Skip to main content

Advertisement

Log in

Identification and Molecular Analysis of Pathogenic Yeasts in Droppings of Domestic Pigeons in Beijing, China

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Feral pigeons are known as reservoirs of pathogenic yeasts that cause opportunistic infections in human. In the outskirts of Beijing, China, pigeons are more frequently raised at homes than are encountered in public areas. Many studies have focused on the presence of pathogenic yeasts in the excreta (fresh or withered) of a variety kinds of birds, pigeon crop and cloacae. One hundred and forty-three samples of fresh droppings were collected from three suburban pigeon-raising homes in an area of northern Beijing, China. The internal transcribed sequences (ITS) of all strains (except for 8 strains of Rhodotorula sp. ) were sequenced and compared with those of the databases of the National Center for Biotechnology Information website (http://www.ncbi.nlm.nih.gov) using the Basic Local Alignment Search Tool (BLAST). Yeasts representing 8 genera, Cryptococcus, Filobasidium, Rhodotorula, Candida, Debaryomyces, Saccaromyces, Trichosporon and Sporidiobolus, were identified from 120 isolates. Cryptococcus was the most prolific genera represented by eight species. The populations of yeast species isolated from fresh pigeon droppings were different among homes. Although it is well established that Cryptococcus neoformans exists mainly in old pigeon guano, several C. neoformans strains were still isolated from fresh pigeon excreta, providing a clue that live cryptococcal cells could move through the gastrointestinal tract of the pigeons. Eight genera identified from fresh droppings of domestic pigeons further confirm that pigeons serve as reservoirs, carriers and even spreaders of Cryptococcus species and other medically significant yeasts. The proportion of pathogenic yeasts in all isolates is more than 90 %.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Mattsson R, Haemig PD, Olsen B. Feral pigeons as carriers of Cryptococcus laurentii, Cryptococcus uniguttulatus and Debaryomyces hansenii. Med Mycol. 1999;37(5):367–9.

  2. Costa AK, Sidrim JJ, Cordeiro RA, Brilhante RS, Monteiro AJ, Rocha MF. Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. Mycopathologia. 2010;169(3):207–13. doi:10.1007/s11046-009-9245-1.

    Article  PubMed  Google Scholar 

  3. Chen J, Varma A, Diaz MR. Cryptococcus neoformans strains and infection in apparently immunocompetent patients, China. Emerg Infect Dis. 2008;14(5):755–62.

    Article  PubMed  CAS  Google Scholar 

  4. Loperena-Alvarez Y, Ren P, Li X, Schoonmaker-Bopp DJ, Ruiz A, Chaturvedi V, et al. Genotypic characterization of environmental isolates of Cryptococcus gattii from Puerto Rico. Mycopathologia. 2010;170(4):279–85. doi:10.1007/s11046-010-9296-3.

    Article  PubMed  Google Scholar 

  5. Costa Sdo P, Lazéra Mdos S, Santos W. First isolation of Cryptococcus gattii molecular type VGII and Cryptococcus neoformans molecular type VNI from environmental sources in the city of Belém, Pará, Brazil. Mem Inst Oswaldo Cruz. 2009;104(4):662–4.

  6. Chee HY, Lee KB. Isolation of Cryptococcus neoformans var. grubii (serotype A) from pigeon droppings in Seoul, Korea. J Microbiol. 2005;43(5):469–72.

    PubMed  CAS  Google Scholar 

  7. Bovers M, Hagen F, Kuramae EE, Hoogveld HL, Dromer F, St-Germain G, et al. AIDS patient death caused by novel Cryptococcus neoformans x C. gattii hybrid. Emerg Infect Dis. 2008;14(7):1105–8.

    Article  PubMed  CAS  Google Scholar 

  8. Rosario I, Soro G, Deniz S, Ferrer O, Acosta F, Padilla D, et al. Presence of C. albidus, C. laurentii and C. uniguttulatus in crop and droppings of pigeon lofts (Columba livia). Mycopathologia. 2010;169(4):315–9. doi:10.1007/s11046-009-9262-0.

    Article  PubMed  CAS  Google Scholar 

  9. Cafarchia C, Romito D, Iatta R, Camarda A, Montagna MT, Otranto D. Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts. Med Mycol. 2006;44(6):485–92. doi:10.1080/13693780600735452.

    Article  PubMed  CAS  Google Scholar 

  10. McCurdy LH, Morrow JD. Infections due to non-neoformans cryptococcal species. Compr Ther. 2003;29(2–3):95–101.

    PubMed  Google Scholar 

  11. Khawcharoenporn T, Apisarnthanarak A, Mundy LM. Non-neoformans cryptococcal infections: a systematic review. Infection. 2007;35(2):51–8. doi:10.1007/s15010-007-6142-8.

    Article  PubMed  CAS  Google Scholar 

  12. Lanzafame M, De Checchi G, Parinello A, Trevenzoli M, Cattelan AM. Rhodotorula glutinis-related meningitis. J Clin Microbiol. 2001;39(1):410.

    Article  PubMed  CAS  Google Scholar 

  13. Pan W, Liao W, Hagen F, Theelen B, Shi W, Meis JF, et al. Meningitis caused by Filobasidium uniguttulatum: case report and overview of the literature. Mycoses. 2011;. doi:10.1111/j.1439-0507.2011.02054.x.

    PubMed  Google Scholar 

  14. Wagner D, Sander A, Bertz H, Finke J, Kern WV. Breakthrough invasive infection due to Debaryomyces hansenii (teleomorph Candida famata) and Scopulariopsis brevicaulis in a stem cell transplant patient receiving liposomal amphotericin B and caspofungin for suspected aspergillosis. Infection. 2005;33(5–6):397–400. doi:10.1007/s15010-005-5082-4.

    Article  PubMed  CAS  Google Scholar 

  15. Munoz P, Bouza E, Cuenca-Estrella M, Eiros JM, Perez MJ, Sanchez-Somolinos M, et al. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis. 2005;40(11):1625–34. doi:10.1086/429916.

    Article  PubMed  Google Scholar 

  16. Rosario I, Acosta B, Colom MF. Pigeons and other birds as a reservoir for Cryptococcus spp. Rev Iberoam Micol. 2008;25(1):S13–8.

    Article  PubMed  Google Scholar 

  17. Mancianti F, Nardoni S, Ceccherelli R. Occurrence of yeasts in psittacines droppings from captive birds in Italy. Mycopathologia. 2002;153(3):121–4.

    Article  PubMed  Google Scholar 

  18. Takashima M, Nakase T. Molecular phylogeny of the genus Cryptococcus and related species based on the sequences of 18S rDNA and internal transcribed spacer regions. Microbiol Cult Coll. 1999;15(2):35–47.

    Google Scholar 

  19. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform Online. 2008;4:193–201.

    PubMed  Google Scholar 

  20. Leaw SN, Chang HC, Sun HF, Barton R, Bouchara JP, Chang TC. Identification of medically important yeast species by sequence analysis of the internal transcribed spacer regions. J Clin Microbiol. 2006;44(3):693–9. doi:10.1128/JCM.44.3.693-699.2006.

    Article  PubMed  CAS  Google Scholar 

  21. Sugita T, Nishikawa A, Ikeda R, Shinoda T. Identification of medically relevant Trichosporon species based on sequences of internal transcribed spacer regions and construction of a database for Trichosporon identification. J Clin Microbiol. 1999;37(6):1985–93.

    PubMed  CAS  Google Scholar 

  22. Li L, Wang Jc, Zhang Qq. Isolation and identification of Cryptococcus neoformans from pigeon dropping. J Clin Dermatol. 2000;29(4):4–6.

  23. Chaskes S, Edberg SC, Singer JM. A DL-DOPA drop test for the identification of Cryptococcus neoformans. Mycopathologia. 1981;74(3):143–8.

    Article  PubMed  CAS  Google Scholar 

  24. Canteros CE, Rodero L, Rivas MC, Davel G. A rapid urease test for presumptive identification of Cryptococcus neoformans. Mycopathologia. 1996;136(1):21–3.

    Article  PubMed  CAS  Google Scholar 

  25. Kwon-Chung KJ, Polacheck I, Bennett JE. Improved diagnostic medium for separation of Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans var. gattii (serotypes B and C). J Clin Microbiol. 1982;15(3):535–7.

    PubMed  CAS  Google Scholar 

  26. Lim CS, Tung CH, Rosli R, Chong PP. An alternative Candida spp. cell wall disruption method using a basic sorbitol lysis buffer and glass beads. J Microbiol Methods. 2008;75(3):576–8. doi:10.1016/j.mimet.2008.07.026.

    Article  PubMed  CAS  Google Scholar 

  27. White T, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a guide to methods and applications. San Diego, CA: Academic Press; 1990. p. 315–22.

  28. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10. doi:10.1016/S0022-2836(05)80360-2.

    PubMed  CAS  Google Scholar 

  29. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25(24):4876–82.

    Article  PubMed  CAS  Google Scholar 

  30. Valerio E, Gadanho M, Sampaio JP. Sporobolomyces odoratus sp. nov., a new species in the Sporidiobolus ruineniae clade. FEMS Yeast Res. 2002;2(1):9–16.

  31. Ferreira-Paim K, Andrade-Silva L, Mora DJ, Pedrosa AL, Rodrigues V, Silva-Vergara ML. Genotyping of Cryptococcus neoformans isolated from captive birds in Uberaba, Minas Gerais, Brazil. Mycoses. 2011;54(5). doi:10.1111/j.1439-0507.2010.01901.x.

  32. Gonzalez-Hein G, Gonzalez-Hein J, Diaz Jarabran MC. Isolation of Cryptococcus neoformans in dry droppings of captive birds in Santiago, Chile. J Avian Med Surg. 2010;24(3):227–36.

    Article  PubMed  Google Scholar 

  33. Quintero E, Castaneda E, Ruiz A. Environmental distribution of Cryptococcus neoformans in the department of Cundinamarca-Colombia. Rev Iberoam Micol. 2005;22(2):93–8.

    Article  PubMed  Google Scholar 

  34. Kobayashi CC, Souza LK, Fernandes Ode F, Silva AC, Sousa ED, et al. Characterization of Cryptococcus neoformans isolated from urban environmental sources in Goiania, Goias State, Brazil. Rev Inst Med Trop Sao Paulo. 2005;47(4):203–7.

    Article  PubMed  Google Scholar 

  35. Caicedo LD, Alvarez MI, Delgado M, Cardenas A. Cryptococcus neoformans in bird excreta in the city zoo of Cali, Colombia. Mycopathologia. 1999;147(3):121–4.

    Article  PubMed  CAS  Google Scholar 

  36. Jang YH, Lee SJ, Lee JH, Chae HS, Kim SH, Choe NH. Prevalence of yeast-like fungi and evaluation of several virulence factors from feral pigeons in Seoul, Korea. Lett Appl Microbiol. 2011;52(4):367–71. doi:10.1111/j.1472-765X.2011.03009.x.

    Article  PubMed  CAS  Google Scholar 

  37. Cordeiro RA, Brilhante RS, Pantoja LD, Moreira Filho RE, Vieira PR, Rocha MF, et al. Isolation of pathogenic yeasts in the air from hospital environments in the city of Fortaleza, northeast Brazil. Braz J Infect Dis. 2010;14(1):30–4.

    Article  PubMed  Google Scholar 

  38. Gori K, Bjorklund MK, Canibe N, Pedersen AO, Jespersen L. Occurrence and identification of yeast species in fermented liquid feed for piglets. Microb Ecol. 2011;61(1):146–53. doi:10.1007/s00248-010-9706-6.

    Article  PubMed  Google Scholar 

  39. Fonseca A, Scorzetti G, Fell JW. Diversity in the yeast Cryptococcus albidus and related species as revealed by ribosomal DNA sequence analysis. Can J Microbiol. 2000;46(1):7–27.

    Article  PubMed  CAS  Google Scholar 

  40. Sugita T, Nishikawa A, Shinoda T. DNA relatedness among the three varieties of Cryptococcus albidus. J Gen Appl Microbiol. 1992;38:83–6.

    Article  CAS  Google Scholar 

  41. Sugita T, Takashima M, Ikeda R, Nakase T, Shinoda T. Intraspecies diversity of Cryptococcus albidus isolated from humans as revealed by sequences of the internal transcribed spacer regions. Microbiol Immunol. 2001;45(4):291–7.

    PubMed  CAS  Google Scholar 

  42. Fell JW, Blatt GM, Statzell-Tallman A. Validation of the basidiomycetous yeast, Sporidiobolus microsporus sp. nov., based on phenotypic and molecular analyses. Antonie Van Leeuwenhoek. 1998;74(4):265–70.

    Article  PubMed  CAS  Google Scholar 

  43. Gadanho M, Sampaio JP, Spencer-Martins I. Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: R. azoricum sp. nov. Can J Microbiol. 2001;47(3):213–21.

    PubMed  CAS  Google Scholar 

  44. Chang HC, Leaw SN, Huang AH, Wu TL, Chang TC. Rapid identification of yeasts in positive blood cultures by a multiplex PCR method. J Clin Microbiol. 2001;39(10):3466–71. doi:10.1128/JCM.39.10.3466-3471.2001.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by National Sci-Tech Key Project (2009ZX10004-203).We thank Hai yin Wang and Wen Zhang, colleagues from the Bioinformatics Office, for the help of the sequence summit to Genbank. We thank Wenjun Li, from Duke University, a lot for critical reading of the manuscript. We also thank Bo Pang, colleagues from the Diarrhea Office for important suggestions of the paper’s structures. Finally, we thank friends Lei Zhao from University of Minnesota for checking grammar.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jin-Xing Lu.

Additional information

Yuan Wu and Peng-Cheng Du have equal contribution to this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, Y., Du, PC., Li, WG. et al. Identification and Molecular Analysis of Pathogenic Yeasts in Droppings of Domestic Pigeons in Beijing, China. Mycopathologia 174, 203–214 (2012). https://doi.org/10.1007/s11046-012-9536-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-012-9536-9

Keywords

Navigation