Skip to main content
SpringerLink
Log in

Intraspecific Diversity and Taxonomy of Emmonsia crescens

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

Abstract

Emmonsia crescens is known as an environmental pathogen causing adiaspiromycosis in small rodents. As the generic name Emmonsia is no longer available for this species, its taxonomic position is re-evaluated. The intraspecific variation of Emmonsia crescens was analyzed using molecular, morphological, and physiological data, and the relationship between frequency of adiaspiromycosis and body temperature of host animals was explored. A North American and a pan-global lineage could be discerned, each with subclusters at low genetic distance. European strains produced the classical type of very large adiaspores, while in the North American lineage adiaspores relatively small, resembling the broad-based budding cells of Blastomyces. Members of the closely related genus Emergomyces may exhibit large, broad-based in addition to small, narrow-based budding cells. We conclude that the morphology of the pathogenic phase in these fungi differs gradationally between species and even populations, and is therefore less suitable as a diagnostic criterion for generic delimitation. Two Emmonsia species are reclassified in Emergomyces.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AFLP:

Amplified fragment length polymorphism

BCP-MS-G:

Bromocresol purple-milk solids-glucose

E.:

Emmonsia

Hd:

Haplotype diversity

IA:

Indexes of association

ITS:

Internal transcribed spacer regions

LSU:

Large subunit rDNA

ML:

Maximum likelihood

rPB2 :

RNA polymerase II

SNP:

Single nucleotide polymorphism

TEF3 :

Translation elongation factor 3-α

TUB2 :

β-Tubulin

TOTM:

Tween 80 opacity test medium

References

  1. Ciferri R, Montemartini A. Taxonomy of Haplosporangium parvum. Mycopath Mycol Appl. 1959;10:303–16.

    Article  CAS  Google Scholar 

  2. Emmons CW, Jellison WL. Emmonsia crescens sp. n. and adiaspiromycosis (haplomycosis in mammals). Ann NY Acad Sci. 1960;89:91–101.

    Article  CAS  Google Scholar 

  3. Sigler L. Adiaspiromycosis and other infections caused by Emmonsia species. In: Hodder A, editor. Topley & Wilson’s microbiology and microbial. 10th ed. London: Wiley; 2005. p. 809–24.

    Google Scholar 

  4. Dvořak J, Otčenašek M, Rosicky B. Adiaspiromycosis caused by Emmonsia crescens, Emmons and Jellison 1960. Studie ČSAV (Acad Praha). 1973;14:1–120.

    Google Scholar 

  5. Jiang Y, Dukik K, Muñoz JF, Sigler L, Schwartz IS, Govender NP, et al. Phylogeny, ecology and taxonomy of systemic pathogens and their relatives in Ajellomycetaceae (Onygenales): Blastomyces, Emergomyces, Emmonsia, Emmonsiellopsis. Fung Divers. 2018;90:245–91. https://doi.org/10.1007/s13225-018-0403-y.

    Article  Google Scholar 

  6. Schwartz IS, McLoud JD, Berman D, Botha A, Lerm B, Colebunders R, et al. Molecular detection of airborne Emergomyces africanus, a thermally dimorphic fungal pathogen, in Cape Town, South Africa. PLoS Negl Trop Dis. 2018;12(1):e0006174. https://doi.org/10.1371/journal.pntd.0006174.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Schwartz IS, Lerm B, Hoving JC, Kenyon C, Horsnell WG, Basson WJ, et al. Emergomyces africanus in soil, South Africa. Emerg Infect Dis. 2018;24:377–80. https://doi.org/10.3201/eid2402.171351.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Cronjé N, Schwartz IS, Retief L, Bastos ADS, Matthee S, Preiser W, et al. Attempted molecular detection of the thermally dimorphic human fungal pathogen Emergomyces africanus in terrestrial small mammals in South Africa. Med Mycol. 2018;56:510–3. https://doi.org/10.1093/mmy/myx065.

    Article  PubMed  Google Scholar 

  9. Seyedmousavi S, de Hoog GS, Guillot J, Verweij PE. Emerging and epizootic fungal infections in animals. Cham: Springer; 2018.

    Book  Google Scholar 

  10. Hubálek Z, Nesvadbová J, Halouzka J. Emmonsiosis of rodents in an agroecosystem. Med Mycol. 1998;36:387–90.

    Article  Google Scholar 

  11. Borman AM, Simpson VR, Palmer MD, Linton CJ, Johnson EM. Adiaspiromycosis due to Emmonsia crescens is widespread in native British mammals. Mycopathologia. 2009;168:153–63. https://doi.org/10.1007/s11046-009-9216-6.

    Article  PubMed  Google Scholar 

  12. Sigler L. Agents of adiaspiromycosis. 1998; p. 571–583. In L. Ajello and R. Hay (ed.), Topley & Wilson’s microbiology and microbial infections, 9th edn, vol. 4. London: Arnold.

  13. Danesi P, Falcaro C, Dukik K, Jiang Y, Rizzoli AP, Allavena R, et al. Molecular diagnosis of Emmonsia-like fungi occurring in wild animals. Mycopathologia. 2019. https://doi.org/10.1007/s11046-019-00353-8.

    Article  PubMed  Google Scholar 

  14. Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B. Food and indoor fungi. Utrecht: CBS KNAW Biodiversity Center; 2010.

    Google Scholar 

  15. Slifkin M. Tween 80 opacity test responses of various Candida species. J Clin Microbiol. 2000;38:4626–8.

    Article  CAS  Google Scholar 

  16. Fischer JB, Kane J. The detection of contamination in Trichophyton rubrum and Trichophyton mentagrophytes. Mycopathologia. 1971;43:169–80.

    CAS  Google Scholar 

  17. Summerbell RC, Rosenthal SA, Kane J. Rapid method for differentiation of Trichophyton rubrum, Trichophyton mentagrophytes, and related dermatophyte species. J Clin Microbiol. 1988;26:2279–82.

    Article  CAS  Google Scholar 

  18. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9. https://doi.org/10.1093/molbev/msr121.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Stamatakis A. RaxML version 8: a tool for phylogenetic analysis and post analysis of large phylogenies. Bioinformatics. 2014;30:1312–3. https://doi.org/10.1093/bioinformatics/btu033.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Ramos-Onsins SE, Sánchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.

    Article  CAS  Google Scholar 

  21. Agapow P, Burt A. Indices of multilocus linkage disequilibrium. Mol Ecol Notes. 2001;1:101–2. https://doi.org/10.1046/j.1471-8278.2000.00014.x.

    Article  CAS  Google Scholar 

  22. Smith JM, Smith NH, O’Rourke M, Spratt BG. How clonal are bacteria? Proc Nat Acad Sci USA. 1993;90:4384–8.

    Article  CAS  Google Scholar 

  23. Su H, Packeu A, Ahmed SA, Al-Hatmi AMS, Blechert O, İlkit M, et al. Species distinction in the Trichophyton rubrum complex. J Clin Microbiol. 2019;57(9):e00352-19. https://doi.org/10.1128/jcm.00352-19.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Hubálek Z. Emmonsiosis of wild rodents and insectivores in Czechland. J Wildl Dis. 1999;35:243–9. https://doi.org/10.7589/0090-3558-35.2.243.

    Article  PubMed  Google Scholar 

  25. Mörner T, Avenäs A, Mattsson R. Adiaspiromycosis in a European beaver from Sweden. J Wildl Dis. 1999;35:367–70. https://doi.org/10.7589/0090-3558-35.2.367.

    Article  PubMed  Google Scholar 

  26. Simpson VR, Gavier-Widen D. Fatal adiaspiromycosis in a wild Eurasian otter (Lutra lutra). Vet Rec. 2000;147:239–41. https://doi.org/10.1136/vr.147.9.239.

    Article  PubMed  CAS  Google Scholar 

  27. Hughes K, Borman AM. Adiaspiromycosis in a wild European rabbit, and a review of the literature. J Vet Diagn Investig. 2018;30:614–8. https://doi.org/10.1177/1040638718772631.

    Article  Google Scholar 

  28. Chantrey JC, Borman AM, Johnson EM, Kipar A. Emmonsia crescens infection in a British water vole (Arvicola terrestris). Jpn J Med Mycol. 2006;44:375–8. https://doi.org/10.1080/13693780500354222.

    Article  Google Scholar 

  29. Seixas F, Travassos P, Pinto ML, Pires I, Pires MA. Pulmonary adiaspiromycosis in a European hedgehog (Erinaceus europaeus) in Portugal. Vet Rec. 2006;158:274–5. https://doi.org/10.1136/vr.158.8.274.

    Article  PubMed  CAS  Google Scholar 

  30. Malatesta D, Simpson VR, Fontanesi L, Fusillo R, Marcelli M, Bongiovanni L, et al. First description of adiaspiromycosis in an Eurasian otter (Lutra lutra) in Italy. Vet Italy. 2014;50:199–202. https://doi.org/10.12834/VetIt.40.1916.8.

    Article  Google Scholar 

  31. Morandi F, Galuppi R, Buitrago MJ, Delogu M, Lowenstine LJ, Panarese S, et al. Disseminated pulmonary adiaspiromycosis in a crested porcupine (Hystrix cristata Linnaeus, 1758). J Wildl Dis. 2012;48:523–5. https://doi.org/10.7589/0090-3558-48.2.523.

    Article  PubMed  Google Scholar 

  32. Dolka I, Gizejewska A, Gizejewski Z, Kołodziejska-Lesisz J, Klucinski W. Pulmonary adiaspiromycosis in the Eurasian beaver (Castor fiber) inhabiting Poland. Pol J Vet Sci. 2017;20:615–7. https://doi.org/10.1515/pjvs-2017-0077.

    Article  PubMed  CAS  Google Scholar 

  33. Hubálek Z, Burda H, Scharff A, Heth G, Nevo E, Sumbera R, et al. Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel. Med Mycol. 2005;43:691–7. https://doi.org/10.1080/13693780500179553.

    Article  PubMed  Google Scholar 

  34. Kim TH, Han JH, Chang SN, Kim DS, Abdelkader TS, Seok SH, et al. Adiaspiromycosis of an Apodemus agrarius captured wild rodent in Korea. Lab Anim Res. 2012;28:67–9. https://doi.org/10.5625/lar.2012.28.1.67.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Matsuda K, Niki H, Yukawa A, Yanagi M, Souma K, Masuko T, et al. First detection of adiaspiromycosis in the lungs of a deer. J Vet Med Sci. 2015;77:981–3. https://doi.org/10.1292/jvms.15-0083.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Johnstone AC, Hussein HM, Woodgyer A. Adiaspiromycosis in suspected cases of pulmonary tuberculosis in the common brushtail possum (Trichosurus vulpecula). N Z Vet J. 1993;41:175–8. https://doi.org/10.1080/00480169.1993.35765.

    Article  PubMed  CAS  Google Scholar 

  37. Albassam MA, Bhatnagar R, Lillie LE, Roy L. Adiaspiromycosis in striped skunks in Alberta, Canada. J Wildl Dis. 1986;22:13–8. https://doi.org/10.7589/0090-3558-22.1.13.

    Article  PubMed  CAS  Google Scholar 

  38. Peterson SW, Sigler L. Molecular genetic variation in Emmonsia crescens and Emmonsia parva, etiologic agents of adiaspiromycosis, and their phylogenetic relationship to Blastomyces dermatitidis (Ajellomyces dermatitidis) and other systemic fungal pathogens. J Clin Microbiol. 1998;36:2918–25.

    Article  CAS  Google Scholar 

  39. Sigler L. Ajellomyces crescens sp. nov., taxonomy of Emmonsia spp., and relatedness with Blastomyces dermatitidis (teleomorph Ajellomyces dermatitidis). J Med Vet Mycol. 1996;34(5):303–14.

    Article  CAS  Google Scholar 

  40. Boily P. Individual variation in metabolic traits of wildnine-banded armadillos (Dasypus novemcinctus), and theaerobic capacity model for the evolution of endothermy. J Exp Biol. 2002;205:3207–14.

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Lynne Sigler, Edmonton, Canada, for constructive discussions, and Xinlei Fan from Beijing Forestry University, and Bingbing Zhang, School of Public Health, Guizhou Medical University, for their important contributions to the methodology and statistical analysis.

Funding

This work was supported by the District science foundation program (NSFC No. 81960368) from National Natural Science Foundation of China.

Author information

Authors and Affiliations

  1. Department of Dermatology, The Affiliated Hospital, Guizhou Medical University, Guiyang, China

    Y. Jiang & H. Lu

  2. Center of Expertise in Mycology of Radboud University Medical Center/Canisius Wilhelmina Hospital, Nijmegen, The Netherlands

    Y. Jiang, S. A. Ahmed, P. E. Verweij & G. S. de Hoog

  3. Department of Pathology, Sidra Medicine, Doha, Qatar

    C. K. M. Tsui

  4. Department of Pathology and Laboratory Medicine, Weill Cornell Medicine-Qatar, Doha, Qatar

    C. K. M. Tsui

  5. Division of Infectious Diseases, Faculty of Medicine, University of British Columbia, Vancouver, Canada

    C. K. M. Tsui

  6. Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands

    F. Hagen & A. H. G. Gerrits van den Ende

  7. Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, The Netherlands

    F. Hagen

  8. Laboratory of Medical Mycology, Jining No. 1 People’s Hospital, Jining, Shandong, China

    F. Hagen

  9. Department of Immunology, Basic Medical School, Guizhou Medical University, Guiyang, China

    Z. Shang

Authors
  1. Y. Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. K. M. Tsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. A. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Hagen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Z. Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. H. G. Gerrits van den Ende
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. E. Verweij
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. H. Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. G. S. de Hoog
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YJ carried out the literature search, strains collection, DNA extraction and sequencing, phylogenetic tree construction, physiology tests, participated in the data analysis and drafted the manuscript. CT performed the genetic data and split tree analysis and interpretation, contributed to the discussion and revision of the manuscript. SA performed the haplotype data analysis. FH and BGVDE carried out the AFLP data analysis interpretation. ZS carried out the statistical analysis. YJ, HL, PEV and SdH participated in the design of the study, statistical analysis and manuscript revision and review. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Y. Jiang or H. Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Abdullah Mohammed Said Al-Hatmi.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, Y., Tsui, C.K.M., Ahmed, S.A. et al. Intraspecific Diversity and Taxonomy of Emmonsia crescens. Mycopathologia 185, 613–627 (2020). https://doi.org/10.1007/s11046-020-00475-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-020-00475-4

Keywords

Search

Navigation