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Exophiala Spinifera and Its Allies: Diagnostics from 109 Morphology to DNA Barcoding UvA-DARE (Digital Academic Repository) Developing species recognition and diagnostics of rare opportunistic fungi Zeng, J. Publication date 2007 Document Version Final published version Link to publication Citation for published version (APA): Zeng, J. (2007). Developing species recognition and diagnostics of rare opportunistic fungi. IBED. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:01 Oct 2021 Developing Species Recognition and Diagnostics of Rare Opportunistic Fungi Opportunistic Rare of Diagnostics and Recognition Species Developing Developing Species Recognition and Diagnostics of Rare Opportunistic Fungi Jingsi Zeng Jingsi Zeng Developing Species Recognition and Diagnostics of Rare Opportunistic Fungi Jingsi Zeng Promotor Prof. Dr. G.S. de Hoog Centraalbureau voor Schimmelcultures Fungal Biodiversity Centre, Royal Netherlands Academy of Arts and Sciences Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam Co-promotor Dr. Y. Gräser Humboldt University, Germany Promotiecommissie W. Admiraal (IBED, Amsterdam) S. Menken (IBED, Amsterdam) M. Sabelis (IBED, Amsterdam) J. Meis (Canisinus-Wilhelmina Ziekenhuis, Nijmegen) G. Haase (RWTH, Aachen) Developing Species Recognition and Diagnostics of Rare Opportunistic Fungi Jingsi Zeng ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. J. W. Zwemmer ten overstaan van een door het college voor promoties ingestelde commissie, in het openbaar te verdedigen in de Aula der Universiteit op dinsdag 18 september 2007, te 10.00 uur Printed by Ponsen & Looijen B.V., Wageningen, the Netherlands The work was financially supported by the joint research project ‘Comparative genomics in search of origins of human pathogenicity in the fungal Tree of Life focusing on species with high morbidity and mortality in Chinese patients’, Scientific cooperation between China and the Netherlands, China Exchange Programme, Royal Netherlands Academy of Arts and Sciences (KNAW). This thesis is dedicated to my dear parents, husband and daughter, my tutors for Master’s degree Prof. Zhaoru Zhu and Prof. Yuechen Zheng 谨献给我亲爱的父母、丈夫及女儿， 以及恩师祝兆如教授和郑岳臣教授 Contents Page Chapter 1 Introduction and outline of thesis 1 Chapter 2 Intraspecific diversity of species of Pseudallescheria boydii 25 complex Chapter 3 Exophiala xenobiotica sp. nov., an opportunistic black yeast 45 inhabiting environments rich in hydrocarbons Chapter 4 Spectrum of clinically relevant Exophiala species in the U.S.A. 65 Chapter 5 Phylogeny of the Exophiala spinifera clade using multilocus 85 sequence data and exploring phylogenetic species concept Chapter 6 Exophiala spinifera and its allies: diagnostics from 109 morphology to DNA barcoding Chapter 7 Susceptibility of Pseudallescheria boydii and Scedosporium 133 apiospermum to new antifungal agents Chapter 8 General dicussion 139 Appendix Summary 151 List of publications and abstracts 155 Acknowledgements 158 Curriculum vitae 161 Chapter 1 Introduction and outline of thesis 1 Chapter 1 Historical overview of species recognition in Pseudallescheria and Exophiala The fungal genera Pseudallescheria and Exophiala include agents of opportunistic infection in humans. They are potentially able to cause a wide diversity of mycoses, varying from cutaneous infections to disseminated syndromes. Most infections are noted in otherwise healthy individuals and are of traumatic nature or concern colonization of cavities or the intestinal tract. Most are typical opportunists in that they expand or disseminate when the innate immunity of the host is impaired. However, some Exophiala species are repeatedly observed to cause fatal, systemic or disseminated infections in patients without any immune disorder. The pathology of these fungi is poorly understood since development of the knowledge was long time hampered by inadequate diagnostics. Although they are among the first fungi reported from deep human infections [1], their taxonomy flourished only since the application of molecular methods [2;3]. In the routine laboratory, species recognition is still problematic. Pseudallescheria Negroni et Fischer The lineage of the genus Pseudallescheria (anamorph Scedosporium) is Eukaryota, Fungi, Ascomycota, Euascomycetes, Microascales, Microascaceae. The species thus far established in the genus are listed in Table 1. Colonies on cornmeal agar are rapid growing, floccose or lanose, initially whitish or grey, becoming grey or brown; ascomata are usually submerged, globose, nonostiolate, 100-200 μm in diameter width; peridium composed of flattened, brown, pseudoparenchymatous cells, 2-3 cells thick; asci are globose to ellipsoidal, symmetrical or slightly flattened, with 2 germ pores, light brown to yellowish; homothallic. Scedosporium, Graphium, or both anamorphs may be formed [4]. In 1893, Costantin described a species Eurotiopsis gayoni Cost. [5]. As the name Eurotiopsis had already been used for an entirely different fungus, Saccardo substituted the generic name Allescheria in 1899 [6]. Based on Costantin’s illustration and descriptions of E. gayoni, Malloch [7] concluded that it should be classified in the genus Monascus van Tiegh., 1884. Thus the genera Allescheria and Eurotiopsis became later synonyms of the genus Monascus. In 1922, a strain, isolated by M. F. Boyd from a patient with mycetoma, was considered to be closely related to but different from Eurotiopsis gayoni. It was described as a 2 Introduction new species, Allescheria boydii Shear in 1922 [8]. When the members of the ascomycete family Microascaceae were studied by Malloch, the ascomata and ascospores produced by A. boydii were found to be significantly different from those produced by either the other species of Monascus or any other genus of cleistothecial ascomycetes [7]. Malloch proposed the new genus Petriellidium in the family Microascaceae for A. boydii. Consequently, six other Petriellidium (Pe. africanum Arx & G. Franz, 1973, Pe. angustum Malloch & Cain, 1972, Pe. desertorum Arx & Moustafa, 1973, Pe. ellipsoideum Arx & Fassatiová, 1973, Pe. fimeti Arx, Mukerji & Singh, 1978 and Pe. fusoideum Arx, 1973) (throughout this chapter Pe will be used for Petriellidium, Ps for Pseudallescheria) were described in this genus [9-11]. In 1943 and again in 1944, Negroni & Fischer described the genus and species Pseudallescheria shearii (as ‘sheari’) for a cleistothecial ascomycete [12;13]. Comparing the type specimens of Petriellidium Malloch and Pseudallescheria Negroni et Fischer, McGinnis et al. indicated that these 2 genera were congeneric [4]. Because of priority, the proper name of this genus is Pseudallescheria. At that moment, a total of 7 Petriellidium species were reclassified on the basis of morphology as distinct species of Pseudallescheria (Ps. boydii, Ps. africana, Ps. angusta, Ps. desertorum, Ps. ellipsoidea, Ps. fimeti and Ps. fusoidea). Members of the genus Pseudallescheria typically produce Scedosporium or Graphimu anamorphs, or both. Until 1991, 2 anamorph species of Pseudallescheria had been accepted, which are Scedosporium apiospermum Sacc. ex Castell. & Chalmers [14] and Scedosporium prolificans (Hennebert & B.G. Desai) Guého & de Hoog [15]. The morphological circumscriptions of Ps. boydii, Ps. angusta, Ps. ellipsoidea and Ps. fusoidea are narrow. A part of isolates maintained as Ps. boydii failed to produce cleistothecia upon inspection from collection strains regardless of growth conditions. Ps. angusta, Ps. fusoidea and Ps. ellipsoidea were later reduced to synonymy with Ps. boydii (Ps. boydii complex) on the basis of identical Internal Transcribed Spacer (ITS) sequences of ribosomal DNA (rDNA) [16] and a ~300 bp fragment of the D1/D2 Large Subunit (LSU) region of rDNA [17]. The recently described species Ps. minutispora Gilgado et al., S. aurantiacum Gilgado et al. [2], and two more species proposed by Gilgado and co-workers [18] have been segregated from Ps. boydii on the basis of genealogical concordance of calmodulin, β-tubulin and ITS region of rDNA genes and phenotypic characters. At this moment, 9 species are accepted in the ascomycete genus Pseudallescheria, but thus far only few outstanding 3 Chapter 1 differences have been found in features of pathogenicity, ecology and antifungal susceptibility between the new species and Ps. boydii [2;19;20]. Excluding molecular data, species recognition still is difficult in the routine lab, and as a result existing differences may be overlooked. Therefore it is essential that more tools become available to recognize species in the genus Pseudallescheria. Exophiala J.W. Carmichael Exophiala is the main genus of
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