Pathogens from the Trichophyton benhamiae complex are one of the most important causes of animal mycoses with significant zoonotic potential. In light of the recently revised taxonomy of this complex, we retrospectively identified 38 Trichophyton isolates that could not be resolved into any of the existing species. These strains were isolated from Iranian and Czech patients during molecular epidemiological surveys on dermatophytosis and were predominantly associated with highly inflammatory tinea corporis cases, suggesting possible zoonotic etiology. Subsequent phylogenetic (4 markers), population genetic (10 markers), and phenotypic analyses supported recognition of two novel species. The first species, Trichophyton persicum sp. nov., was identified in 36 cases of human dermatophytosis and one case of feline dermatophytosis, mainly in Southern and Western Iran. The second species, Trichophyton spiraliforme sp. nov., is only known from a single case of tinea corporis in a Czech patient who probably contracted the infection from a dog. Although the zoonotic sources of infections summarized in this study are very likely, little is known about the host spectrum of these pathogens. Awareness of these new pathogens among clinicians should refine our knowledge about their poorly explored geographic distribution. IMPORTANCE In this study, we describe two novel agents of dermatophytosis and summarize the clinical manifestation of infections. These new pathogens were discovered thanks to long-term molecular epidemiological studies conducted in Czechia and Iran. Zoonotic origins of the human infections are highly probable, but the animal hosts of these pathogens are poorly known. Further research is needed to refine our knowledge about these new dermatophytes.

Allergy Research Center Mashhad University of Medical Sciencesgrid 411583 a Mashhad Iran

Cellular and Molecular Research Center Medical Basic Sciences Research Institute Ahvaz Jundishapur University of Medical Sciences Ahvaz Iran

Department of Botany Faculty of Science Charles University Prague Czech Republic

Department of Dermatology and Venereology 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Department of Medical Mycology and Parasitology School of Medicine Shiraz University of Medical Sciencesgrid 412571 4 Shiraz Iran

Department of Medical Parasitology and Mycology School of Medicine Shahid Beheshti University of Medical Sciences Tehran Iran

Department of Parasitology and Mycology Faculty of Medicine Mashhad University of Medical Sciencesgrid 411583 a Mashhad Iran

Infectious and Tropical Diseases Research Center Health Research Institute Ahvaz Jundishapur University of Medical Sciences Ahvaz Iran

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology Czech Academy of Sciences Prague Czech Republic

Medical Mycology Research Center Chiba University Chiba Japan

Medicinal Plants Research Center Yasuj University of Medical Sciences Yasuj Iran

Zobrazit více v PubMed

Havlickova B, Czaika VA, Friedrich M. 2008. Epidemiological trends in skin mycoses worldwide. Mycoses 51(Suppl 4):2–15. doi: 10.1111/j.1439-0507.2008.01606.x. PubMed DOI

Deng W, Liang P, Zheng Y, Su Z, Gong Z, Chen J, Feng P, Chen J. 2020. Differential gene expression in HaCaT cells may account for the various clinical presentation caused by anthropophilic and geophilic dermatophytes infections. Mycoses 63:21–29. doi: 10.1111/myc.13021. PubMed DOI

Martinez-Rossi NM, Peres NT, Rossi A. 2017. Pathogenesis of dermatophytosis: sensing the host tissue. Mycopathologia 182:215–227. doi: 10.1007/s11046-016-0057-9. PubMed DOI

Ginter-Hanselmayer G, Nenoff P. 2019. Clinically relevant mycoses dermatomycoses, p 145–176.

Degreef H. 2008. Clinical forms of dermatophytosis (ringworm infection). Mycopathologia 166:257–265. doi: 10.1007/s11046-008-9101-8. PubMed DOI

Gräser Y, Monod M, Bouchara J-P, Dukik K, Nenoff P, Kargl A, Kupsch C, Zhan P, Packeu A, Chaturvedi V, de Hoog GS. 2018. New insights in dermatophyte research. Med Mycol 56:S2–S9. doi: 10.1093/mmy/myx141. PubMed DOI

John AM, Schwartz RA, Janniger CK. 2018. The kerion: an angry tinea capitis. Int J Dermatol 57:3–9. doi: 10.1111/ijd.13423. PubMed DOI

Hube B, Hay R, Brasch J, Veraldi S, Schaller M. 2015. Dermatomycoses and inflammation: the adaptive balance between growth, damage, and survival. J Mycol Med 25:e44–e58. doi: 10.1016/j.mycmed.2014.11.002. PubMed DOI

Gnat S, Nowakiewicz A, Łagowski D, Zięba P. 2019. Host- and pathogen-dependent susceptibility and predisposition to dermatophytosis. J Med Microbiol 68:823–836. doi: 10.1099/jmm.0.000982. PubMed DOI

Čmoková A, Kolařík M, Dobiáš R, Hoyer LL, Janouškovcová H, Kano R, Kuklová I, Lysková P, Machová L, Maier T, Mallátová N, Man M, Mencl K, Nenoff P, Peano A, Prausová H, Stubbe D, Uhrlaß S, Větrovský T, Wiegand C, Hubka V. 2020. Resolving the taxonomy of emerging zoonotic pathogens in the DOI

Bonifaz A, Archer‐Dubon C, Saúl A. 2004. Tinea imbricata or Tokelau. Int J Dermatol 43:506–510. doi: 10.1111/j.1365-4632.2004.02171.x. PubMed DOI

Pihet M, Bourgeois H, Mazière J-Y, Berlioz-Arthaud A, Bouchara J-P, Chabasse D. 2008. Isolation of PubMed DOI

Agnetti F, Righi C, Scoccia E, Felici A, Crotti S, Moretta I, Moretti A, Maresca C, Troiani L, Papini M. 2014. PubMed DOI

Ming PX, Ti YLX, Bulmer GS. 2006. Outbreak of PubMed DOI

Kielstein P. 1990. Systematic control of dermatophytosis profunda of cattle in the former GDR. Mycoses 33:575–580. doi: 10.1111/myc.1990.33.11-12.575. PubMed DOI

Lund A, Bratberg AM, Næss B, Gudding R. 2014. Control of bovine ringworm by vaccination in Norway. Vet Immunol Immunopathol 158:37–45. doi: 10.1016/j.vetimm.2013.04.007. PubMed DOI

Sabou M, Denis J, Boulanger N, Forouzanfar F, Glatz I, Lipsker D, Poirier P, Candolfi E, Letscher-Bru V. 2018. Molecular identification of PubMed DOI

Kimura U, Yokoyama K, Hiruma M, Kano R, Takamori K, Suga Y. 2015. Tinea faciei caused by PubMed DOI

Hubka V, Čmoková A, Peano A, Větrovský T, Dobiáš R, Mallátová N, Lysková P, Mencl K, Janouškovcová H, Stará J, Kuklová I, Doležalová J, Hamal P, Svobodová L, Koubková J, Kolařík M. 2018. Zoonotic dermatophytoses: clinical manifestation, diagnosis, etiology, treatment, epidemiological situation in the Czech Republic. Čes Slov Dermatol 93:208–235.

Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, Herrmann J, Wetzig T, Schroedl W, Gräser Y. 2014. PubMed DOI

Barzic CL, Cmokova A, Denaes C, Arné P, Hubka V, Guillot J, Risco-Castillo V. 2021. Detection and control of dermatophytosis in wild European hedgehogs ( PubMed DOI PMC

Hubka V, Peano A, Cmokova A, Guillot J. 2018. Common and emerging dermatophytoses in animals: well-known and new threats, p 31–79.

de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, Kupsch C, Stielow JB, Freeke J, Göker M, Rezaei-Matehkolaei A, Mirhendi H, Gräser Y. 2017. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 182:5–31. doi: 10.1007/s11046-016-0073-9. PubMed DOI PMC

Gräser Y, Kuijpers A, Presber W, de Hoog GS. 2000. Molecular taxonomy of the PubMed DOI PMC

Gräser Y, Kuijpers A, Presber W, de Hoog GS. 1999. Molecular taxonomy of PubMed DOI

Brasch J, Gräser Y. 2005. PubMed DOI PMC

Hubka V, Nissen CV, Jensen RH, Arendrup MC, Cmokova A, Kubatova A, Skorepova M, Kolarik M. 2015. Discovery of a sexual stage in PubMed DOI

Hainsworth S, Kučerová I, Sharma R, Cañete-Gibas CF, Hubka V. 2020. Three-gene phylogeny of the genus PubMed DOI

Hubka V, Cmokova A, Skorepova M, Mikula P, Kolarik M. 2014. PubMed DOI

Lorch JM, Minnis AM, Meteyer CU, Redell JA, White JP, Kaarakka HM, Muller LK, Lindner DL, Verant ML, Shearn-Bochsler V, Blehert DS. 2015. The fungus PubMed DOI

Kano R, Kimura U, Kakurai M, Hiruma J, Kamata H, Suga Y, Harada K. 2020. PubMed DOI

Heidemann S, Monod M, Gräser Y. 2010. Signature polymorphisms in the internal transcribed spacer region relevant for the differentiation of zoophilic and anthropophilic strains of PubMed DOI

Gräser Y, Scott J, Summerbell R. 2008. The new species concept in dermatophytes—a polyphasic approach. Mycopathologia 166:239–256. doi: 10.1007/s11046-008-9099-y. PubMed DOI

Khurana A, Masih A, Chowdhary A, Sardana K, Borker S, Gupta A, Gautam R, Sharma P, Jain D. 2018. Correlation of PubMed DOI PMC

Taghipour S, Shamsizadeh F, Pchelin IM, Rezaei-Matehhkolaei A, Zarei Mahmoudabadi A, Valadan R, Ansari S, Katiraee F, Pakshir K, Zomorodian K, Abastabar M. 2020. Emergence of terbinafine resistant PubMed DOI PMC

Ebert A, Monod M, Salamin K, Burmester A, Uhrlaß S, Wiegand C, Hipler UC, Krüger C, Koch D, Wittig F, Verma SB, Singal A, Gupta S, Vasani R, Saraswat A, Madhu R, Panda S, Das A, Kura MM, Kumar A, Poojary S, Schirm S, Gräser Y, Paasch U, Nenoff P. 2020. Alarming India‐wide phenomenon of antifungal resistance in dermatophytes: a multicentre study. Mycoses 63:717–728. doi: 10.1111/myc.13091. PubMed DOI

Shamsizadeh F, Ansari S, Zarei Mahmoudabadi A, Hubka V, Čmoková A, Guillot J, Rafiei A, Zomorodian K, Nouripour-Sisakht S, Diba K, Mohammadi T, Zarrinfar H, Rezaei-Matehkolaei A. 2021. PubMed DOI

Ansari S, Ahmadi B, Hedayati MT, Nouripour‐Sisakht S, Taghizadeh‐Armaki M, Fathi M, Deravi N, Shokoohi GR, Rezaei‐Matehkolaei A. 2021. Investigation of PubMed DOI

Zareshahrabadi Z, Totonchi A, Rezaei-Matehkolaei A, Ilkit M, Ghahartars M, Arastehfar A, Motamedi M, Nouraei H, Sharifi Lari M, Mohammadi T, Zomorodian K. 2021. Molecular identification and antifungal susceptibility among clinical isolates of dermatophytes in Shiraz, Iran (2017–2019). Mycoses 64:385–393. doi: 10.1111/myc.13226. PubMed DOI

Hayette M-P, Sacheli R. 2015. Dermatophytosis, trends in epidemiology and diagnostic approach. Curr Fungal Infect Rep 9:164–179. doi: 10.1007/s12281-015-0231-4. DOI

Khosravi A, Aghamirian M, Mahmoudi M. 1994. Dermatophytoses in Iran. Mycoses 37:43–48. doi: 10.1111/j.1439-0507.1994.tb00284.x. PubMed DOI

Ansari S, Hedayati MT, Zomorodian K, Pakshir K, Badali H, Rafiei A, Ravandeh M, Seyedmousavi S. 2016. Molecular characterization and PubMed DOI

Zamani S, Sadeghi G, Yazdinia F, Moosa H, Pazooki A, Ghafarinia Z, Abbasi M, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. 2016. Epidemiological trends of dermatophytosis in Tehran, Iran: a five-year retrospective study. J Mycol Med 26:351–358. doi: 10.1016/j.mycmed.2016.06.007. PubMed DOI

Ahmadi B, Mirhendi H, Shidfar M, Nouripour-Sisakht S, Jalalizand N, Geramishoar M, Shokoohi G. 2015. A comparative study on morphological versus molecular identification of dermatophyte isolates. J Mycol Med 25:29–35. doi: 10.1016/j.mycmed.2014.10.022. PubMed DOI

Rezaei-Matehkolaei A, Makimura K, de Hoog GS, Shidfar MR, Zaini F, Eshraghian M, Naghan PA, Mirhendi H. 2013. Molecular epidemiology of dermatophytosis in Tehran, Iran, a clinical and microbial survey. Med Mycol 51:203–207. doi: 10.3109/13693786.2012.686124. PubMed DOI

Didehdar M, Shokohi T, Khansarinejad B, Sefidgar SAA, Abastabar M, Haghani I, Amirrajab N, Mondanizadeh M. 2016. Characterization of clinically important dermatophytes in North of Iran using PCR-RFLP on ITS region. J Mycol Med 26:345–350. doi: 10.1016/j.mycmed.2016.06.006. PubMed DOI

Farokhipor S, Ghiasian S, Nazeri H, Kord M, Didehdar M. 2018. Characterizing the clinical isolates of dermatophytes in Hamadan city, central west of Iran, using PCR-RLFP method. J Mycol Med 28:101–105. doi: 10.1016/j.mycmed.2017.11.009. PubMed DOI

Ebrahimi M, Zarrinfar H, Naseri A, Najafzadeh MJ, Fata A, Parian M, Khorsand I, Babič MN. 2019. Epidemiology of dermatophytosis in northeastern Iran; a subtropical region. Curr Med Mycol 5:16–21. doi: 10.18502/cmm.5.2.1156. PubMed DOI PMC

Rezaei-Matehkolaei A, Rafiei A, Makimura K, Gräser Y, Gharghani M, Sadeghi-Nejad B. 2016. Epidemiological aspects of dermatophytosis in Khuzestan, southwestern Iran, an update. Mycopathologia 181:547–553. doi: 10.1007/s11046-016-9990-x. PubMed DOI

Bontems O, Fratti M, Salamin K, Guenova E, Monod M. 2020. Epidemiology of dermatophytoses in Switzerland according to a survey of dermatophytes isolated in Lausanne between 2001 and 2018. J Fungi 6:95. doi: 10.3390/jof6020095. PubMed DOI PMC

Uhrlaß S, Krüger C, Nenoff P. 2015. PubMed DOI

Packeu A, Stubbe D, Roesems S, Goens K, Van Rooij P, de Hoog GS, Hendrickx M. 2020. Lineages within the PubMed DOI

Kaszubiak A, Klein S, de Hoog GS, Gräser Y. 2004. Population structure and evolutionary origins of PubMed DOI

Rezaei-Matehkolaei A, Makimura K, de Hoog GS, Shidfar MR, Satoh K, Najafzadeh MJ, Mirhendi H. 2012. Multilocus differentiation of the related dermatophytes PubMed DOI

Ziółkowska G, Nowakiewicz A, Gnat S, Trościańczyk A, Zięba P, Majer Dziedzic B. 2015. Molecular identification and classification of PubMed DOI

Komarek J, Wurst Z. 1989. Dermatophytes in clinically healthy dogs and cats. Vet Med (Praha) 34:59–63. PubMed

Drouot S, Mignon B, Fratti M, Roosje P, Monod M. 2009. Pets as the main source of two zoonotic species of the PubMed DOI

Weiß R, Böhm KH, Mumme J, Nicklas W. 1979. 13 Jahre veterinärmedizinische mykologische Routinediagnostik. Dermatophytennachweise in den Jahren 1965 bis 1977. Sabouraudia 17:345–353. doi: 10.1080/00362177985380521. PubMed DOI

Cabañes F, Abarca ML, Bragulat MR, Castella G. 1996. Seasonal study of the fungal biota of the fur of dogs. Mycopathologia 133:1–7. doi: 10.1007/BF00437092. PubMed DOI

Cafarchia C, Gasser RB, Figueredo LA, Weigl S, Danesi P, Capelli G, Otranto D. 2013. An improved molecular diagnostic assay for canine and feline dermatophytosis. Med Mycol 51:136–143. doi: 10.3109/13693786.2012.691995. PubMed DOI

Sieklucki U, Oh SH, Hoyer LL. 2014. Frequent isolation of PubMed DOI PMC

Yahyaraeyat R, Shokri H, Khosravi A, Soltani M, Erfanmanesh A, Nikaein D. 2009. Occurrence of animals dermatophytosis in Tehran, Iran. World J Zool 4:200–204.

Shokri H, Khosravi A. 2016. An epidemiological study of animals dermatomycoses in Iran. J Mycol Med 26:170–177. doi: 10.1016/j.mycmed.2016.04.007. PubMed DOI

Khosravi A, Mahmoudi M. 2003. Dermatophytes isolated from domestic animals in Iran. Mycoses 46:222–225. doi: 10.1046/j.1439-0507.2003.00868.x. PubMed DOI

Khosravi A. 1996. Fungal flora of the hair coat of stray cats in Iran. Mycoses 39:241–243. doi: 10.1111/j.1439-0507.1996.tb00133.x. PubMed DOI

Abastabar M, Jedi A, Guillot J, Ilkit M, Eidi S, Hedayati MT, Shokohi T, Daie Ghazvini R, Rezaei-Matehkolaei A, Katiraee F, Javidnia J, Ahmadi B, Badali H. 2019. PubMed DOI

Moosavi A, Ghazvini R, Ahmadikia K, Hashemi S, Geramishoar M, Mohebali M, Yekaninejad M, Bakhshi H, Khodabakhsh M. 2019. The frequency of fungi isolated from the skin and hair of asymptomatic cats in rural area of Meshkin-shahr-Iran. J Mycol Med 29:14–18. doi: 10.1016/j.mycmed.2019.01.004. PubMed DOI

Łagowski D, Gnat S, Nowakiewicz A, Osińska M. 2021. Assessment of the subtilisin gene profile in PubMed DOI

Mohammadi R, Abastabar M, Mirhendi H, Badali H, Shadzi S, Chadeganipour M, Pourfathi P, Jalalizand N, Haghani I. 2015. Use of restriction fragment length polymorphism to rapidly identify dermatophyte species related to dermatophytosis. Jundishapur J Microbiol 8:e17296. doi: 10.5812/jjm.8(5)2015.17296. PubMed DOI PMC

Hubka V, Větrovský T, Dobiášová S, Skořepová M, Lysková P, Mencl K, Mallátová N, Janouškovcová H, Hanzlíčková J, Dobiáš R, Čmoková A, Stará J, Hamal P, Svobodová L, Kolařík M. 2014. Molecular epidemiology of dermatophytoses in the Czech Republic—two-year-study results. Čes Slov Dermatol 89:167–174.

Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi: 10.1111/j.1365-294x.1993.tb00005.x. PubMed DOI

White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, p 315–322.

Kawasaki M, Anzawa K, Ushigami T, Kawanishi J, Mochizuki T. 2011. Multiple gene analyses are necessary to understand accurate phylogenetic relationships among PubMed DOI

Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330. doi: 10.1128/aem.61.4.1323-1330.1995. PubMed DOI PMC

Mirhendi H, Makimura K, de Hoog GS, Rezaei-Matehkolaei A, Najafzadeh MJ, Umeda Y, Ahmadi B. 2015. Translation elongation factor 1-α gene as a potential taxonomic and identification marker in dermatophytes. Med Mycol 53:215–224. doi: 10.1093/mmy/myu088. PubMed DOI

Kano R, Kawasaki M, Mochizuki T, Hiruma M, Hasegawa A. 2012. Mating genes of the PubMed DOI

Symoens F, Jousson O, Packeu A, Fratti M, Staib P, Mignon B, Monod M. 2013. The dermatophyte species PubMed DOI

Hubka V, Nováková A, Jurjević Ž, Sklenář F, Frisvad JC, Houbraken J, Arendrup MC, Jørgensen KM, Siqueira JPZ, Gené J, Kolařík M. 2018. Polyphasic data support the splitting of PubMed DOI

Réblová M, Hubka V, Thureborn O, Lundberg J, Sallstedt T, Wedin M, Ivarsson M. 2016. From the tunnels into the treetops: new lineages of black yeasts from biofilm in the Stockholm metro system and their relatives among ant-associated fungi in the PubMed DOI PMC

Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773. doi: 10.1093/molbev/msw260. PubMed DOI

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Clement M, Posada D, Crandall KA. 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x. PubMed DOI

Leigh JW, Bryant D. 2015. POPART: full‐feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. doi: 10.1111/2041-210X.12410. DOI

Schlüter PM, Harris SA. 2006. Analysis of multilocus fingerprinting data sets containing missing data. Mol Ecol Notes 6:569–572. doi: 10.1111/j.1471-8286.2006.01225.x. DOI

Kelly KL, Judd DB, Inter-Society Color Council. 1964. ISCC-NBS color-name charts illustrated with centroid colors. US National Bureau of Standards, Chicago, IL.

Rippon JW. 1988. Medical mycology: the pathogenic fungi and the pathogenic actinomycetes, 3rd ed. Saunders, Philadelphia, PA.

Lebasque J. 1933. Les champignons des teignes du cheval et des bovidés. Faculté des Sciences de Paris, Paris, France.

Comparative gene expression analysis in closely related dermatophytes reveals secondary metabolism as a candidate driver of virulence

Resolving Phylogenetic Relationships Within the Trichophyton mentagrophytes Complex: A RADseq Genomic Approach Challenges Status of 'Terbinafine-Resistant' Trichophyton indotineae as Distinct Species

First Step on the Way to Identify Dermatophytes Using Odour Fingerprints

Wild rodents harbour high diversity of Arthroderma

Defining the relationship between phylogeny, clinical manifestation, and phenotype for Trichophyton mentagrophytes/interdigitale complex; a literature review and taxonomic recommendations

Cases of dermatophytosis caused by Trichophyton benhamiae var. luteum and T. europaeum, newly described dermatophytes within the T. benhamiae complex

Host-driven subspeciation in the hedgehog fungus, Trichophyton erinacei, an emerging cause of human dermatophytosis

Subtyping Options for Microsporum canis Using Microsatellites and MLST: A Case Study from Southern Italy

An Outbreak of Trichophyton quinckeanum Zoonotic Infections in the Czech Republic Transmitted from Cats and Dogs

Zobrazit více v PubMed

Dryad
10.5061/dryad.59zw3r275