Skip to main content

Advertisement

Log in

Saprochaete/Magnusiomyces: identification, virulence factors, and antifungal susceptibility of a challenging rare yeast

  • Bacterial and Fungal Pathogenesis - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Saprochaete/Magnusiomyces is among rare yeasts which might emerge as causes of breakthrough infections and nosocomial outbreaks. Identification to the species level might be a challenge in clinical laboratories. Data on virulence factors are scarce and antifungal susceptibility testing methodology is not definite. The aim of this study was to confirm species identification of clinical Saprochaete/Magnusiomyces isolates, find out their virulence factors, and obtain antifungal minimum inhibitory concentrations with two reference methods. Of the 57 isolates included, 54 were Saprochaete capitata and four were Saprochaete clavata as identified by ID32C, MALDI-TOF MS, and sequencing. When tested using phenotypic methods, all isolates were negative for coagulase, hemolysis, acid proteinase, and phospholipase, 56.1% were positive for esterase, and 19.3% had intermediate surface hydrophobicity. All isolates formed biofilms, with 40.4% of the isolates producing more biomass than biofilm-positive reference strain Candida albicans MYA-274. Antifungal susceptibility testing needed an adjusted spectrophotometric inoculum than recommended in reference methods for Candida/Cryptococcus. In conclusion, Saprochaete/Magnusiomyces species could be identified using methods available in the clinical laboratories. Despite the disadvantages of the phenotypic methods, esterase positivity was observed for the first time. A high biomass production was observed in biofilms. The need for standardization of antifungal susceptibility testing was brought to attention.

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.

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available at Turkish High Education Council Thesis Center (https://tez.yok.gov.tr/UlusalTezMerkezi/giris.jsp, No: 752412) and from the corresponding author on reasonable request.

References

  1. Chen SC, Perfect J, Colombo AL et al (2021) Global guideline for the diagnosis and management of rare yeast infections: an initiative of the ECMM in cooperation with ISHAM and ASM. Lancet Infect Dis 21:e375–e386. https://doi.org/10.1016/S1473-3099(21)00203-6

    Article  PubMed  Google Scholar 

  2. Tanabe MB, Patel SA (2018) Blastoschizomyces capitatus pulmonary infections in immunocompetent patients: case report, case series and literature review. Epidemiol Infect 146:58–64. https://doi.org/10.1017/S0950268817002643

    Article  CAS  PubMed  Google Scholar 

  3. Menu E, Criscuolo A, Desnos-Ollivier M et al (2020) Saprochaete clavata outbreak infecting cancer center through dishwasher. Emerg Infect Dis 26:2031–2038. https://doi.org/10.3201/eid2609.200341

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gurgui M, Sanchez F, March F et al (2011) Nosocomial outbreak of Blastoschizomyces capitatus associated with contaminated milk in a haematological unit. J Hosp Infect 78:274–278. https://doi.org/10.1016/j.jhin.2011.01.027

    Article  CAS  PubMed  Google Scholar 

  5. Subramanya Supram H, Gokhale S, Chakrabarti A et al (2016) Emergence of Magnusiomyces capitatus infections in Western Nepal. Med Mycol 54:103–110. https://doi.org/10.1093/mmy/myv075

    Article  PubMed  Google Scholar 

  6. Duran Graeff L, Seidel D, Vehreschild MJ et al (2017) Invasive infections due to Saprochaete and Geotrichum species: report of 23 cases from the FungiScope Registry. Mycoses 60:273–279. https://doi.org/10.1111/myc.12595

    Article  CAS  PubMed  Google Scholar 

  7. Hazırolan G, Aypak A, Aksu N (2017) An unusual case of urinary tract infection caused by Saprochaete capitata under anidulafungin treatment. J Mycol Med 27:387–390. https://doi.org/10.1016/j.mycmed.2017.04.001

    Article  PubMed  Google Scholar 

  8. Kaplan E, Al-Hatmi AMS, Ilkit M et al (2018) Molecular diagnostics of arthroconidial yeasts, frequent pulmonary opportunists. J Clin Microbiol:56. https://doi.org/10.1128/JCM.01427-17

  9. de Hoog GS, Smith MT (2004) Ribosomal gene phylogeny and species delimitation in Geotrichum and its teleomorphs. Stud Mycol 50:489–516

    Google Scholar 

  10. Desnos-Ollivier M, Blanc C, Garcia-Hermoso D et al (2014) Misidentification of Saprochaete clavata as Magnusiomyces capitatus in clinical isolates: utility of internal transcribed spacer sequencing and matrix-assisted laser desorption ionization-time of flight mass spectrometry and importance of reliable databases. J Clin Microbiol 52:2196–2198. https://doi.org/10.1128/JCM.00039-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246. https://doi.org/10.1073/pnas.1117018109

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  12. Pontieri E, Caracciolo C, Ceddia T et al (2005) Genetic variability among Blastoschizomyces capitatus isolates from different clinical sources. Int J Immunopathol Pharmacol 18:531–539. https://doi.org/10.1177/039463200501800313

    Article  CAS  PubMed  Google Scholar 

  13. D'Antonio D, Parruti G, Pontieri E et al (2004) Slime production by clinical isolates of Blastoschizomyces capitatus from patients with hematological malignancies and catheter-related fungemia. Eur J Clin Microbiol Infect Dis 23:787–789. https://doi.org/10.1007/s10096-004-1207-4

    Article  CAS  PubMed  Google Scholar 

  14. CLSI. CLSI Document M27A (2022) Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts, 4th edn. Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  15. EUCAST. The European Committee on Antimicrobial Susceptibility Testing. 2020. EUCAST Definitive Document E.DEF 7.3.2 Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. Accessed 20.09.2023; Available from: http://www.eucast.org/astoffungi/clinicalbreakpointsforantifungals/

  16. Lockhart SR, Messer SA, Pfaller MA et al (2008) Geographic distribution and antifungal susceptibility of the newly described species Candida orthopsilosis and Candida metapsilosis in comparison to the closely related species Candida parapsilosis. J Clin Microbiol 46:2659–2664. https://doi.org/10.1128/JCM.00803-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Al-Dabbagh AAH, Ajah HA, Salman JAS (2023) Detection of virulence factors from Candida spp. isolated from oral and vaginal candidiasis in Iraqi patients. Arch Razi Inst 78:465–474. https://doi.org/10.22092/ARI.2022.359464.2420

    Article  Google Scholar 

  18. Jafari M, Salari S, Pakshir K et al (2017) Exoenzyme activity and possibility identification of Candida dubliniensis among Candida albicans species isolated from vaginal candidiasis. Microb Pathog 110:73–77. https://doi.org/10.1016/j.micpath.2017.06.024

    Article  CAS  PubMed  Google Scholar 

  19. Yiğit N, Aktas AE, Ayyildiz A (2008) Detection of coagulase activity in pathogenic Candida species. J Int Med Res 36:1378–1382. https://doi.org/10.1177/147323000803600627

    Article  PubMed  Google Scholar 

  20. Alp S, Arikan S (2008) Investigation of extracellular elastase, acid proteinase and phospholipase activities as putative virulence factors in clinical isolates of Aspergillus species. J Basic Microbiol 48:331–337. https://doi.org/10.1002/jobm.200700349

    Article  PubMed  Google Scholar 

  21. Dağ A, Çerikçioğlu N (2006) Investigation of some virulence factors of Trichosporon asahii strains isolated from the clinical samples of hospitalized patients. Mikrobiyol Bul 40:225–235

    PubMed  Google Scholar 

  22. Slifkin M (2000) Tween 80 opacity test responses of various Candida species. J Clin Microbiol 38:4626–4628. https://doi.org/10.1128/JCM.38.12.4626-4628.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Melo AS, Bizerra FC, Freymuller E et al (2011) Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol 49:253–262. https://doi.org/10.3109/13693786.2010.530032

    Article  CAS  PubMed  Google Scholar 

  24. Pierce CG, Uppuluri P, Tummala S et al (2010) A 96 well microtiter plate-based method for monitoring formation and antifungal susceptibility testing of Candida albicans biofilms. J Vis Exp. https://doi.org/10.3791/2287

  25. Aslan H, Gulmez D (2016) Investigation of the correlation between biofilm forming ability of urinary Candida isolates with the use of urinary catheters and change of antifungal susceptibility in the presence of biofilm. Mikrobiyol Bul 50:256–265. https://doi.org/10.5578/mb.24248

    Article  CAS  PubMed  Google Scholar 

  26. CDC. OFD-500-P03 antifungal susceptibility testing yeasts using gradient diffusion strips. 2020. Accessed 10.09.2023; Available from: https://www.cdc.gov/fungal/lab-professionals/afst-yeasts.html

  27. Aydın M, Kuştimur S, Kalkancı A et al (2019) Identification of medically important yeasts by sequence analysis of the internal transcribed spacer and D1/D2 region of the large ribosomal subunit. Rev Iberoam Micol 36:129–138. https://doi.org/10.1016/j.riam.2019.05.002

    Article  PubMed  Google Scholar 

  28. Posteraro B, Efremov L, Leoncini E et al (2015) Are the conventional commercial yeast identification methods still helpful in the era of new clinical microbiology diagnostics? A meta-analysis of their accuracy. J Clin Microbiol 53:2439–2450. https://doi.org/10.1128/JCM.00802-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kolecka A, Khayhan K, Groenewald M et al (2013) Identification of medically relevant species of arthroconidial yeasts by use of matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 51:2491–2500. https://doi.org/10.1128/Jcm.00470-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Demir F, Kuştimur S (2014) Investigation of some virulence factors in Trichosporon spp. strains. Mikrobiyol Bul 48:628–638

    Article  PubMed  Google Scholar 

  31. Sun W, Su J, Xu S et al (2012) Trichosporon asahii causing nosocomial urinary tract infections in intensive care unit patients: genotypes, virulence factors and antifungal susceptibility testing. J Med Microbiol 61:1750–1757. https://doi.org/10.1099/jmm.0.049817-0

    Article  CAS  PubMed  Google Scholar 

  32. Hazırolan G, Koçak N, Karagöz A (2018) Sequence-based identification, genotyping and virulence factors of Trichosporon asahii strains isolated from urine samples of hospitalized patients (2011-2016). J Mycol Med 28:452–456. https://doi.org/10.1016/j.mycmed.2018.06.006

    Article  PubMed  Google Scholar 

  33. Danchik C, Casadevall A (2020) Role of cell surface hydrophobicity in the pathogenesis of medically-significant fungi. Front Cell Infect Microbiol 10:594973. https://doi.org/10.3389/fcimb.2020.594973

    Article  PubMed  Google Scholar 

  34. ElGindi M, Al-Baghdadi R, Jackman AB et al (2021) Where the infection is isolated rather than the specific species correlates with adherence strength, whereas biofilm density remains static in clinically isolated Candida and arthroconidial yeasts. Can J Microbiol 67:497–505. https://doi.org/10.1139/cjm-2020-0215

    Article  CAS  PubMed  Google Scholar 

  35. Kraft L, Ribeiro VST, Petroski LP et al (2023) Saprochaete clavata invasive infection: characterization, antifungal susceptibility, and biofilm evaluation of a rare yeast isolated in Brazil. Rev Inst Med Trop Sao Paulo 65:e12. https://doi.org/10.1590/S1678-9946202365012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Noster J, Koeppel MB, Desnos-Olivier M et al (2022) Bloodstream infections caused by Magnusiomyces capitatus and Magnusiomyces clavatus: epidemiological, clinical, and microbiological features of two emerging yeast species. Antimicrob Agents Chemother 66:e0183421. https://doi.org/10.1128/AAC.01834-21

    Article  PubMed  Google Scholar 

  37. CLSI. CLSI Document M38-A (2002) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, approved standard-first edn. Clinical and Laboratory Standards Institute/National Committee for Clinical Laboratory Standards, Wayne, PA

    Google Scholar 

  38. Fernandez-Ruiz M, Guinea J, Puig-Asensio M et al (2017) Fungemia due to rare opportunistic yeasts: data from a population-based surveillance in Spain. Med Mycol 55:125–136. https://doi.org/10.1093/mmy/myw055

    Article  PubMed  Google Scholar 

  39. EUCAST. The European Committee on Antimicrobial Susceptibility Testing. 2020. Breakpoint tables for interpretation of MICs for antifungal agents Version 10.0. Accessed; Available from: http://www.eucast.org/astoffungi/clinicalbreakpointsforantifungals/

  40. CLSI. CLSI Document M27M44S (2022) Clinical and Laboratory Standards Institute, Performance standards for antifungal susceptibility testing of yeasts, 3rd edn. Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  41. Esposto MC, Prigitano A, Lo Cascio G et al (2019) Yeast-like filamentous fungi: molecular identification and in vitro susceptibility study. Med Mycol 57:909–913. https://doi.org/10.1093/mmy/myy133

    Article  CAS  PubMed  Google Scholar 

  42. Cuenca-Estrella M, Gomez-Lopez A, Mellado E et al (2006) Head-to-head comparison of the activities of currently available antifungal agents against 3,378 Spanish clinical isolates of yeasts and filamentous fungi. Antimicrob Agents Chemother 50:917–921. https://doi.org/10.1128/AAC.50.3.917-921.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Prof. Dr. Sevtap Arikan-Akdagli for her constructive comments and Dr. Ceylan Polat for her help in improving Figure 1.

Funding

This study was supported by the Hacettepe University Scientific Research Unit (Project Code: THD-2022-19827).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study’s conception and design. Material preparation and data collection were performed by Beyzanur Kaşaltı, and analysis was performed by Beyzanur Kaşaltı and Dolunay Gülmez. The first draft of the manuscript was written by Beyzanur Kaşaltı and finalized by Dolunay Gülmez. All authors commented on previous and final versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Dolunay Gülmez.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Rosana Puccia

Part of this work was presented in the 37th ANKEM Rational Antibiotic Use Congress, 26–30th October 2022, Antalya, Türkiye.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 132 kb)

ESM 2

(DOCX 733 kb)

ESM 3

(DOCX 572 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaşaltı, B., Gülmez, D. Saprochaete/Magnusiomyces: identification, virulence factors, and antifungal susceptibility of a challenging rare yeast. Braz J Microbiol 55, 41–49 (2024). https://doi.org/10.1007/s42770-024-01248-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-024-01248-7

Keywords

Navigation