Skip to main content
SpringerLink
Log in

Parengyodontium album Isolated from Cutaneous Lesions of a Pacific White-Sided Dolphin (Lagenorhynchus obliquidens) During Treatment for Paracoccidioidomycosis Ceti

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

Abstract

The prominence of seafood in Japan motivates close monitoring of its seas and marine lives for potentially pathogenic fungi. During the treatments of the male Pacific white-sided dolphin (Lagenorhynchus obliquidens) for paracoccidioidomycosis ceti (PCM-C), 5 white and floccose colonies showing identical genotype and morphological characteristics were isolated from two skin biopsy samples of cutaneous granulomatous lesions in 2018. The isolates were identified as Parengyodontium album known as one of fungal species having abilities to produce industrially important proteases, and to become a causative agent for emerging mycosis based on morphological and molecular biological characteristics. These lesions consisted of non-malignant pearl-like structures of hyperplastic keratinocytes. Interestingly, although the isolates could grow at 35 °C, their DNA sequences were phylogenetically located in a cluster consisting of environmental and clinical isolates lacking the ability to grow at 35 °C, based on previous reports. The opportunistic infection we observed in the dolphin might be caused by immune disorder due to PCM-C. Notably, although P. album is recognized as non-harmful, and has significant industrial importance and antitumor activity, it has potential to cause not only superficial but also systemic infection, and presents difficulties in treatment because of its high resistance to antifungal compounds.

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

Similar content being viewed by others

References

  1. Vilela R. Mendoza: 9. Paracoccidioidomycosis ceti (Lacaziosis/Lobomycosis) in Dolphins. In: Seyedmousavi S, de Hoog GS, Guillot J, Verweij PE, editors. Emerging and epizootic fungal infections in animals. Switzerland: Springer; 2018. p. 177–92.

    Chapter  Google Scholar 

  2. Ueda K, Sano A, Yamate J, Itano EN, Kuwamura M, Izawa T, Tanaka M, Hasegawa Y, Chibana H, Izumisawa Y, Miyahara H, Uchida S. Two cases of lacaziosis in bottlenose dolphins (Tursiops truncatus) in Japan. Case Rep Vet Med. 2013;2013:9.

    Google Scholar 

  3. Bossart GD, Romano TA, Peden-Adams MM, Schaefer AM, Rice CD, Fair PA, Reif JS. Comparative innate and adaptive immune responses in Atlantic bottlenose dolphins (Tursiops truncatus) with viral, bacterial, and fungal infections. Front Immunol. 2019;10:1125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Huhn FO, Stock G. Bericht über eine fadenpilz-granulomatose der mamma als differential diagnostischer beitrag zum bild eines “inflammatorischen karzinoms”. Geburtshilfe Frauenheilkd. 1977;37:692–7.

    CAS  PubMed  Google Scholar 

  5. Seeliger HPR. Infections of man by opportunistic molds-their identification and nomenclature of their diseases. Mycoses. 1983;26:587–98.

    Article  CAS  Google Scholar 

  6. de Hoog GS. The genera Beauveria, Isaria, Tritirachium and Acrodontium gen. nov. Stud Mycol. 1972;1:1–41.

    Google Scholar 

  7. Augustinsky J, Kammeyer P, Husain A, et al. Engyodontium album endocarditis. J Clin Microbiol. 1990;28:1479–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Balasingham S, Chalkias S, Aetal B. A case of bovine valve endocarditis caused by Engyodontium album. Med Mycol. 2011;49:430–4.

    Article  PubMed  Google Scholar 

  9. Macêdo DPC, Neves RP, de Souza-Motta CM, Magalhães OMC. Engyodontium album fungaemia: the first reported case. Braz J Microbiol. 2007;38:110–2.

    Article  Google Scholar 

  10. Thamke DC, Mendiratta DK, Dhabarde A, Shukla AK. Mycotic keratitis due to Engyodontium album: first case report from India. Indian J Med Microbiol. 2015;33:303–4.

    Article  CAS  PubMed  Google Scholar 

  11. McDonnell PJ, Werblin TP, Sigler L, Greem WR. Mycotic keratitis due to Beauveria alba. Cornea. 1984;3:213–6.

    Article  PubMed  Google Scholar 

  12. Tsang C-C, Chan JFW, Pong WM, Chen JHK, Nagan AHY, Cheung M, Lai CKC, Tsang DNC, Lau SKP, Woo PC. Cutaneous hyalohyphomycosis due to Parengyodontium album gen. et comb. nov. Med Mycol. 2016;54:699–713.

    Article  CAS  PubMed  Google Scholar 

  13. Chellappan S, Jasmin C, Basheer SM, Elyas KK, Bhat SG, Chandrasekaran M. Production, purification and partial characterization of a novel protease from marine Engyodontium album BTMFS10 under solid state fermentation. Process Biochem. 2005. https://doi.org/10.1016/j.procbio.2005.10.017.

    Article  Google Scholar 

  14. Anaya-Eugenio GD, Rebollar-Ramos D, González MDC, Raja H, Mata R, de Carcache BEJ. Apoptotic activity of xanthoquinodin JBIR-99, from Parengyodontium album MEXU 30054, in PC-3 human prostate cancer cells. Chem Biol Interact. 2019. https://doi.org/10.1016/j.cbi.2019.108798.

    Article  PubMed  Google Scholar 

  15. Alil I, Rakshit SK, Siwarungson N, Punnapayak H, Lotrakul P, Prasongsuk S, Akbar A, Rehman ZU. Identification and phylogenetic analysis of halophilic fungus isolated from a man-made solar saltern in Thailand. Lasbela Univ J Sci Technol. 2013;2:47–52.

    Google Scholar 

  16. Minakawa T, Ueda K, Sano A, Kamisako H, Iwanaga M, Komine T, Wada S. A Suspected case of paracoccidioidomycosis ceti in a male aquarium-maintained Pacific white-sided dolphin (Lagenorhynchus obliquidens) in Japan. Jap J Zoo Wildlife Med. 2018;23:45–50.

    Article  Google Scholar 

  17. Sano A, Tanaka R, Nishimura K, Kurokawa CS, Coelho KLR, Franco M, Montenegro MR, Miyaji M. Characteristics of 17 Paracoccidioides brasiliensis isolates. Mycoscience. 1997;38:117–22.

    Article  Google Scholar 

  18. Schocha CL, Seifertb KA, Huhndorfc S, Robertd V, Spougea JL, Levesqueb CA, Chenb W. Fungal Barcoding Consortiuma: Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. PNAS. 2012;109:6241–6.

    Article  Google Scholar 

  19. Murata Y, Sano A, Ueda Y, Inomata T, Takayama A, Poonwan N, Nanthawan M, Mikami Y, Miyaji M, Nishimura K, Kamei K. Molecular epidemiology of canine histoplasmosis in Japan. Med Mycol. 2007;45:233–47.

    Article  CAS  PubMed  Google Scholar 

  20. White TJ, Bruns T, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MH, Gelfand DH, Shinsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego, CA: Academic Press; 1990. p. 315–22.

    Google Scholar 

  21. Komori T, Sano A, Yarita K, Kitagawa T, Kamei K, Nishimura K. Phylogenetic analysis of Histoplasma capsulatum based on partial sequence of the D1/D2 region of the 28S rRNA gene. Nippon Ishinkin Gakkai Zasshi. 2005;46:291–5.

    Article  CAS  Google Scholar 

  22. Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Suska A, Tanney JB, Kocsube S, Szigeti G, Yaguchi T, Frisvad JC. Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology. 2014;78:141–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. CLSI Document M38-A2. Wayne: Clinical and Laboratory Standards Institute; 2008.

  25. Ueda K, Nakamura I, Itano EN, Takemura K, Nakazato Y, Sano A. Trichosporon asteroides Isolated from cutaneous lesions of a suspected case of “paracoccidioidomycosis ceti” in a bottlenose dolphin (Tursiops truncatus). Mycopathologia. 2017;182:937–46.

    Article  CAS  PubMed  Google Scholar 

  26. Tanaka M, Izawa T, Kuwamura M, Nakao T, Maezono Y, Ito S, Murata M, Murakami M, Sano A, Yamate J. Deep granulomatous dermatitis of the fin caused by Fusarium solani in a false killer whale (Pseudorca crassidens). J Vet Med Sci. 2012;74:779–82.

    Article  PubMed  Google Scholar 

  27. Sharmin S, Ohori A, Sano A, Kamei K, Yamaguchi M, Takeo K, Uno J, Nishimura K, Miyaji M. Histoplasma capsulatum variety duboisii isolated in Japan from an HIV-infected Ugandan patient. Jpn J Med Mycol. 2003;44:299–306.

    Article  Google Scholar 

  28. Feder V, Kmetzsch L, Staats CC, Vidal-Figueiredo N, Ligabue-Braun R, Carlini CR, Vainstein MH. Cryptococcus gattii urease as a virulence factor and the relevance of enzymatic activity in cryptococcosis pathogenesis. FEBS J. 2015;282:1406–18.

    Article  CAS  PubMed  Google Scholar 

  29. Takahashi H, Ueda K, Itano EN, Yanagisawa M, Murata Y, Murata M, Yaguchi T, Murakami M, Kamei K, Inomata T, Miyahara H, Sano A, Uchida S. Candida albicans and C. tropicalis isolates from the expired breathes of captive dolphins and their environments in an aquarium. Vet Med Int. 2010;10:62.

    Google Scholar 

  30. Brilhante RSN, Rodrigues PHA, de Alencar LC, Riello GB, Ribeiro JF, de Oliveira JS, Castelo-Branco DSCM, Bandeira TJBG, Monteiro AJ, Rocha MFG, Cordeiro RA, Moreira JLB, Sidrim JJC. Evidence of fluconazole-resistant Candida species in tortoises and sea turtles. Mycopathologia. 2015;180:421–6.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to express our sincere gratitude to Dr. Shinji Sasaki (Faculty of Agriculture, University of the Ryukyus) for the gene analysis. This research was done based on an agreement between the University of the Ryukyus and the Okinawa Churashima Foundation. We would also like to thank Editage (www.editage.jp) for English language editing.

Author information

Authors and Affiliations

  1. Faculty of Agriculture, University of the Ryukyus, Sembaru 1, Nishihara-Cho, Nakagusuku-Gun, Okinawa, 903-0213, Japan

    Hikaru Kanegae, Nanako Tomino, Yuichi Nakamura & Ayako Sano

  2. Okinawa Churashima Foundation, Aza Ishikawa 888, Motobu-Cho, Kunigami-Gun, Okinawa, 905-0206, Japan

    Tomoko Minakawa & Keiichi Ueda

  3. Medical Mycology, Research Center, Chiba University, 1-8-1, Inohana, Chuo-ku, Chiba, 260-8673, Japan

    Takashi Yaguchi

  4. Laboratory of Veterinary Pathology, Division of Veterinary Sciences, Rinku-Campus, Osaka Prefecture University, Rinku-OraiKita 1-58, Izumisano, Osaka, 598-8531, Japan

    Takeshi Izawa

  5. The United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-24 Korimoto, Kagoshima, 890-0065, Japan

    Ayako Sano

  6. Department of Pathological Science, CCB, State University of Londrina, P.O. Box 6001, Londrina, PR, 86051-970, Brazil

    Eiko Nakagawa Itano

Authors
  1. Hikaru Kanegae
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nanako Tomino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuichi Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomoko Minakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takashi Yaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takeshi Izawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ayako Sano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eiko Nakagawa Itano
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Keiichi Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Hikaru Kanegae contributed to mycological and molecular biological studies. Nanako Tomino contributed to partial mycological studies. Yuichi Nakamura contributed to molecular biological studies. Tomoko Minakawa contributed to clinical managements and evaluation of antifungal susceptibilities. Takashi Yaguchi contributed to molecular biological identification, Takeshi Izawa histopathological findings. Ayako Sano is the supervisor and corresponding author. Eiko Nakagawa Itano contributed to epidemiological discussions. Keiichi Ueda is the co-supervisor, contributed to clinical managements and has equal responsibilities to the correspondent author.

Corresponding author

Correspondence to Ayako Sano.

Ethics declarations

Conflicts of interest

None.

Additional information

Publisher's Note

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

Handling Editor: Rui Kano.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanegae, H., Tomino, N., Nakamura, Y. et al. Parengyodontium album Isolated from Cutaneous Lesions of a Pacific White-Sided Dolphin (Lagenorhynchus obliquidens) During Treatment for Paracoccidioidomycosis Ceti. Mycopathologia 185, 1021–1031 (2020). https://doi.org/10.1007/s11046-020-00484-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-020-00484-3

Keywords

Search

Navigation