Medical Mycology Unit, Department of Microbiology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi, India.
Department of Zoology, Ramjas College, University of Delhi, Delhi, India.
mBio. 2022 Apr 26;13(2):e0051822. doi: 10.1128/mbio.00518-22. Epub 2022 Mar 31.
Candida auris is a multidrug-resistant nosocomial fungal pathogen. While the marine environment was recently identified as a natural niche for C. auris, the environment(s) that might have contributed to the development and spread of antifungal resistance in C. auris remains a mystery. Because stored fruits are often treated with fungicides to prevent postharvest spoilage, we hypothesized that stored fruits could serve as a possible selective force for and a transmission reservoir of antifungal-resistant isolates of pathogenic yeasts, including C. auris. To test this hypothesis, we screened fruits to study the diversity of pathogenic yeasts and their antifungal susceptibility profiles. Among the 62 screened apples, the surfaces of 8 were positive for C. auris, and all were stored apples. Whole-genome sequencing (WGS) showed that C. auris strains from apples were genetically diverse and exhibited broad phylogenetic distribution among the subclades within clade I. Interestingly, strains from apples had closely related strains from other sources in India, including from patients, hospitals, and marine environments, and from clinical strains from other parts of the world. A broad range of fungicides, including dimethyl inhibitors (DMIs), were detected in stored apples, and all C. auris isolates exhibited reduced sensitivity to DMIs. Interestingly, C. auris was not isolated from freshly picked apples. Together, the results suggest a potentially complex ecology for C. auris with agriculture fungicide application on stored fruits as a significant selective force for drug resistance in clinics. In 2019, the U.S. Centers for Disease Control and Prevention classified the multidrug-resistant Candida auris as one of five pathogens posing the most urgent threats to public health. At present, the environment(s) that might have contributed to the development and spread of antifungal resistance in C. auris is unknown. Here, we tested whether fruits could be a source of multidrug-resistant C. auris. We identified genetically diverse C. auris strains with reduced sensitivity to major triazole dimethyl inhibitors fungicides on the surfaces of stored apples. The successful isolation of C. auris from apples here calls for additional investigations into plants as a reservoir of C. auris. Our findings suggest that C. auris in the natural ecosystem may come in contact with agriculture fungicides and that stored fruits could be a significant niche for the selection of azole resistance in C. auris and other human fungal pathogens.
耳念珠菌是一种多重耐药的医院真菌病原体。尽管海洋环境最近被确定为耳念珠菌的天然栖息地，但导致耳念珠菌产生抗真菌耐药性的环境仍然是个谜。由于储存的水果通常用杀菌剂处理以防止采后腐烂，我们假设储存的水果可能是致病性酵母（包括耳念珠菌）的抗真菌耐药分离株的一个可能的选择力和传播储库。为了验证这一假设，我们对水果进行了筛选，以研究致病性酵母的多样性及其抗真菌敏感性谱。在筛选的 62 个苹果中，有 8 个苹果表面检测出耳念珠菌阳性，且均为储存苹果。全基因组测序（WGS）显示，来自苹果的耳念珠菌菌株具有遗传多样性，并在 I 亚群内的亚群中表现出广泛的系统发育分布。有趣的是，来自苹果的菌株与来自印度其他来源的菌株密切相关，包括来自患者、医院和海洋环境的菌株，以及来自世界其他地区的临床菌株。在储存的苹果中检测到广泛的杀菌剂，包括二甲酰亚胺（DMIs），所有耳念珠菌分离株对 DMIs 的敏感性降低。有趣的是，没有从新鲜采摘的苹果中分离出耳念珠菌。综上所述，结果表明，农业杀菌剂在储存水果上的应用可能是耳念珠菌的一个复杂生态系统，是临床耐药性的一个重要选择力。2019 年，美国疾病控制与预防中心将多重耐药性耳念珠菌列为对公共健康构成最紧迫威胁的五种病原体之一。目前，导致耳念珠菌产生抗真菌耐药性的环境尚不清楚。在这里，我们测试了水果是否可能是多药耐药性耳念珠菌的来源。我们在储存苹果的表面发现了遗传上不同的耳念珠菌菌株，它们对主要三唑二甲酰亚胺类杀菌剂的敏感性降低。成功地从苹果中分离出耳念珠菌，这呼吁对植物作为耳念珠菌的储库进行进一步研究。我们的研究结果表明，自然界中的耳念珠菌可能会接触到农业杀菌剂，而储存的水果可能是耳念珠菌和其他人类真菌病原体选择唑类耐药性的一个重要生态位。
