Candida auris on Apples: Diversity and Clinical Significance

被引:40
作者
Yadav, Anamika [1 ,2 ]
Jain, Kusum [1 ,2 ]
Wang, Yue [3 ]
Pawar, Kalpana [1 ]
Kaur, Hardeep [2 ]
Sharma, Krishan Kumar [4 ]
Tripathy, Vandana [4 ]
Singh, Ashutosh [1 ]
Xu, Jianping [3 ]
Chowdhary, Anuradha [1 ]
机构
[1] Univ Delhi, Vallabhbhai Patel Chest Inst, Dept Microbiol, Med Mycol Unit, Delhi, India
[2] Univ Delhi, Ramjas Coll, Dept Zool, Delhi, India
[3] McMaster Univ, Dept Biol, Hamilton, ON, Canada
[4] ICAR Indian Agr Res Inst, All India Network Project Pesticide Residues, New Delhi, India
来源
MBIO | 2022年 / 13卷 / 02期
关键词
C; auris ecology; natural environment; fungicides; dimethyl inhibitors; cross-resistance; agriculture azoles; YEAST; EXPOSURE; FRUITS;
D O I
10.1128/mbio.00518-22
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
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. IMPORTANCE 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. 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.
引用
收藏
页数:18
相关论文
共 49 条
[11]   Tracing the Evolutionary History and Global Expansion of Candida auris Using Population Genomic Analyses [J].
Chow, Nancy A. ;
Munoz, Jose F. ;
Gade, Lalitha ;
Berkow, Elizabeth L. ;
Li, Xiao ;
Welsh, Rory M. ;
Forsberg, Kaitlin ;
Lockhart, Shawn R. ;
Adam, Rodney ;
Alanio, Alexandre ;
Alastruey-Izquierdo, Ana ;
Althawadi, Sahar ;
Arauz, Ana Belen ;
Ben-Ami, Ronen ;
Bharat, Amrita ;
Calvo, Belinda ;
Desnos-Ollivier, Marie ;
Escandon, Patricia ;
Gardam, Dianne ;
Gunturu, Revathi ;
Heath, Christopher H. ;
Kurzai, Oliver ;
Martin, Ronny ;
Litvintseva, Anastasia P. ;
Cuomo, Christina A. .
MBIO, 2020, 11 (02)
[12]   Candida blankii: an emerging yeast in an outbreak of fungaemia in neonates in Delhi, India [J].
Chowdhary, A. ;
Stielow, J. B. ;
Upadhyaya, G. ;
Singh, P. K. ;
Singh, A. ;
Meis, J. F. .
CLINICAL MICROBIOLOGY AND INFECTION, 2020, 26 (05) :648.e5-648.e8
[13]   A multicentre study of antifungal susceptibility patterns among 350 Candida auris isolates (2009-17) in India: role of the ERG11 and FKS1 genes in azole and echinocandin resistance [J].
Chowdhary, Anuradha ;
Prakash, Anupam ;
Sharma, Cheshta ;
Kordalewska, Milena ;
Kumar, Anil ;
Sarma, Smita ;
Tarai, Bansidhar ;
Singh, Ashutosh ;
Upadhyaya, Gargi ;
Upadhyay, Shalini ;
Yadav, Priyanka ;
Singh, Pradeep K. ;
Khillan, Vikas ;
Sachdeva, Neelam ;
Perlin, David S. ;
Meis, Jacques F. .
JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY, 2018, 73 (04) :891-899
[14]   Candida auris: A rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally [J].
Chowdhary, Anuradha ;
Sharma, Cheshta ;
Meis, Jacques F. .
PLOS PATHOGENS, 2017, 13 (05)
[15]   Rapid and precise alignment of raw reads against redundant databases with KMA [J].
Clausen, Philip T. L. C. ;
Aarestrup, Frank M. ;
Lund, Ole .
BMC BIOINFORMATICS, 2018, 19
[16]   Cross-resistance to fluconazole induced by exposure to the agricultural azole tetraconazole: an environmental resistance school? [J].
Gadelha Rocha, Marcos Fabio ;
Alencar, L. P. ;
Paiva, M. A. N. ;
Melo, Luciana Magalhaes ;
Bandeira, Silviane Praciano ;
Ponte, Y. B. ;
Sales, Jamille Alencar ;
Guedes, G. M. M. ;
Castelo-Branco, D. S. C. M. ;
Bandeira, T. J. . P. G. ;
Cordeiro, R. A. ;
Pereira-Neto, W. A. ;
Brandine, G. S. ;
Bezerra Moreira, Jose Luciano ;
Costa Sidrim, Jose Julio ;
Nogueira Brilhante, Raimunda Samia .
MYCOSES, 2016, 59 (05) :281-290
[17]   Prevalence ofCandida aurisin Canadian acute care hospitals among at-risk patients, 2018 [J].
Garcia-Jeldes, Hector Felipe ;
Mitchell, Robyn ;
McGeer, Allison ;
Rudnick, Wallis ;
Amaratunga, Kanchana ;
Vallabhaneni, Snigdha ;
Lockhart, Shawn R. ;
Bharat, Amrita .
ANTIMICROBIAL RESISTANCE AND INFECTION CONTROL, 2020, 9 (01)
[18]   Endophytic yeasts in Malus domestica and Pyrus communis fruits under anthropogenic impact [J].
Glushakova, A. M. ;
Kachalkin, A. V. .
MICROBIOLOGY, 2017, 86 (01) :128-135
[19]  
Iwasaki S., 2012, EAR NOSE CLIN, V57, P35, DOI [10.11334/jibi.57.35, DOI 10.11334/JIBI.57.35]
[20]   On the Origins of a Species: What Might Explain the Rise of Candida auris? [J].
Jackson, Brendan R. ;
Chow, Nancy ;
Forsberg, Kaitlin ;
Litvintseva, Anastasia P. ;
Lockhart, Shawn R. ;
Welsh, Rory ;
Vallabhaneni, Snigdha ;
Chiller, Tom .
JOURNAL OF FUNGI, 2019, 5 (03)