Molecular identification of non-Cryptococcus yeasts associated with pigeon droppings in Shiraz, Southern Iran

Document Type: Short paper

Authors

1 Department of Parasitology and Mycology, Basic Sciences in Infectious Diseases Research Center, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

2 MSc in Medical Mycology, Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

3 Department of Parasitology and Mycology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

4 BSc in Microbiology, Department of Parasitology and Mycology, Basic Sciences in Infectious Diseases Research Center, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Background: Birds are considered as a reservoir for pathogenic and non-pathogenic fungi. Pigeon droppings have the potential for spreading these fungi to the environment. Cryptococcus species are important fungi associated with pigeon droppings. In this regard, there are many types of yeast associated with guano that is important for human and animal health. Aims: The main objective of this study is the identification of non-Cryptococcus yeasts isolated from pigeon dropping in Shiraz, Southern Iran. Methods: A total of 100 unknown yeasts, which were previously screened and identified as non-Cryptococcus from pigeon guano through the conventional methods, were used in this study. Identification of the isolates was performed based on conventional methods and DNA sequence analysis of internal transcribed spacer (ITS) rDNA gene region. The sequence results were deposited in NCBI database using the Basic Local Alignment Search Tool (BLAST). Results: A total of 16 species belonging to 7 genera were identified as Candida spp. 51% (8 species), Rhodotorula sp. 24%, Trichosporon spp. 21% (3 species), Rhodosporidium 2%, Saccharomyces 1%, Rhizoctonia 1%, and Meyerozyma 1%. The predominant isolates were Rhodotorula rubra (24%), Candida famata (20%), and Trichosporon asahii (13%). The other species were Rhodosporidium kratochvilovae 2 (2%), Saccharomyces cerevisiae 1 (1%), Rhizoctonia solani 1 (1%), and Meyerozyma caribbica 1 (1%). Conclusion: Pigeon excreta examined in this study were associated with several kinds of opportunistic yeasts which could cause diseases in prone human and animals.

Keywords


Abulreesh, HH; Organji1, SR; Elbanna, K; Haridy Osman, GE; Almalki1, MHK and Abdel-Mallek, AY (2015). First report of environmental isolation of Cryptococcus neoformans and other fungi from pigeon droppings in Makkah, Saudi Arabia and in vitro susceptibility testing. Asian Pac. J. Trop. Dis., 5: 622-626.

Asada, N; Uryu, H; Koseki, M; Takeuchi, M; Komatsu, M and Matsue, K (2006). Successful treatment of breakthrough Trichosporon asahii fungemia with voriconazole in a patient with acute myeloid leukemia. Clin. Infec. Dis., 43: e39-e41.

Bautista-Rosales, PU; Calderon-Santoyo, M; Servín-Villegas, R; Ochoa-Álvarez, NA and Ragazzo-Sánchez, JA (2013). Action mechanisms of the yeast Meyerozyma caribbica for the control of the phytopathogen Colletotrichum gloeosporioides in mangoes. Biol. Control. 65: 293-301.

Bellemain, E; Carlsen, T; Brochmann, C; Coissac, E; Taberlet, P and Kauserud, H (2010). ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol., 10: 189.

Biegańska, MJ; Rzewuska, M; Dąbrowska, I; Malewska-Biel, B; Ostrzeszewicz, M and Dworecka-Kaszak, B (2018). Mixed infection of respiratory tract in a dog caused by Rhodotorula mucilaginosa and Trichosporon jirovecii: a case report. Mycopathologia. 183: 637-644.

Cafarchia, C; Camarda, A; Romito, D; Campolo, M; Quaglia, NC; Tullio, D and Otranto, D (2006). Occurrence of yeasts in cloacae of migratory birds. Mycopathologia. 161: 229-234.

Cafarchia, C; Iatta, R; Danesi, P; Camarda, A; Capelli, G and Otranto, D (2018). Yeasts isolated from cloacal swabs, feces, and eggs of laying hens. Med. Mycol., 57: 340-345.

Chagas-Neto, TC; Chaves, GM; Melo, ASA and Colombo, AL (2009). Bloodstream infections due to Trichosporon spp.: species distribution, Trichosporon asahii genotypes determined on the basis of ribosomal DNA intergenic spacer 1 sequencing, and antifungal susceptibility testing. J. Clin. Microbiol., 47: 1074-1081.

Chakrabarti, A; Singh, K; Narang, A; Singhi, S; Batra, R; Rao, KLN; Ray, P; Gopalan, S; Das, S; Gupta, V; Gupta, AK; Bose, SM and McNeil, MM (2001). Outbreak of Pichia anomala infection in the pediatric service of a tertiary-care center in Northern India. J. Clin. Microbiol., 39: 1702-1706.

Chee, HY and Lee, KB (2005). Isolation of Cryptococcus neoformans var. grubii (serotype A) from pigeon droppings in Seoul, Korea. J. Microbiol., 43: 469-472.

Chen, SCA; Marriott, D; Playford, EG; Nguyenb, Q; Ellis, D; Meyer, W; Sorrella, TC and Slavin, M (2009). Candidaemia with uncommon Candida species: predisposing factors, outcome, antifungal susceptibility, and implications for management. Clin. Microbiol. Infec., 15: 662-669.

Costa, AK; Sidrim, JJC; Cordeiro, RA; Brilhante, RSN; Monteiro, AJ and Rocha, MFG (2010). Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. Mycopathologia. 169: 207-213.

Deem, SL (2003). Fungal diseases of birds of prey. Vet. Clin. North Am. Exot. Anim. Pract., 6: 363-376.

Ghiasian, SA; Maghsood, AH and Mirhendi, SH (2006). Disseminated, fatal Trichosporon asahii infection in a bone marrow transplant recipient. J. Microbiol. Immunol. Infect., 39: 426.

Haag-Wackernagel, D and Moch, H (2004). Health hazards posed by feral pigeons J. Infect., 48: 307-313.

Harrigan, WF (1998). Laboratory methods in food microbiology. London, UK, Gulf Professional Publishing.

Jadhav, VJ and Pal, M (2013). Human and domestic animal infections caused by Candida albicans. J. Mycopathol. Res., 51: 243-249.

Kaore, NM; Atul, AR; Khan, MZ and Ramnani, VK (2012). A rare case of human mycosis by Rhizoctonia solani. Indian J. Med. Microbiol., 30: 361-363.

Karnik, K; Reichle, JK; Fischetti, AJ and Goggin, JM (2009). Computed tomographic findings of fungal rhinitis and sinusitis in cats. Vet. Radiol. Ultrasound. 50: 65-68.

Kaygusuz, I; Mulazimoglu, L; Cerikcioglu, N; Toprak, A; Oktay, A and Korten, V (2003). An unusual native tricuspid valve endocarditis caused by Candida colliculosa. Clin. Microbiol. Infec., 9: 319-322.

Khosravi, AR (1997). Isolation of Cryptococcus neoformans from pigeon (Columba livia) droppings in northern Iran. Mycopathologia. 139: 93-95.

Lanzafame, M; De Checchi, G; Parinello, A and Cattelan, MTAM (2001). Rhodotorula glutinis-related meningitis. J. Clin. Microbiol., 39: 410.

Lee, WD; Fong, JJ; Eimes, JA and Lim, YW (2017). Diversity and abundance of human-pathogenic fungi associated with pigeon faeces in urban environments. Mol. Ecol., 26: 4574-4585.

Makimura, K; Murayama, SY and Yamaguchi, H (1994).
Detection of a wide range of medically important fungi by the polymerase chain reaction. J. Med. Microbiol., 40: 358-364.

Mancianti, F; Nardoni, S and Ceccherelli, R (2002). Occurrence of yeasts in psittacines droppings from captive birds in Italy. Mycopathologia. 153: 121.

Medina, IR; Fuentes, LR; Arteaga, MB; Valcárcel, FR; Arbelo, FA; Castillo, DP; Suárez, SD; Quintana, OF; Gutiérrez, BV; Sergent, FS and Acosta-Hernández, B (2017). Pigeons and their droppings as reservoirs of Candida and other zoonotic yeasts. Rev. Iberoam. Micol., 34: 211-214.

Miceli, MH; Díaz, JA and Lee, SA (2011). Emerging opportunistic yeast infections. Lancet Infect. Dis., 11: 142-151.

Munoz, P; Bouza, E; Cuenca-Estrella, M; Eiros, JM; Jesús Pérez, M; Sánchez-Somolinos, M; Rincón, C; Hortal, J and Peláez, T (2005). Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin. Infect. Dis., 40: 1625-1634.

Murphy, N; Damjanovic, V; Hart, CA; Buchanan, CR; Whitaker, R and Cooke, RWI (1986). Infection and colonisation of neonates by Hansenula anomala. Lancet. 327: 291-293.

Nweze, EI; Kechia, FA; Dibua, UE; Charles, EZE and Uwakwe, SONOJA (2015). Isolation of Cryptococcus neoformans from environmental samples collected in Southeastern Nigeria. Rev. Inst. Med. Trop. S. Paulo. 57: 295-298.

Pakshir, K; Fakhim, H; Vaezi, A; Meise, JF; Mahmoodi, M; Zomorodian, K; Javidnia, J; Ansari, S; Hagen, F and Badali, H (2018). Molecular epidemiology of environmental Cryptococcus species isolates based on amplified fragment length polymorphism. J. Mycol. Med., 28: 599-605.

Radosavljevic, M; Koenig, H; Letscher-Bru, V; Waller, J; Maloisel, F; Lioure, B and Herbrecht, R (1999). Candida catenulata fungemia in a cancer patient. J. Clin. Microbiol., 37: 475-477.

Rastogi, G and Sani, RK (2011). Molecular techniques to assess microbial community structure, function, and dynamics in the environment. In: Ahmad, I; Ahmad, F and Pichtel, J (Eds.), Microbes and microbial technology. (1st Edn.), New York, Springer-Verlag. PP: 29-57.

Rodriguez-Tudela, JL; Diaz-Guerra, TM; Mellado, E; Cano, V; Tapia, C; Perkins, A; Gomez-Lopez, A; Rodero, L and Cuenca-Estrella, M (2005). Susceptibility patterns and molecular identification of Trichosporon species. Antimicrob. Agents Chemother., 49: 4026-4034.

Simi, W; Leite-J, DP; Paula, CR; Hoffmann-Santos, HD; Takahara, DT and Hahna, RC (2018). Yeasts and filamentous fungi in psittacidae and birds of prey droppings in midwest region of Brazil: a potential hazard to human health. Braz. J. Biol., 79: 414-422.

Soltani, M; Bayat, M; Hashemi, SJ; Zia, MA and Pestechian, N (2013). Isolation of Cryptococcus neoformans and other opportunistic fungi from pigeon droppings. J. Res. Med. Sci., 18: 56.

Tsiodras, S; Kelesidis, T; Kelesidis, I; Bauchinger, U and E. Falagasde, M (2008). Human infections associated with wild birds. J. Infect., 56: 83-98.

Wirth, F and Goldani, LZ (2012). Epidemiology of Rhodotorula: an emerging pathogen. Interdiscip. Perspect. Infect. Dis., 2012: 465717.