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Wild and partially synanthropic bird yeast diversity, in vitro virulence, and antifungal susceptibility of Candida parapsilosis and Candida tropicalis strains isolated from feces

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Abstract

Yeast complexes in the fecal samples of wild (Dendrocopos major, Picus viridis) and partially synanthropic (Bombycilla garrulus, Garrulus glandarius, Pica pica, and Pyrrhula pyrrhula) birds were studied in a forest ecosystem during winter. A total of 18 yeast species were identified: 16 ascomycetes and two basidiomycetes belonging to five subphyla of fungi: Saccharomycotina (15), Pezizomycotina (1), Agaricomycotina (1), and Pucciniomycotina (1). Most yeast species were found in the fecal samples of P. pyrrhula (Candida parapsilosis, C. zeylanoides, Debaryomyces hansenii, Hanseniaspora uvarum, Metschnikowia pulcherrima, Meyerozyma carpophila, M. guilliermondii, Rhodotorula mucilaginosa); the lowest number of yeast species was observed in the feces of B. garrulus (C. parapsilosis, C. zeylanoides, Met. pulcherrima, and Rh. mucilaginosa). The opportunistic species of the genus Candida were found only in feces of partially synanthropic birds: C. parapsilosis was observed in the feces of B. garrulus, G. glandarius, P. pica, and P. pyrrhula; its relative abundance was 69.3%, 49.1%, 10.5%, and 1.1%, respectively; C. tropicalis was observed in the feces of P. pica and G. glandarius; its relative abundance was 54.6% and 7.1%, respectively. Strains of C. parapsilosis and C. tropicalis isolated from the feces of partially synanthropic birds were evaluated for their susceptibility to conventional antifungal agents (fluconazole, voriconazole, amphotericin B) and hydrolytic activity. A total of 160 strains were studied. Resistance to fluconazole was detected in 86.8% of C. parapsilosis strains and in 87% of C. tropicalis strains; resistance to voriconazole was detected in 71.7% of C. parapsilosis and in 66.7% of C. tropicalis strains, and the lowest percentage of resistant strains was detected to amphotericin B, 2.8% and 3.7% in C. parapsilosis and C. tropicalis strains, respectively. Multiresistance was detected in one strain of C. parapsilosis isolated from P. pica feces and in one strain of C. tropicalis isolated from G. glandarius feces. Phospholipase and hemolysin activities in the strains of C. parapsilosis were low (mean Pz values of 0.93 and 0.91, respectively); protease activity was moderate (mean Pz value of 0.53). The ability to produce hydrolytic enzymes was higher in the isolated strains of C. tropicalis. The mean Pz values of phospholipase and hemolysin activities were moderate (mean Pz values of 0.63 and 0.60, respectively), whereas protease activity was high (mean Pz value of 0.32). Thus, wild and partially synanthropic birds play an important role in disseminating of various yeast species. These yeasts can enter the topsoil via feces and contribute to the formation of allochthonous and uneven soil yeast diversity in natural ecosystems. In addition, partially synanthropic birds can be vectors of virulent strains of opportunistic Candida species from urban environments to natural biotopes.

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The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

The study was carried out on the scientific equipment of the Collective Usage Center “I.I. Mechnikov NIIVS,” Moscow, Russia, with the finantial support of the project by the Russian Federation represented by the Ministry of Science of Russia (Agreement No. 075-15-2021-676 dated 28.07.2021).

Funding

The study was funded by the Russian Ministry of Science and Higher Education (Agreement No. 075-15-2021-1051) and as a part of the Scientific Project of the State Order of the Goverment of Russian Federation to Lomonosov Moscow State University (No. 121040800174-6).

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А.V. Kachalkin: conceptualization; data curation; visualization; writing original draft; funding acquisition; supervision. А.М. Glushakova: conceptualization; data curation; formal analysis; methodology; visualization; writing original draft.

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Correspondence to Anna Glushakova.

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The study was approved by the Ethics Committee of Lomonosov Moscow State University.

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The authors declare no competing interests.

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Glushakova, A., Kachalkin, A. Wild and partially synanthropic bird yeast diversity, in vitro virulence, and antifungal susceptibility of Candida parapsilosis and Candida tropicalis strains isolated from feces. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00437-y

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