Skip to main content

Advertisement

Log in

Comparative Genomics and Molecular Analysis of Epidermophyton floccosum

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Epidermophyton floccosum is one of the most common agents of human superficial fungal infections, compared with genus Trichophyton and Microsporum, it possesses uniqueness in ecology traits and rarely causing hair infections. E. floccosum is so far the only representative species of genera Epidermophyton, and it is known as anthropophilic dermatophytes. To further reveal the genome sequences and clues of virulence factors, thus in this study, we sequenced the genome of E. floccosum (CGMCC (F) E1d), and performed comparative genomic analysis with other dermatophytes. It is revealed that E. floccosum owns the largest genome size and similar GC content compared with other dermatophytes. A total of 7565 genes are predicted. By comparing with the closest species N. gypseum, our study reveals that number and structure of adhesion factors, secreted proteases and LysM domain might contribute to the pathogenic and ecological traits of E. floccosum. Mating genes is also detected in genome data. Furthermore, we performed AFLP analysis trying to discuss intraspecific differences of E. floccosum, but no significant relationship is found between genotype and geographical distribution. Upon above, our study provides a deeper understanding and strong foundation for future researches about E. floccosum.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, et al. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia. 2017;182(1–2):5–31. https://doi.org/10.1007/s11046-016-0073-9.

    Article  PubMed  Google Scholar 

  2. McCormack P, Benham RW. An unusual finding in Epidermophyton floccosum. J Investig Dermatol. 1952;19(5):315–7. https://doi.org/10.1038/jid.1952.104.

    Article  CAS  PubMed  Google Scholar 

  3. Cabañes FJ, Bragulat MR, Bruguera T, Abarca L. The growth of Epidermophyton floccosum and E. stockdaleae at different temperatures. Mycopathologia. 1990;112(3):157–63. https://doi.org/10.1007/bf00436647.

    Article  PubMed  Google Scholar 

  4. Cabañes FJ, Abarca L, Bragulat M, Bruguera T. Sensitivity of some strains of the genus Epidermophyton to different antifungal agents. Mycopathologia. 1989;105(3):153–6. https://doi.org/10.1007/bf00437247.

    Article  PubMed  Google Scholar 

  5. Zamani S, Sadeghi G, Yazdinia F, Moosa H, Pazooki A, Ghafarinia Z, et al. Epidemiological trends of dermatophytosis in Tehran, Iran: a five-year retrospective study. J Mycol Med. 2016;26(4):351–8. https://doi.org/10.1016/j.mycmed.2016.06.007.

    Article  CAS  PubMed  Google Scholar 

  6. Nweze EI, Eke IE. Dermatophytes and dermatophytosis in the eastern and southern parts of Africa. Med Mycol. 2018;56(1):13–28. https://doi.org/10.1093/mmy/myx025.

    Article  CAS  PubMed  Google Scholar 

  7. Qiangqiang Z, Limo Q, Qixian Q. Case report. Disseminated tinea of the verrucous type due to epidermophyton floccosum. Mycoses. 2001;44(7–8):326–9.

    Article  CAS  PubMed  Google Scholar 

  8. Mary ES, Mark GT. Invasive disease due to Epidermophyton floccosum in an immunocompromised patient with Behçet’s syndrome. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 1997;25(1):153–4.

    Article  Google Scholar 

  9. Rivera ZS, Losada L, Nierman WC. Back to the future for dermatophyte genomics. MBio. 2012. https://doi.org/10.1128/mBio.00381-12.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Burmester A, Shelest E, Glöckner G, Heddergott C, Schindler S, Staib P, et al. Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol. 2011;12(1):R7. https://doi.org/10.1186/gb-2011-12-1-r7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Martinez DA, Oliver BG, Graser Y, Goldberg JM, Li W, Martinez-Rossi NM, et al. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. MBio. 2012;3(5):e00259-12. https://doi.org/10.1128/mBio.00259-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Zhan P, Dukik K, Li D, Sun J, Stielow JB, Gerrits van den Ende B, et al. Phylogeny of dermatophytes with genomic character evaluation of clinically distinct Trichophyton rubrum and T. violaceum. Stud Mycol. 2018;89:153–75. https://doi.org/10.1016/j.simyco.2018.02.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hsueh YP, Heitman J. Orchestration of sexual reproduction and virulence by the fungal mating-type locus. Curr Opin Microbiol. 2008;11(6):517–24. https://doi.org/10.1016/j.mib.2008.09.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Metin B, Heitman J. Sexual reproduction in dermatophytes. Mycopathologia. 2017;182(1–2):45–55. https://doi.org/10.1007/s11046-016-0072-x.

    Article  CAS  PubMed  Google Scholar 

  15. Restrepo CM, Llanes A, Lleonart R. Use of AFLP for the study of eukaryotic pathogens affecting humans. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2018;63:360–9. https://doi.org/10.1016/j.meegid.2017.09.017.

    Article  CAS  Google Scholar 

  16. Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–89. https://doi.org/10.1101/gr.1224503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. https://doi.org/10.1093/nar/gkh340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. https://doi.org/10.1093/sysbio/syq010.

    Article  CAS  PubMed  Google Scholar 

  19. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England). 2012;28(23):3150–2. https://doi.org/10.1093/bioinformatics/bts565.

    Article  CAS  Google Scholar 

  20. Nielsen H. Predicting Secretory Proteins With SignalP. Methods Mol Biol (Clifton, NJ). 2017;1611:59–73. https://doi.org/10.1007/978-1-4939-7015-5_6.

    Article  CAS  Google Scholar 

  21. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80. https://doi.org/10.1006/jmbi.2000.4315.

    Article  CAS  PubMed  Google Scholar 

  22. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol. 2004;337(2):243–53. https://doi.org/10.1016/j.jmb.2004.01.025.

    Article  CAS  PubMed  Google Scholar 

  23. Mercer DK, Stewart CS. Keratin hydrolysis by dermatophytes. Med Mycol. 2019;57(1):13–22. https://doi.org/10.1093/mmy/myx160.

    Article  CAS  PubMed  Google Scholar 

  24. Makimura K, Murayama SY, Yamaguchi H. Detection of a wide range of medically important fungi by the polymerase chain reaction. J Med Microbiol. 1994;40(5):358–64. https://doi.org/10.1099/00222615-40-5-358.

    Article  CAS  PubMed  Google Scholar 

  25. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995;23(21):4407–14. https://doi.org/10.1093/nar/23.21.4407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gao Y, Zhan P, Hagen F, Menken SBJ, Sun J, Rezaei-Matehkolaei A, et al. Molecular epidemiology and in vitro antifungal susceptibility of Trichophyton schoenleinii, agent of tinea capitis favosa. Mycoses. 2019;62(5):466–74. https://doi.org/10.1111/myc.12889.

    Article  CAS  PubMed  Google Scholar 

  27. Kosanke S, Hamann L, Kupsch C, Moreno Garcia S, Chopra A, Gräser Y. Unequal distribution of the mating type (MAT) locus idiomorphs in dermatophyte species. Fungal Genet Biol FG B. 2018;118:45–53. https://doi.org/10.1016/j.fgb.2018.07.003.

    Article  CAS  PubMed  Google Scholar 

  28. Gastebois A, Fontaine T, Latgé JP, Mouyna I. beta(1–3)Glucanosyltransferase Gel4p is essential for Aspergillus fumigatus. Eukaryot Cell. 2010;9(8):1294–8. https://doi.org/10.1128/ec.00107-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kamei M, Yamashita K, Takahashi M, Fukumori F, Ichiishi A, Fujimura M. Deletion and expression analysis of beta-(1,3)-glucanosyltransferase genes in Neurospora crassa. Fungal Genet Biol FG & B. 2013;52:65–72. https://doi.org/10.1016/j.fgb.2012.12.001.

    Article  CAS  Google Scholar 

  30. Alshahni MM, Yamada T, Yo A, Murayama SY, Kuroda M, Hoshino Y, et al. Insight into the draft whole-genome sequence of the dermatophyte Arthroderma vanbreuseghemii. Sci Rep. 2018;8(1):15127. https://doi.org/10.1038/s41598-018-33505-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Muszewska A, Taylor JW, Szczesny P, Grynberg M. Independent subtilases expansions in fungi associated with animals. Mol Biol Evol. 2011;28(12):3395–404. https://doi.org/10.1093/molbev/msr176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Chen J, Yi J, Liu L, Yin S, Chen R, Li M, et al. Substrate adaptation of Trichophyton rubrum secreted endoproteases. Microb Pathog. 2010;48(2):57–61. https://doi.org/10.1016/j.micpath.2009.12.001.

    Article  CAS  PubMed  Google Scholar 

  33. Descamps F, Brouta F, Monod M, Zaugg C, Baar D, Losson B, et al. Isolation of a Microsporum canis gene family encoding three subtilisin-like proteases expressed in vivo. J Investig Dermatol. 2002;119(4):830–5. https://doi.org/10.1046/j.1523-1747.2002.01784.x.

    Article  CAS  PubMed  Google Scholar 

  34. Baldo A, Mathy A, Tabart J, Camponova P, Vermout S, Massart L, et al. Secreted subtilisin Sub3 from Microsporum canis is required for adherence to but not for invasion of the epidermis. Br J Dermatol. 2010;162(5):990–7. https://doi.org/10.1111/j.1365-2133.2009.09608.x.

    Article  CAS  PubMed  Google Scholar 

  35. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, Stulemeijer IJ, et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol. 2008;69(1):119–36. https://doi.org/10.1111/j.1365-2958.2008.06270.x.

    Article  CAS  PubMed  Google Scholar 

  36. de Jonge R, Thomma BP. Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol. 2009;17(4):151–7. https://doi.org/10.1016/j.tim.2009.01.002.

    Article  CAS  PubMed  Google Scholar 

  37. Kar B, Patel P, Free SJ. Trichophyton rubrum LysM proteins bind to fungal cell wall chitin and to the N-linked oligosaccharides present on human skin glycoproteins. PLoS ONE. 2019;14(4):e0215034. https://doi.org/10.1371/journal.pone.0215034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Persinoti GF, Martinez DA, Li W, Döğen A, Billmyre RB, Averette A, et al. Whole-genome analysis illustrates global clonal population structure of the ubiquitous dermatophyte pathogen Trichophyton rubrum. Genetics. 2018;208(4):1657–69. https://doi.org/10.1534/genetics.117.300573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ansari S, Ahmadi B, Norouzi M, Ansari Z, Afsarian MH, Lotfali E, et al. Epidermophyton floccosum: nucleotide sequence analysis and antifungal susceptibility testing of 40 clinical isolates. J Med Microbiol. 2019;68(11):1655–63. https://doi.org/10.1099/jmm.0.001074.

    Article  CAS  PubMed  Google Scholar 

  40. Khosravi A, Behzad F, Sabokbar A, Shokri H, Haddadi S, Masoudi-Nejad A. Molecular typing of Epidermophyton floccosum isolated from patients with dermatophytosis by RAPD-PCR. J Basic Microbiol. 2010;50(Suppl 1):S68-73. https://doi.org/10.1002/jobm.201000089.

    Article  PubMed  Google Scholar 

  41. De Baere T, Summerbell R, Theelen B, Boekhout T, Vaneechoutte M. Evaluation of internal transcribed spacer 2-RFLP analysis for the identification of dermatophytes. J Med Microbiol. 2010;59(Pt 1):48–54. https://doi.org/10.1099/jmm.0.013870-0.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by The National Natural Science Foundation of China (No. 81972949), the Scientific and Technological Innovation Projects of Medicine and Health of Chinese Academy of Medical Sciences (No. 2016-I2M-3-021), the Nanjing Incubation Program for National Clinical Research Center (No. 2019060001) and the Basical Scientific Research Fund Projects of Chinese Academy of Medical Sciences (No. 2018PT31013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weida Liu.

Ethics declarations

Conflict of interest

The authors declare that they have on conflict of interest.

Additional information

Handling Editor: Vishnu Chaturvedi

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Ge, L., Mei, H. et al. Comparative Genomics and Molecular Analysis of Epidermophyton floccosum. Mycopathologia 186, 487–497 (2021). https://doi.org/10.1007/s11046-021-00567-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-021-00567-9

Keywords

Navigation