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Ovchinnikov R.S., Zhigalin A.V., Gaynullina A.G., Yuzhakov A.G., Tutenkov O.Yu., Savinov V.A., Moskvitina N.S., Kapustin A.V., Laishevtcev A.I., Gulykin A.M. The role of fungi in the etiology of mass skin lesions in sables Martes zibellina L. 1758 in Tomsk region. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2023, Vol. 58, № 4, p.745-756.
(how to cite this article)

doi: 10.15389/agrobiology.2023.4.745eng

UDC: 636.934.55:591.2

Acknowledgements:
The study was carried out within the framework of the state assignments of the Ministry of Science and Higher Education of the Russian Federation (projects No. 0721-2020-00190 and No. FGUG-2022-0009), and with the support of the Russian Foundation for Basic Research (RFBR) grant No 20-04-60010 “Study of the diversity, circulation and pathogenic potential of coronaviruses in natural reservoirs on the territory of Western and Eastern Siberia"

 

THE ROLE OF FUNGI IN THE ETIOLOGY OF MASS SKIN LESIONS IN SABLES Martes zibellina L. 1758 IN TOMSK REGION

R.S. Ovchinnikov1 ✉, A.V. Zhigalin2, 3, A.G. Gaynullina1,
A.G. Yuzhakov1, O.Yu. Tutenkov2, V.A. Savinov1,
N.S. Moskvitina2, A.V. Kapustin1, A.I. Laishevtcev1, A.M. Gulykin1

1Federal Scientific Centre Skryabin and Kovalenko All-Russian Research Institute of Experimental Veterinary RAS, 24/1, Ryazanskii Prosp., Moscow, 109428 Russia, e-mail rsovchinnikov@mail.ru (✉ corresponding author), gainullinaalla@gmail.com, Anton_oskol@mail.ru, visik06@mail.ru, kapustin_andrei@mail.ru, a-laishevtsev@bk.ru, admin@viev.ru;
2National Research Tomsk State University, 36, Prosp. Lenina, Tomsk, 634056 Russia, e-mail alex-zhigalin@mail.ru, tutenkov@mail.ru, mns_k@mail.ru;
3Dagestan State University, Institute of Ecology and Sustainable Development, 43а, ul. Gadzhieva, Makhachkala, Republic of Dagestan, 367000 Russia

ORCID:
Ovchinnikov R.S. orcid.org/0000-0001-6634-9879
Savinov V.A. orcid.org/0000-0003-1891-0005
Zhigalin A.V. orcid.org/0000-0003-4661-0560
Moskvitina N.S. orcid.org/0000-0002-3425-7723
Gaynullina A.G. orcid.org/0000-0002-0545-0559
Kapustin A.V. orcid.org/0000-0003-0136-2487
Yuzhakov A.G. orcid.org/0000-0002-0426-9678
Laishevtcev A.I. orcid.org/0000-0002-5050-2274
Tutenkov O.Yu. orcid.org/0009-0003-2844-9635
Gulykin A.M. orcid.org/0000-0003-2160-4770

Final revision received July 23, 2022
Accepted February 2, 2023

Mass skin lesions in sables Martes zibellina in Siberia have been known since the 18th century, but their etiology is still not well understood. The disease affects up to 62 % of hunted sables, causing damage to the skin and causing serious economic loss. One of the versions suggests the participation of microscopic fungi in the occurrence of this dermatosis. In the present work, it was established for the first time that keratinophilic dermatophyte fungi of various species are involved in the etiology of skin disease in sables, some of which were discovered in the territory of the Russian Federation for the first time. The aim of the work was to reveal and identify clinically significant fungi in sables with clinical manifestations of skin diseases. Pathological material (hair, crusts) was taken from the affected areas of the skins of wild sables (Martes zibellina L. 1758), hunted during the 2018-2019 hunting season in various areas of the Tomsk region. A total of 28 samples of pathological material were studied. Mycological examination included a Wood's lamp test, direct microscopy of the pathological material, inoculation on mycological media, followed by identification of isolated fungal cultures. Inoculation was performed on DTM-Expert, a differential diagnostic medium for dermatophytes (FNTs VIEV RAS, Russia) and on Sabouraud medium with chloramphenicol (HiMedia Laboratories Pvt. Ltd., India). The incubation was carried out under aerobic conditions at 26-28 °C, the incubation period was up to 21 days. To study the cultural and morphological features, the cultures were re-inoculated on Sabouraud agar in Petri dishes, incubated for 10-14 days. For molecular genetic identification, isolated colonies of fungi grown on Sabouraud’s medium were selected for 10 days at 26-28 °C. DNA was isolated using the GeneJET Plant Genomic DNA Purification Kit (Thermo Fisher Scientific, USA) according to the manufacturer's instructions. The resulting DNA was used to carry out the polymerase chain reaction (PCR). Regions of the internal transcribed spacer (ITS) of the ribosomal RNA  gene were sequenced. Phylogenetic analysis of the obtained nucleotide sequences was performed using the SeqMan application (DNASTAR Lasergene v.7.1.0, https://www.dnastar.com/software/laser-gene/). Sequence alignment with those available in the GenBank database was performed using the Standard Nucleotide BLAST software package (http://www.ncbi.nlm.nih.gov/BLAST/). The resulting nucleotide sequences of particular interest were deposited to the GenBank NCBI database. When examining the affected sables, skin lesions were found, which were localized mainly in the back, waist, and sides. They were characterized by loss of guard hairs, alopecia, formation of crusts and scabs. Dark spots were often observed in the area of lesions from the side of the skin. Lesions were observed both in males and females, mainly in young animals. During visual examination, samples of pathological material were sticky bundles of hair (downy, less often guard hair) with dried crusts and scales at the base. The result of the fluorescent test with a Wood’s lamp in all samples was negative. Microscopy revealed bundles of downy hairs stuck together and a large amount of purulent debris, which made it difficult to detect fungal elements. As a result of cultural mycological analysis, 51 cultures were isolated, 18 taxa (species and genera) of fungi were identified. At the same time, keratinophilic dermatophyte fungi (Arthroderma cuniculi, Chrysosporium carmichaelii, Chrysosporium spp.) were isolated from 12 % of the samples, probably acting as etiological agents of dermatosis. Growth of dermatophytes was observed only on the DTM-Expert selective differential diagnostic medium; fast-growing non-dermatophyte fungi grew on ordinary media. Non-dermatophyte fungi with keratinolytic properties were also isolated — Scopulariopsis brevicaulis (16 %), Acremonium spp. (14 %), Aspergillus spp. (36 %), which can act as secondary opportunistic pathogens.

Keywords: pathogenic fungi, animal mycoses, dermatomycoses, dermatophytes, Arthroderma, Chrysosporium, Martes zibellina, sable.

 

REFERENCES

  1. Seyedmousavi S., Bosco S.D.M., De Hoog S., Ebel F., Elad D., Gomes R.R., Jacobsen I.D., Jensen H.E., Martel A., Mignon B., Pasmans F., Piecková E., Rodrigues A.M., Singh K., Vicente V.A., Wibbelt G., Wiederhold N.P., Guillot J. Fungal infections in animals: a patchwork of different situations. Medical Mycology,2018, 56(suppl_1): S165-S187 CrossRef
  2. James T.Y., Toledo L.F., Rödder D., da Silva Leite D., Belasen A.M., Betancourt-Román C.M., Jenkinson T.S., Soto-Azat C., Lambertini C., Longo A.V., Ruggeri J., Collins J.P., Burrowes P.A., Lips K.R., Zamudio K.R., Longcore J.E. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution, 2015, 5(18): 4079-4097 CrossRef
  3. Hoyt J.R., Kilpatrick A.M., Langwig K.E. Ecology and impacts of white-nose syndrome on bats. Nature Reviews Microbiology, 2021, 19(3): 196-210 CrossRef
  4. Davy C.M., Shirose L., Campbell D., Dillon R, McKenzie C., Nemeth N., Braithwaite T., Cai H., Degazio T., Dobbie T., Egan S., Fotherby H., Litzgus J. D., Manorome P., Marks S., Paterson J. E., Sigler L., Slavic D., Slavik E., Urquhart J., Jardine C. Revisiting ophidiomycosis (snake fungal disease) after a decade of targeted research. Frontiers in Veterinary Science, 2021, 8: 665805 CrossRef
  5. Ross A.A., Rodrigues Hoffmann A., Neufeld J.D. The skin microbiome of vertebrates. Microbiome, 2019, 7: 79 CrossRef
  6. Williams C.L., Caraballo-Rodríguez A.M., Allaband C., Zarrinpar A., Knight R., Gauglitz J.M. Wildlife-microbiome interactions and disease: exploring opportunities for disease mitigation across ecological scales. Drug Discovery Today: Disease Models, 2018, 28: 105-115 CrossRef
  7. Anstead G.M., Sutton D.A., Graybill J.R. Adiaspiromycosis causing respiratory failure and a review of human infections due to Emmonsia and Chrysosporium spp. Journal of Clinical Microbiology, 2012, 50(4): 1346-1354 CrossRef
  8. Schwartz I.S., Kenyon C., Feng P., Govender N.P., Dukik K., Sigler L., Jiang Y., Stielow J.B., Muñoz J.F., Cuomo C.A., Botha A., Stchigel A.M., de Hoog G.S. 50 years of emmonsia disease in humans: the dramatic emergence of a cluster of novel fungal pathogens. PLoS Pathogens, 2015, 11(11): e1005198 CrossRef
  9. Losnak D.O., Rocha F.R., Almeida B.S., Batista K.Z.S., Althoff S.L., Haupt J., Ruiz L.S., Anversa L., Lucheis S.B., Paiz L.M., Donalisio M.R., Richini Pereira V.B. Molecular detection of fungi of public health importance in wild animals from Southern Brazil. Mycoses, 2018, 61(7): 455-463 CrossRef
  10. Stepanenko N.D. Kozhnoe zabolevanie soboley v prirodnykh usloviyakh [Skin disease of sables in nature]. Kirov, 2007 (in Russ.).
  11. Tyuten’kov O.Yu., Sokolova N.M., Trifonova M.G. Teriofauna Rossii i sopredel’nykh territoriy: mezhdunarodnoesoveshchanie: Khs»ezdTeriologicheskogoobshchestva pri RAN [Theriofauna of Russia and adjacent territories: international meeting: X Congress of the theriological society of the Russian Academy of Sciences]. Moscow, 2016: 433 (in Russ.).
  12. de Hoog G.S., Guarro J., Gené J., Figueras M.J. Atlas of clinical fungi. CBS, Utrecht, 2000.
  13. Anbu P., Gopinath S.C.B., Hilda A., Mathivanan N., Annadurai G. Secretion of keratinolytic enzymes and keratinolysis by Scopulariopsis brevicaulis and Trichophyton mentagrophytes: regression analysis. Canadian Journal of Microbiology, 2006, 52(11): 1060-1069 CrossRef
  14. Tosti A., Piraccini B., Stinchi C., Lorenzi S. Onychomycosis due to Scopulariopsis brevicaulis: clinical features and response to systemic antifungals. The British Journal of Dermatology, 1996, 135(5): 799-802 CrossRef
  15. Manoyan M.G., Ovchinnikov R.S. Tezisy dokladov «Sovremennaya mikologiya v Rossii: Pervyy s»ezd mikologov Rossii» [Abstracts of reports «Modern mycology in Russia: the first congress of mycologists of Russia»]. Moscow, 2002: 414-415 (in Russ.).
  16. Rodrigues Marcondes N., Ledesma Taira C., Cirena Vandresen D., Estivalet Svidzinski T.I., Kadowaki M.K., Peralta R.M. New feather-degrading filamentous fungi. Microbial Ecology, 2008, 56(1): 13-17 CrossRef
  17. Perdomo H., Sutton D.A. García D., Fothergill A.W., Cano J., Gené J., Summerbell R.C., Rinaldi M.G., Guarro J. Spectrum of clinically relevant Acremonium species in the United States. Journal of Clinical Microbiology, 2011, 49(1): 243-256 CrossRef
  18. Hainsworth S., Kučerová I., Sharma R., Cañete-Gibas C.F., Hubka V. Three-gene phylogeny of the genus Arthroderma: basis for future taxonomic studies. Medical Mycology, 2021, 59(4): 355-365. CrossRef
  19. Dawson C.O. Two new species of Arthroderma isolated from soil from rabbit burrows. Sabouraudia, 1963, 2(3): 185-191 CrossRef
  20. Baumbach C.M., Müller S., Reuschel M., Uhrlaß S., Nenoff P., Baums C.G., Schrödl W. Identification of zoophilic dermatophytes using MALDI-TOF mass spectrometry. Frontiers in Cellular and Infection Microbiology, 2021, 11: 631681 CrossRef
  21. Zaki S.M., Mikami Y., El-Din A.A.K., Youssef Y.A. Keratinophilic fungi recovered from muddy soil in Cairo Vicinities, Egypt. Mycopathologia, 2005, 160(3): 245-251 CrossRef
  22. Ovchinnikov R.S., Vasyliev D.B. Pathogenic chrysosporium-related fungi in reptiles and other animals. In: Recent trends in human and animal mycology. K. Singh, N. Srivastava (eds.). Springer, Singapore, 2019: 47-80 CrossRef
  23. Savinov V.A., Ovchinnikov R.S., Kapustin A.V., Laishevtcev A.I., Gulykin A.M. Development of a differential diagnostic nutrient medium for the express diagnosis of animal dermatophytosis In: IOP Conference Series: Earth and Environmental Science. V. 315. IOP Publishing, 2019, 315(2): 022071 CrossRef
  24. Dekker J.P. Metagenomics for clinical infectious disease diagnostics steps closer to reality. Journal of Clinical Microbiology, 2018, 56(9): e00850-18 CrossRef
  25. Křivanec K., Otčenášek M. Importance of free living mustelid carnivores in circulation of adiaspiromycosis. Mycopathologia, 1977, 60(3): 139-144.
  26. Borman A.M., Simpson V.R., Palmer M.D., Linton C.J., Johnson E.M. Adiaspiromycosis due to Emmonsia crescens is widespread in native British mammals. Mycopathologia, 2019, 168(4): 153-163 CrossRef

 

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