (HOG) pathway effectors mpkC and sakA. The deletion mutant also showed a moderate reduction in cytotoxicity toward A549 epithelial cells and altered TNF production in RAW 264.7 macrophages, whereas the overexpression strain exhibited a significant decrease in TNF levels. GRAsp analysis predicted this gene to be associated with the phenylalanine/tyrosine catabolic pathway. Accordingly, pyomelanin production and related metabolites were analyzed. Moreover, double deletion mutants ∆maiA ∆10610 and ∆hmgA led to a marked reduction in pyomelanin production, accompanied by altered tyrosine consumption and homogentisic acid (HGA) production. Since pyomelanin biosynthesis depends on the conversion of HGA into benzoquinone acetate (BQA), a step traditionally considered spontaneous, we investigated the potential interaction between Afu4g10610 and HGA. Molecular docking analysis supported the binding of HGA at the predicted dimer interface of the protein and suggested potential binding of FADH₂ to the protein, as an electron donor. Together, these findings identify Afu4g10610 as a stress-associated protein that contributes to cell wall and osmotic stress adaptation and suggest a potential contribution to HGA-to-BQA conversion during pyomelanin biosynthesis. More broadly, our results support the possible involvement of an enzymatic component in a step previously considered spontaneous in A. fumigatus.
Eduardo Pelegri-Martinez, U. Perez-Cuesta, Saioa Cendon-Sanchez et al.· Frontiers in Microbiology· 0 citations
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