Liu Xinyao, Tao Yiran, Zhang Linwan, Liu Yuzhou, Shi Dongmei, Wang Jiao, Xue Peng, Xu Bin, Fang Wenjie, Ran Yuping
Laboratory of Pathogen Research, West China Hospital, Sichuan University, Chengdu, China; Department of Dermatovenereology, West China Hospital, Sichuan University, Chengdu, China.
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.
Redox Biol. 2025 Jun 14;85:103708. doi: 10.1016/j.redox.2025.103708.
Candida auris is a fungal pathogen with frequent development of multidrug-resistance or pan-drug resistance. Currently, the treatment options for Candida auris are limited. Therefore, there is an urgent need for alternative therapeutic strategies. Antimicrobial photodynamic therapy (aPDT), which generates reactive oxygen species (ROS) through light-activated photosensitizers, has shown promise against C. auris; however, its molecular mechanism remains unclear. To investigate COP1T-HA-mediated PDT-induced genomic alterations, we constructed a 3D genome map of Candida species, which uncovered the reorganization of chromatin architecture in response to PDT treatment. Our data showed that low-dose PDT causes subtle local adjustments in chromatin topology, whereas high-dose PDT leads to more pronounced changes in A/B compartmentalization, topologically associating domain (TAD) organization, and chromatin looping associated with key genes related to mitochondrial energy metabolism. Confocal imaging confirmed that high-dose COP1T-HA-mediated PDT induces localized ROS accumulation near the nucleus and a temporally ordered cellular stress response. Furthermore, functional validation through QCR10, NDUFA5, and MP knockouts confirmed the essential roles of these genes in mitochondrial integrity, ATP synthesis, ROS homeostasis, and biofilm formation. Mutants showed altered mitochondrial membrane potential, intracellular pH imbalance, and enhanced glycolytic compensation, highlighting the impact of electron transport disruption on energy metabolism. This study provides the first comprehensive insight into COP1T-HA-mediated PDT-induced chromatin reorganization in C. auris and establishes a direct connection between 3D genome remodeling and fungal energy metabolism, offering a foundation for chromatin-targeted antifungal strategies.
耳念珠菌是一种真菌病原体,常出现多药耐药或泛耐药情况。目前,针对耳念珠菌的治疗选择有限。因此,迫切需要替代治疗策略。抗菌光动力疗法(aPDT)通过光激活的光敏剂产生活性氧(ROS),已显示出对耳念珠菌有治疗前景;然而,其分子机制仍不清楚。为了研究COP1T-HA介导的光动力疗法诱导的基因组改变,我们构建了念珠菌属的三维基因组图谱,揭示了染色质结构在光动力疗法治疗后的重组情况。我们的数据表明,低剂量光动力疗法会导致染色质拓扑结构发生细微的局部调整,而高剂量光动力疗法会使A/B区室化、拓扑相关结构域(TAD)组织以及与线粒体能量代谢相关关键基因的染色质环化发生更明显的变化。共聚焦成像证实,高剂量COP1T-HA介导的光动力疗法会在细胞核附近诱导局部ROS积累以及产生时间有序的细胞应激反应。此外,通过敲除QCR10、NDUFA5和MP进行功能验证,证实了这些基因在线粒体完整性、ATP合成、ROS稳态和生物膜形成中的重要作用。突变体表现出线粒体膜电位改变、细胞内pH失衡以及糖酵解补偿增强,突出了电子传递中断对能量代谢的影响。本研究首次全面深入了解了COP1T-HA介导的光动力疗法在耳念珠菌中诱导的染色质重组,并建立了三维基因组重塑与真菌能量代谢之间的直接联系,为以染色质为靶点的抗真菌策略提供了基础。