Vol1Art1

Opportunistic yeasts on stored apples: A One Health perspective

Ayşe Sultan Karakoyun1, Nevzat Ünal1,2, Banu Metin3, Esra Yıldırım Servi3, Bram Spruijtenburg4,5, Muhammed Alper Özarslan6, Ramazan Gümral7, Aylin Döğen8, Macit Ilkit1#, Hazal Kandemir9, Jacques F. Meis5,10, Çağrı Ergin11, and Sybren de Hoog5

1Division of Mycology, Faculty of Medicine, Çukurova University, Adana, Türkiye; 2University of Health Sciences, Adana City Training and Research Hospital, Laboratory of Medical Microbiology, Adana, Türkiye; 3Department of Food Engineering, Faculty of Engineering and Natural Sciences, Istanbul Sabahattin Zaim University, Istanbul, Türkiye; 4Department of Medical Microbiology and Infectious Diseases, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands; 5Center of Expertise for Mycology, Radboudumc / Canisius Wilhelmina Hospital, Nijmegen, The Netherlands; 6Department of Microbiology, Faculty of Medicine, Ege University, Izmir, Türkiye; 7Department of Microbiology, Gulhane Training and Research Hospital, University of Health Sciences, Ankara, Türkiye; 8Department of Pharmaceutical Microbiology, Faculty of Pharmacy, Mersin University, Mersin, Türkiye; 9Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; 10University of Cologne, Faculty of Medicine and University Hospital Cologne, Institute of Translational Research, Department I of Internal Medicine, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases and ECMM Excellence Center for Medical Mycology, Cologne, Germany; 11Department of Medical Microbiology, Faculty of Medicine, Pamukkale University, Denizli, Türkiye 

Abstract

The emergence of resistance to antifungal drugs and fungicides challenges human health and food security worldwide. We investigated the presence of fungi on the surface of stored apples, and addressed the ecological characteristics and importance of the Candida parapsilosis and Exophiala dermatitidis species complexes from a “One Health” perspective. We collected 528 stored apples from marketplaces in 26 cities in Türkiye. Surface samples from each apple were inoculated onto Sabouraud’s glucose agar and on a high-salt alkaline screening medium. Culture plates were incubated at 37°C and 40°C for 10 days and checked for yeast growth every alternate day. Fourteen isolates were obtained from the surfaces of 13 (2.5%) stored apples. Final identification for Candida and Exophiala isolates was based on the sequencing of the rDNA internal transcribed spacer region and the D1-D2 region of the large subunit rDNA. We identified nine Candida parapsilosis, one Exophiala dermatitidis, and four Exophiala phaeomuriformis isolates. Mating genotypes were determined for all isolates using PCR with species-specific primers. Antifungal susceptibility profiles of four antifungal compounds were determined for all isolates using an E-test. A fluconazole-susceptible and -resistant isolate displayed an identical short tandem repeat (STR) genotype; all the other C. parapsilosis isolates differed from each other in one or more STR markers. Although the association between fruits and fungi is well established, we report the isolation of a human-pathogenic Exophiala species for the first time. Since the association of E. dermatitidis and C. parapsilosis has been noted previously in other habitats such as dishwashers, this species combination might be viewed as an ecological community. This concept of common environmental factors shared by divergent habitats may ease source-tracking of infectious fungi. 

Open Access

Cite this article :
Karakoyun AS, Ünal N, Metin B, Servi EY, Spruijtenburg B, Özarslan MA, Gümral R, Döğen A, Ilkit M, Kandemir H, Meis JF, Ergin C & de Hoog GS. 2023. Opportunistic yeasts on stored apples: A One Health perspective. One Health Mycology 1(1), 4-13.

ISSN nummer: xxxxxx

Keywords: Candida parapsilosis; Exophiala; genotyping; saprotrophs; sexual reproduction; short tandem repeats

Article highlights:

  • Exophiala dermatitidis and Candida parapsilosis are occasionally found on fresh apples.
  • The apple skin can be can be viewed as an oligotrophic habitat.
  • The same combination of black and white yeasts is known from dishwashers and can be viewed as a microbial community.

#Correspondence: macitilkit@gmail.com

Article info:
Received 3 August 2023
Revised 7 September 2023
Accepted 7 September 2023
Appeared online 15 September 2023
One Health Mycology 1(1): 4−13, 2023