Dermatophytes; Host shift; MAT idiomorph distribution; Phylogeny; Physicochemical features; Tinea capitis; Ecology, Evolution, Behavior and Systematics; Agricultural and Biological Sciences (miscellaneous)
Abstract :
[en] The Microsporum canis complex consists of one zoophilic species, M. canis, and two anthropophilic species, M. audouinii and M. ferrugineum. These species are the most widespread zoonotic pathogens causing dermatophytosis in cats and humans worldwide. To clarify the evolutionary relationship between the three species and explore the potential host shift process, this study used phylogenetic analysis, population structure analysis, multispecies coalescent analyses, determination of MAT idiomorph distribution, sexual crosses, and macromorphology and physicochemical features to address the above questions. The complex of Microsporum canis, M. audouinii and M. ferrugineum comprises 12 genotypes. MAT1-1 was present only in M. canis, while the anthropophilic entities contained MAT1-2. The pseudocleistothecia were yielded by the mating behaviour of M. canis and M. audouinii. Growth rates and lipase, keratinolysis and urea hydrolytic capacities of zoophilic M. canis isolates were all higher than those of anthropophilic strains; DNase activity of M. ferrugineum exceeded that of M. canis. The optimum growth temperature was 28 °C, but 22 °C favoured the development of macroconidia. Molecular data, physicochemical properties and phenotypes suggest the adaptation of zoophilic M. canis to anthropophilic M. ferrugineum, with M. audouinii in an intermediate position.
Disciplines :
Microbiology
Author, co-author :
Zhou, Xin ; Center of Expertise in Mycology of Radboud University Medical Center, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands ; Department of Dermatology, 3rd Affiliated Hospital, Sun Yat-senen University, Guangzhou, China
Ahmed, Sarah A ; Center of Expertise in Mycology of Radboud University Medical Center, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands ; Foundation Atlas of Clinical Fungi, Hilversum, The Netherlands
Tang, Chao; Center of Expertise in Mycology of Radboud University Medical Center, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands
Grisolia, Maria Eduarda ; Bioprocess Engineering and Biotechnology, Federal University of Paraná, Curitiba, Brazil
Warth, José Francisco Ghignatti; Microbiology, Parasitology and Pathology Graduate Program, Federal University of Paraná, Curitiba, Brazil
Webster, Kristen; Department of Dermatology, Center for Medical Mycology, University Hospitals, Cleveland, USA
Peano, Andrea; Department of Veterinary Sciences, University of Turin, Grugliasco, Italy
Cafarchia, Claudia ; Department of Veterinary Medicine, University of Bari Aldo Moro, Bari, Italy
Hayette, Marie-Pierre ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
Sacheli, Rosalie ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
Matos, Tadeja; Medical Faculty, Institute of Microbiology and Immunology, University of Ljubljana, Ljubljana, Slovenia
Kang, Yingqian; Key Laboratory of Environmental Pollution Monitoring and Disease Control, Ministry of Education of Guizhou & Guizhou Talent Base for Microbiology and Human Health, School of Basic Medical Sciences, Key Laboratory of Microbiology and Parasitology of Education Department of Guizhou, Guizhou Medical University, Guiyang, China. 449164105@qq.com ; Guizhou Provincial Academician Workstation of Microbiology and Health, Guizhou Academy of Tobacco Science, Guiyang, China. 449164105@qq.com
de Hoog, G Sybren ; Center of Expertise in Mycology of Radboud University Medical Center, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands. sybren.dehoog@radboudumc.nl ; Foundation Atlas of Clinical Fungi, Hilversum, The Netherlands. sybren.dehoog@radboudumc.nl ; Bioprocess Engineering and Biotechnology, Federal University of Paraná, Curitiba, Brazil. sybren.dehoog@radboudumc.nl ; Key Laboratory of Environmental Pollution Monitoring and Disease Control, Ministry of Education of Guizhou & Guizhou Talent Base for Microbiology and Human Health, School of Basic Medical Sciences, Key Laboratory of Microbiology and Parasitology of Education Department of Guizhou, Guizhou Medical University, Guiyang, China. sybren.dehoog@radboudumc.nl
Feng, Peiying ; Department of Dermatology, 3rd Affiliated Hospital, Sun Yat-senen University, Guangzhou, China. fengpeiying77@163.com
CSC - China Scholarship Council CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior
Funding text :
This project was supported by the Natural Science Foundation of Guangdong Province of China (No.2020A1515011183). XZ was supported by China Scholarship Council (No.202006380049). MEG was supported by CAPES-PrInt (No.88887.311835/2018-00). The funders had no role in study design, data collection and analysis, publication decision, or manuscript preparation. This work also was supported by the 111 Project (D20009); China-Ukraine Intergovernmental Exchange Project (8); National Natural Science Foundation of China (NSFC; no. 32060034); International Science and Technology Cooperation Base of Guizhou Province ([2020]4101); Talent Base Project of Guizhou Province, China [RCJD2018-22]; High-level Innovation Talent Project of Guizhou Province(GCC[2022]036-1); Major Science and Technology Projects of China Tobacco [No.110202101048(LS-08)]; Foundation of Key Laboratory of Microbiology and Parasitology of Education Department, Guizhou (QJJ [2022] 019); Ministry of Education Project(07150120711).
Aho R (1987) Mycological studies on Microsporum equinum isolated in Finland, Sweden and Norway. J Med Vet Mycol 25(4):255–260 DOI: 10.1080/02681218780000591
Aneke CI, Čmoková A, Hubka V, Rhimi W, Otranto D, Cafarchia C (2021) Subtyping options for Microsporum canis using microsatellites and MLST: a case study from Southern Italy. Pathogens 11(1):4 DOI: 10.3390/pathogens11010004
Bentubo HD, Gompertz OF (2014) Effects of temperature and incubation time on the in vitro expression of proteases, phospholipases, lipases and DNases by different species of Trichosporon. Springerplus 3:377 DOI: 10.1186/2193-1801-3-377
Brasch J, Müller S, Gräser Y (2015) Unusual strains of Microsporum audouinii causing tinea in Europe. Mycoses 58(10):573–577 DOI: 10.1111/myc.12358
Brito-Santos F, Figueiredo-Carvalho MHG, Coelho RA, Sales A, Almeida-Paes R (2017) Tinea capitis by Microsporum audouinii: case reports and review of published global literature 2000–2016. Mycopathologia 182(11–12):1053–1060 DOI: 10.1007/s11046-017-0181-1
Brosh-Nissimov T, Ben-Ami R, Astman N, Malin A, Baruch Y, Galor I (2018) An outbreak of Microsporum canis infection at a military base associated with stray cat exposure and person-to-person transmission. Mycoses 61(7):472–476 DOI: 10.1111/myc.12771
Cafarchia C, Figueredo LA, Coccioli C, Camarda A, Otranto D (2012) Enzymatic activity of Microsporum canis and Trichophyton mentagrophytes from breeding rabbits with and without skin lesions. Mycoses 55(1):45–49 DOI: 10.1111/j.1439-0507.2010.01997.x
Cerikçioğlu N (2009) Mating types, sexual reproduction and ploidy in fungi: effects on virulence. Mikrobiyol Bul 43(3):507–513
Chah KF, Majiagbe KA, Kazeem HM, Ezeanyika O, Agbo IC (2012) Dermatophytes from skin lesions of domestic animals in Nsukka, Enugu State, Nigeria. Vet Dermatol 23(6):522-e104 DOI: 10.1111/j.1365-3164.2012.01089.x
Choi JS, Gräser Y, Walther G, Peano A, Symoens F, de Hoog S (2012) Microsporum mirabile and its teleomorph Arthroderma mirabile, a new dermatophyte species in the M. cookei clade. Med Mycol 50(2):161–169 DOI: 10.3109/13693786.2011.594456
Ciesielska A, Stączek P (2020) A new molecular marker for species-specific identification of Microsporum canis. Braz J Microbiol 51(4):1505–1508 DOI: 10.1007/s42770-020-00340-y
de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M et al (2017) Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 182(1–2):5–31 DOI: 10.1007/s11046-016-0073-9
de Hoog GS, Guarro J, Gené J, Ahmed S, Al-Hatmi AMS, Figueras MJ & Vitale RG (2020) Atlas of Clinical Fungi, 4th edition. Hilversum
Douglas J, Jiménez-Silva CL, Bouckaert R (2022) StarBeast3: adaptive parallelized bayesian inference under the multispecies coalescent. Syst Biol 71(4):901–916 DOI: 10.1093/sysbio/syac010
Drenth A, McTaggart AR, Wingfield BD (2019) Fungal clones win the battle, but recombination wins the war. IMA Fungus 10:18 DOI: 10.1186/s43008-019-0020-8
Evans BA, Pickerill ES, Vyas VK, Bernstein DA (2018) CRISPR-mediated genome editing of the human fungal pathogen Candida albicans. J Vis Exp (141)
Fernandes S, Amaro C, da Luz MM, Inácio J, Araújo T, Vieira R et al (2013) Kerion caused by Microsporum audouinii in a child. Med Mycol Case Rep 2:52–54 DOI: 10.1016/j.mmcr.2013.02.002
Gräser Y, Kuijpers AF, El Fari M, Presber W, de Hoog GS (2000) Molecular and conventional taxonomy of the Microsporum canis complex. Med Mycol 38(2):143–153 DOI: 10.1080/mmy.38.2.143.153
Hasegawa A, Usui K (1974) The perfect state of Microsporum canis. Nihon Juigaku Zasshi 36(5):447–449 DOI: 10.1292/jvms1939.36.447
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
Hermoso de Mendoza M, Hermoso de Mendoza J, Alonso JM, Rey JM, Sanchez S, Martin R et al (2010) A zoonotic ringworm outbreak caused by a dysgonic strain of Microsporum canis from stray cats. Rev Iberoam Micol 27(2):62–65 DOI: 10.1016/j.riam.2009.12.007
Jain N, Sharma M (2011) Distribution of dermatophytes and other related fungi in Jaipur city, with particular reference to soil pH. Mycoses 54(1):52–58 DOI: 10.1111/j.1439-0507.2009.01751.x
Jain N, Sharma M (2012) Biodiversity of keratinophilic fungal flora in university campus, Jaipur, India. Iran J Public Health 41(11):27–33
Kane J, Padhye AA, Ajello L (1982) Microsporum equinum in North America. J Clin Microbiol 16(5):943–947 DOI: 10.1128/jcm.16.5.943-947.1982
Kano R, Aihara S, Nakamura Y, Watanabe S, Hasegawa A (2001) Chitin synthase 1 (Chs1) gene sequences of Microsporum equinum and Trichophyton equinum. Vet Microbiol 78(1):85–90. 10.1016/s0378-1135(00)00243-1 DOI: 10.1016/s0378-1135(00)00243-1
Kieliger S, Glatz M, Cozzio A, Bosshard PP (2015) Tinea capitis and tinea faciei in the Zurich area—an 8-year survey of trends in the epidemiology and treatment patterns. J Eur Acad Dermatol Venereol 29(8):1524–1529 DOI: 10.1111/jdv.12908
Kolivras A, Lateur N, De Maubeuge J, Scheers C, Wiame L, Song M (2003) Tinea capitis in Brussels: epidemiology and new management strategy. Dermatology 206(4):384–387 DOI: 10.1159/000069964
Kosanke S, Hamann L, Kupsch C, Moreno Garcia S, Chopra A, Gräser Y (2018) Unequal distribution of the mating type (MAT) locus idiomorphs in dermatophyte species. Fungal Genet Biol 118:45–53 DOI: 10.1016/j.fgb.2018.07.003
Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74(2):298–340 DOI: 10.1128/MMBR.00005-10
Leeming JG, Elliott TS (1995) The emergence of Trichophyton tonsurans tinea capitis in Birmingham. UK Br J Dermatol 133(6):929–931 DOI: 10.1111/j.1365-2133.1995.tb06928.x
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116 DOI: 10.1111/2041-210X.12410
López-Martínez R, Manzano-Gayosso P, Mier T, Méndez-Tovar LJ, Hernández-Hernández F (1994) Exoenzymes of dermatophytes isolated from acute and chronic tinea. Rev Latinoam Microbiol 36(1):17–20
Nenoff P, Gebhardt M, Klonowski E, Koch D, Krüger C, Uhrlaß S (2020) Microsporum ferrugineum-an anthropophilic dermatophyte in Germany: case report and review of the literature. Hautarzt 71(9):705–710 DOI: 10.1007/s00105-020-04601-7
Nielsen K, Heitman J (2007) Sex and virulence of human pathogenic fungi. Adv Genet 57:143–173 DOI: 10.1016/S0065-2660(06)57004-X
Oke OO, Onayemi O, Olasode OA, Omisore AG, Oninla OA (2014) The prevalence and pattern of superficial fungal infections among school children in Ile-Ife. South-Western Nigeria Dermatol Res Pract 2014:842917
Persinoti GF, Martinez DA, Li W, Döğen A, Billmyre RB, Averette A et al (2018) Whole-genome analysis illustrates global Clonal population structure of the ubiquitous dermatophyte pathogen Trichophyton rubrum. Genetics 208(4):1657–1669 DOI: 10.1534/genetics.117.300573
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 67(5):901–904 DOI: 10.1093/sysbio/syy032
Rezaei-Matehkolaei A, Makimura K, de Hoog GS, Shidfar MR, Satoh K, Najafzadeh MJ et al (2012) Multilocus differentiation of the related dermatophytes Microsporum canis, Microsporum ferrugineum and Microsporum audouinii. J Med Microbiol 61(Pt 1):57–63 DOI: 10.1099/jmm.0.036541-0
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302 DOI: 10.1093/molbev/msx248
Sabou M, Denis J, Boulanger N, Forouzanfar F, Glatz I, Lipsker D et al (2018) Molecular identification of Trichophyton benhamiae in Strasbourg, France: a 9-year retrospective study. Med Mycol 56(6):723–734 DOI: 10.1093/mmy/myx100
Sacheli R, Cuypers L, Seidel L, Darfouf R, Adjetey C, Lagrou K et al (2021) Epidemiology of dermatophytes in belgium: a 5 years’ survey. Mycopathologia 186(3):399–409 DOI: 10.1007/s11046-021-00542-4
Sánchez M, Colom F (2010) Extracellular DNase activity of Cryptococcus neoformans and Cryptococcus gattii. Rev Iberoam Micol 27(1):10–13 DOI: 10.1016/j.riam.2009.11.004
Scott JA, Untereiner WA (2004) Determination of keratin degradation by fungi using keratin azure. Med Mycol 42(3):239–246 DOI: 10.1080/13693780310001644680
Shamsizadeh F, Pchelin IM, Makimura K, Alshahni MM, Satoh K, Katiraee F et al (2020) DNA topoisomerase 2 gene polymorphism in dermatophytes. Mycoses 63(7):694–703 DOI: 10.1111/myc.13086
Sharma R, de Hoog S, Presber W, Gräser Y (2007) A virulent genotype of Microsporum canis is responsible for the majority of human infections. J Med Microbiol 56(Pt 10):1377–1385 DOI: 10.1099/jmm.0.47136-0
Smith KJ, Neafie RC, Skelton HG 3rd, Barrett TL, Graham JH, Lupton GP (1991) Majocchi’s granuloma. J Cutan Pathol 18(1):28–35 DOI: 10.1111/j.1600-0560.1991.tb00598.x
Stielow JB, Lévesque CA, Seifert KA, Meyer W, Iriny L, Smits D et al (2015) One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes. Persoonia 35:242–263 DOI: 10.3767/003158515X689135
Subelj M, Marinko JS, Učakar V (2014) An outbreak of Microsporum canis in two elementary schools in a rural area around the capital city of Slovenia. Epidemiol Infect 142(12):2662–2666 DOI: 10.1017/S0950268814000120
Takatori K, Hasegawa A (1985) mating experiment of Microsporum canis and Microsporum equinum isolated from animals with Nannizzia otae. Mycopathologia 90(1):59–63 DOI: 10.1007/BF00437278
Tang C, Kong X, Ahmed SA, Thakur R, Chowdhary A, Nenoff P et al (2021) Taxonomy of the Trichophyton mentagrophytes/T. interdigitale Species complex harboring the highly virulent, multiresistant genotype T. indotineae. Mycopathologia 186(3):315–326 DOI: 10.1007/s11046-021-00544-2
Viani FC, Dos Santos JI, Paula CR, Larson CE, Gambale W (2001) Production of extracellular enzymes by Microsporum canis and their role in its virulence. Med Mycol 39(5):463–468 DOI: 10.1080/mmy.39.5.463.468
Viguié-Vallanet C, Serre M, Masliah L, Tourte-Schaefer C (2005) Epidemic of Trichophyton tonsurans tinea capitis in a nursery school in the Southern suburbs of Paris. Ann Dermatol Venereol 132(5):432–438 DOI: 10.1016/S0151-9638(05)79304-2
West BC (1982) Five-year follow-up of a man with subcutaneous mycetomas caused by Microsporum audouinii. Am J Clin Pathol 77(6):767–769 DOI: 10.1093/ajcp/77.6.767
Zhan P, Li D, Wang C, Sun J, Geng C, Xiong Z et al (2015) Epidemiological changes in tinea capitis over the sixty years of economic growth in China. Med Mycol 53(7):691–698 DOI: 10.1093/mmy/myv057
Zhan P, Dukik K, Li D, Sun J, Stielow JB, Gerrits van den Ende B et al (2018) Phylogeny of dermatophytes with genomic character evaluation of clinically distinct Trichophyton rubrum and T. violaceum. Stud Mycol 89:153–175 DOI: 10.1016/j.simyco.2018.02.004
Zonta YR, Dezen ALO, Della Coletta AM, Yu KST, Carvalho L, Dos Santos LA et al (2020) Paracoccidioides brasiliensis releases a DNase-like protein that degrades NETs and allows for fungal escape. Front Cell Infect Microbiol 10:592022 DOI: 10.3389/fcimb.2020.592022
