Skip to main content
SpringerLink
Log in

Multilocus microsatellite analysis of European and African Candida glabrata isolates

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

This study aimed to elucidate the genetic relatedness and epidemiology of 127 clinical and environmental Candida glabrata isolates from Europe and Africa using multilocus microsatellite analysis. Each isolate was first identified using phenotypic and molecular methods and subsequently, six unlinked microsatellite loci were analyzed using automated fluorescent genotyping. Genetic relationships were estimated using the minimum-spanning tree (MStree) method. Microsatellite analyses revealed the existence of 47 different genotypes. The fungal population showed an irregular distribution owing to the over-representation of genetically different infectious haplotypes. The most common genotype was MG-9, which was frequently found in both European and African isolates. In conclusion, the data reported here emphasize the role of specific C. glabrata genotypes in human infections for at least some decades and highlight the widespread distribution of some isolates, which seem to be more able to cause disease than others.

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

Access this article

Log in via an institution

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. Bolotin-Fukuhara M, Fairhead C (2014) Candida glabrata: a deadly companion? Yeast 31:279–288. doi:10.1002/yea.3019

    Article  CAS  PubMed  Google Scholar 

  2. Pfaller MA, Andes DR, Diekema DJ, Horn DL, Reboli AC, Rotstein C, Franks B, Azie NE (2014) Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2,496 patients: data from the Prospective Antifungal Therapy (PATH) registry 2004–2008. PLoS One 9, e101510. doi:10.1371/journal.pone.0101510

    Article  PubMed  PubMed Central  Google Scholar 

  3. Quindós G (2014) Epidemiology of candidaemia and invasive candidiasis. A changing face. Rev Iberoam Micol 31:42–48. doi:10.1016/j.riam.2013.10.001

    Article  PubMed  Google Scholar 

  4. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36:288–305. doi:10.1111/j.1574-6976.2011.00278.x

    Article  CAS  PubMed  Google Scholar 

  5. Li L, Redding S, Dongari-Bagtzoglou A (2007) Candida glabrata: an emerging oral opportunistic pathogen. J Dent Res 86:204–215. doi:10.1177/154405910708600304

    Article  CAS  PubMed  Google Scholar 

  6. Tomczak H, Szałek E, Grześkowiak E (2014) The problems of urinary tract infections with Candida spp. aetiology in women. Postepy Hig Med Dosw (Online) 68:1036–1039. doi:10.5604/17322693.1118989

    Article  Google Scholar 

  7. Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62:10–24. doi:10.1099/jmm.0.045054-0

    Article  CAS  PubMed  Google Scholar 

  8. Pfaller MA, Castanheira M, Messer SA, Moet GJ, Jones RN (2010) Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY Antimicrobial Surveillance Program (2008–2009). Diagn Microbiol Infect Dis 68:278–283. doi:10.1016/j.diagmicrobio.2010.06.015

    Article  PubMed  Google Scholar 

  9. Turner SA, Butler G (2014) The Candida pathogenic species complex. Cold Spring Harb Perspect Med 4:a019778. doi:10.1101/cshperspect.a019778

    Article  PubMed  Google Scholar 

  10. Chapeland-Leclerc F, Hennequin C, Papon N, Noël T, Girard A, Socié G, Ribaud P, Lacroix C (2010) Acquisition of flucytosine, azole, and caspofungin resistance in Candida glabrata bloodstream isolates serially obtained from a hematopoietic stem cell transplant recipient. Antimicrob Agents Chemother 54:1360–1362. doi:10.1128/AAC.01138-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Abbes S, Sellami H, Sellami A, Hadrich I, Amouri I, Mahfoudh N, Neji S, Makni F, Makni H, Ayadi A (2012) Candida glabrata strain relatedness by new microsatellite markers. Eur J Clin Microbiol Infect Dis 31:83–91. doi:10.1007/s10096-011-1280-4

    Article  CAS  PubMed  Google Scholar 

  12. Amouri I, Sellami H, Abbes S, Hadrich I, Mahfoudh N, Makni H, Ayadi A (2012) Microsatellite analysis of Candida isolates from recurrent vulvovaginal candidiasis. J Med Microbiol 61:1091–1096. doi:10.1099/jmm.0.043992-0

    Article  PubMed  Google Scholar 

  13. Brisse S, Pannier C, Angoulvant A, de Meeus T, Diancourt L, Faure O, Muller H, Peman J, Viviani MA, Grillot R, Dujon B, Fairhead C, Hennequin C (2009) Uneven distribution of mating types among genotypes of Candida glabrata isolates from clinical samples. Eukaryot Cell 8:287–295. doi:10.1128/EC.00215-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Foulet F, Nicolas N, Eloy O, Botterel F, Gantier JC, Costa JM, Bretagne S (2005) Microsatellite marker analysis as a typing system for Candida glabrata. J Clin Microbiol 43:4574–4579. doi:10.1128/JCM.43.9.4574-4579.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Criseo G, Scordino F, Romeo O (2015) Current methods for identifying clinically important cryptic Candida species. J Microbiol Methods 111:50–56. doi:10.1016/j.mimet.2015.02.004

    Article  CAS  PubMed  Google Scholar 

  16. Romeo O, Scordino F, Pernice I, Lo Passo C, Criseo G (2009) A multiplex PCR protocol for rapid identification of Candida glabrata and its phylogenetically related species Candida nivariensis and Candida bracarensis. J Microbiol Methods 79:117–120. doi:10.1016/j.mimet.2009.07.016

    Article  CAS  PubMed  Google Scholar 

  17. Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611. doi:10.1111/j.1755-0998.2011.03014.x

    Article  CAS  PubMed  Google Scholar 

  18. Hunter PR, Gaston MA (1998) Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 26:2465–2466

    Google Scholar 

  19. Esposto MC, Prigitano A, Romeo O, Criseo G, Trovato L, Tullio V, Fadda ME, Tortorano AM; FIMUA Working Group (2013) Looking for Candida nivariensis and C. bracarensis among a large Italian collection of C. glabrata isolates: results of the FIMUA working group. Mycoses 56:394–396. doi:10.1111/myc.12026

    Article  Google Scholar 

  20. Van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M (2007) Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13:1–46. doi:10.1111/j.1469-0691.2007.01786.x

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale F. Stagno d’Alcontres, 31, 98166, Messina, Italy

    V. Chillemi, C. Lo Passo, S. Rharmitt, G. Criseo & O. Romeo

  2. CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands

    A. D. van Diepeningen

  3. Department of Human Pathology, University of Messina, Via Consolare Valeria, 98125, Messina, Italy

    D. Delfino & A. Cascio

  4. Department of Microbiology, Plateau State University, P.M.B 2012, Bokkos, Plateau State, Nigeria

    N. E. Nnadi

  5. Medical Microbiology Department, Faculty of Medicine, Uludag University, 16059, Bursa, Turkey

    B. D. Cilo

  6. Biology Department, Minho University, Campus de Gualtar, 4710-057, Braga, Portugal

    P. Sampaio

  7. Institut für Pilzkrankheiten, Luisenstrasse 50, 10117, Berlin, Germany

    H.-J. Tietz

  8. Servicio de Microbiología, Hospital Universitario y Politécnico La Fe, Valencia, España

    J. Pemán

  9. IRCCS Centro Neurolesi “Bonino-Pulejo”, SS113, 98124, Messina, Italy

    O. Romeo & F. Scordino

Authors
  1. V. Chillemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Lo Passo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. D. van Diepeningen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Rharmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Delfino
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Cascio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. E. Nnadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. B. D. Cilo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. P. Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. H.-J. Tietz
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. J. Pemán
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. G. Criseo
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. O. Romeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. F. Scordino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. Romeo.

Ethics declarations

Funding

This research was supported in part by the EU Mare Nostrum (EUMN-III Call) program of the European Union, grant agreement number 2011-4050/001-EMA2. Dr Sanae Rharmitt was the recipient of a scholarship (10 months) signed within the EUMN program for PhD students (F.S. 1.04.11.01 UORI) under the supervision of Prof Orazio Romeo.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study formal consent is not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chillemi, V., Lo Passo, C., van Diepeningen, A.D. et al. Multilocus microsatellite analysis of European and African Candida glabrata isolates. Eur J Clin Microbiol Infect Dis 35, 885–892 (2016). https://doi.org/10.1007/s10096-016-2610-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-016-2610-3

Keywords

Search

Navigation