Multilocus phylogeny of the Trichophyton mentagrophytes species complex and the application of matrix-assisted laser desorption/ionization–time-of-flight (MALDI-TOF) mass spectrometry for the rapid identification of dermatophytes

LITERATURE CITED

• Ahmadi B, Mirhendi H, Makimura K, de Hoog GS, Shidfar MR, Nouripour-Sisakht S, Jalalizand N. 2016. Phylogenetic analysis of dermatophyte species using DNA sequence polymorphism in calmodulin gene. Medical Mycology 54:500–514.
   PubMed Web of Science ®Google Scholar
• Ajello L, Bostick L, Cheng S-L. 1968. The relationship of Trichophyton quinckeanum to Trichophyton mentagrophytes. Mycologia 60:1185–1189.
   PubMed Web of Science ®Google Scholar
• Ajello L, Cheng S-L. 1967. The perfect state of Trichophyton mentagrophytes. Sabouraudia 5:230–234.
   PubMedGoogle Scholar
• Beguin H, Pyck N, Hendrickx M, Planard C, Stubbe D, Detandt M. 2012. The taxonomic status of Trichophyton quinckeanum and T. interdigitale revisited: a multigene phylogenetic approach. Medical Mycology 50:871–882.
   PubMed Web of Science ®Google Scholar
• Chollet A, Cattin V, Fratti M, Mignon B, Monod M. 2015a. Which fungus originally was Trichophyton mentagrophytes? Historical review and illustration by a clinical case. Mycopathologia 180:1–5.
   PubMed Web of Science ®Google Scholar
• Chollet A, Wespi B, Roosje P, Unger L, Venner M, Goepfert C, Monod M. 2015b. An outbreak of Arthroderma vanbreuseghemii dermatophytosis at a veterinary school associated with an infected horse. Mycoses 58:233–238.
   PubMed Web of Science ®Google Scholar
• de Hoog GS, Bowman B, Gräser Y, Haase G, El Fari M, Gerrits van den Ende AH, Melzer-Krick B, Untereiner WA. 1998. Molecular phylogeny and taxonomy of medically important fungi. Medical Mycology 36( Supplement 1):52–56.
   PubMed Web of Science ®Google Scholar
• de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, Kupsch C, Stielow JB, Freeke J, Göker M, Rezaei-Matehkolaei A, MirhendiH, Gräser Y. 2017. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 182:5–31.
   PubMed Web of Science ®Google Scholar
• de Respinis S, Monnin V, Girard V, Welker M, Arsac M, Cellière B, Durand G, Bosshard PP, Farina C, Passera M, Van Belkum A, Petrini O, Tonolla M. 2014. Matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry using the Vitek MS system for rapid and accurate identification of dermatophytes on solid cultures. Journal of Clinical Microbiology 52:4286–4292.
   PubMed Web of Science ®Google Scholar
• de Respinis S, Tonolla M, Pranghofer S, Petrini L, Petrini O, Bosshard PP. 2013. Identification of dermatophytes by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Medical Mycology 51:514–521.
   PubMed Web of Science ®Google Scholar
• Fréalle E, Rodrigue M, Gantois N, Aliouat CM, Delaporte E, Camus D, Dei-Cas E, Kauffmann-Lacroix C, Guillot J, Delhaes L. 2007. Phylogenetic analysis of Trichophyton mentagrophytes human and animal isolates based on MnSOD and ITS sequence comparison. Microbiology 153:3466–3477.
   PubMed Web of Science ®Google Scholar
• Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61:1323–1330.
   PubMed Web of Science ®Google Scholar
• Gräser Y, El Farl M, Vilgalys R, Kuijpers AF, de Hoog GS, Presber W, Tietz H. 1999a. Phylogeny and taxonomy of the family Arthrodermataceae (dermatophytes) using sequence analysis of the ribosomal ITS region. Medical Mycology 37:105–114.
   PubMed Web of Science ®Google Scholar
• Gräser Y, Kuijpers AF, Presber W, de Hoog GS. 1999b. Molecular taxonomy of Trichophyton mentagrophytes and T. tonsurans. Medical Mycology 37:315–330.
   PubMed Web of Science ®Google Scholar
• Gräser Y, Scott J, Summerbell R. 2008. The new species concept in dermatophytes—a polyphasic approach. Mycopathologia 166:239–256.
   PubMed Web of Science ®Google Scholar
• 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 Trichophyton interdigitale and other species of T. mentagrophytes sensu lato. British Journal of Dermatology 162:282–295.
   PubMed Web of Science ®Google Scholar
• Karabıçak N, Karatuna O, İlkit M, Akyar I. 2015. Evaluation of the Bruker matrix-assisted laser desorption-ionization time-of-flight mass spectrometry (MALDI-TOF MS) system for the identification of clinically important dermatophyte species. Mycopathologia 180:165–171.
   PubMed Web of Science ®Google Scholar
• Kaufman G, Horwitz BA, Hadar R, Ullmann Y, Berdicevsky I. 2004. Green fluorescent protein (GFP) as a vital marker for pathogenic development of the dermatophyte Trichophyton mentagrophytes. Microbiology 150:2785–2790.
   PubMed Web of Science ®Google Scholar
• l’Ollivier C, Ranque S. 2017. MALDI-TOF-based dermatophyte identification. Mycopathologia 182:183–192.
   PubMed Web of Science ®Google Scholar
• Martiny D, Busson L, Wybo I, El Haj RA, Dediste A, Vandenberg O. 2012. Comparison of the Microflex LT and Vitek MS systems for routine identification of bacteria by matrix-assisted laser desorption ionization time of flight mass spectrometry. Journal of Clinical Microbiology 50:1313–1325.
   PubMed Web of Science ®Google Scholar
• McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme van Reine WF, Smith GF, Wiersema JH, Turland NJ, eds. 2012. International Code of Nomenclature for algae, fungi and plants (Melbourne Code) adopted by the 18th International Botanical Congress Melbourne, Australia, July 2011. Regnum Vegetabile 154. Ruggell, Liechtenstein: A.R.G. Ganter Verlag. 240 p.
   Google Scholar
• 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. Medical Mycology 53:215–224.
   PubMed Web of Science ®Google Scholar
• Mukherjee PK, Leidich SD, Isham N, Leitner I, Ryder NS, Ghannoum MA. 2003. Clinical Trichophyton rubrum strain exhibiting primary resistance to terbinafine. Antimicrobial Agents and Chemotherapy 47:82–86.
   PubMed Web of Science ®Google Scholar
• Nenoff P, Erhard M, Simon JC, Muylowa GK, Herrmann J, Rataj W, Gräser Y. 2013. MALDI-TOF mass spectrometry—a rapid method for the identification of dermatophyte species. Medical Mycology 51:17–24.
   PubMed Web of Science ®Google Scholar
• O’Donnell K, Cigelnik E. 1997. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7:103–116.
   PubMed Web of Science ®Google Scholar
• Packeu A, De Bel A, l’Ollivier C, Ranque S, Detandt M, Hendrickx M. 2014. Fast and accurate identification of dermatophytes by matrix-assisted laser desorption ionization-time of flight mass spectrometry: validation in the clinical laboratory. Journal of Clinical Microbiology 52:3440–3443.
   PubMed Web of Science ®Google Scholar
• Packeu A, Hendrickx M, Beguin H, Martiny D, Vandenberg O, Detandt M. 2013. Identification of the Trichophyton mentagrophytes complex species using MALDI-TOF mass spectrometry. Medical Mycology 51:580–585.
   PubMed Web of Science ®Google Scholar
• Rezaei-Matehkolaei A, Mirhendi H, Makimura K, de Hoog GS, Satoh K, Najafzadeh MJ, Shidfar MR. 2014. Nucleotide sequence analysis of beta tubulin gene in a wide range of dermatophytes. Medical Mycology 52:674–688.
   PubMed Web of Science ®Google Scholar
• 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. Systematic Biology 61:539–542.
   PubMed Web of Science ®Google Scholar
• Sanguinetti M, Posteraro B. 2017. Identification of molds by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Journal of Clinical Microbiology 55:369–379.
   PubMed Web of Science ®Google Scholar
• Sendid B, Ducoroy P, Francois N, Lucchi G, Spinali S, Vagner O, Damiens S, Bonnin A, Poulain D, Dalle F. 2013. Evaluation of MALDI-TOF mass spectrometry for the identification of medically-important yeasts in the clinical laboratories of Dijon and Lille hospitals. Medical Mycology 51:25–32.
   PubMed Web of Science ®Google Scholar
• Suh SO, Houseknecht JL, Grosso KM, Carrion ME. 2015. Characterization of medically important yeast Trichosporon mucoides and its close sister Trichosporon dermatis by traditional and advanced technologies. Journal of Medical Microbiology 64:1135–1143.
   PubMed Web of Science ®Google Scholar
• Suh SO, Zhou JJ. 2010. Methylotrophic yeasts near Ogataea (Hansenula) polymorpha: a proposal of O. angusta comb. nov. and Candida parapolymorpha sp. nov. FEMS Yeast Research 10:631–638.
   PubMed Web of Science ®Google Scholar
• Summerbell RC, Moore MK, Starink-Willemse M, Van Iperen A. 2007. ITS barcodes for Trichophyton tonsurans and T. equinum. Medical Mycology 45:193–200.
   PubMed Web of Science ®Google Scholar
• Swofford DL. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
   Google Scholar
• Symoens F, Jousson O, Planard C, Fratti M, Staib P, Mignon B, Monod M. 2011. Molecular analysis and mating behaviour of the Trichophyton mentagrophytes species complex. International Journal of Medical Microbiology 301:260–266.
   PubMed Web of Science ®Google Scholar
• Takashio M. 1972. Is Arthroderma benhamiae the perfect state of Trichophyton mentagrophytes? Sabouraudia 10:122–127.
   Google Scholar
• Takashio M. 1973. Etude des phénomènes de reproduction liés au vieillissement et au rajeunissement des cultures de champignons. Annales de la Société Belge de Médicine Tropical 53:427–580.
   Google Scholar
• Takashio M. 1974. Observation of African and European strains of Arthroderma benhamiae. International Journal of Dermatology 13:94–101.
   PubMed Web of Science ®Google Scholar
• Tatusova TA, Madden TL. 1999. Blast 2 sequences—a new tool for comparing protein and nucleotide sequences. FEMS Microbiology Letters 174:247–250.
   PubMed Web of Science ®Google Scholar
• Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tool. Nucleic Acids Research 25:4876–4882.
   PubMed Web of Science ®Google Scholar
• Weitzman I, Summerbell RC. 1995. The dermatophytes. Clinical Microbiology Reviews 8:240–259.
   PubMed Web of Science ®Google Scholar