Studies in Mycology 61 (2008) Black fungal extremes Edited by G.S. de Hoog and M. Grube CBS Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences Black fungal extremes STUDIE S IN MYCOLOGY 61, 2008 Studies in Mycology The Studies in Mycology is an international journal which publishes systematic monographs of filamentous fungi and yeasts, and in rare occasions the proceedings of special meetings related to all fields of mycology, biotechnology, ecology, molecular biology, pathology and systematics. For instructions for authors see www.cbs.knaw.nl. EXECUTIVE EDITOR Prof. dr Robert A. Samson, CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] LAYOUT EDITOR S Manon van den Hoeven-Verweij, CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Kasper Luijsterburg, CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] SCIENTIFIC EDITOR S Prof. dr Uwe Braun, Martin-Luther-Universität, Institut für Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, D-06099 Halle, Germany. E-mail: [email protected] Prof. dr Pedro W. Crous, CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr David M. Geiser, Department of Plant Pathology, 121 Buckhout Laboratory, Pennsylvania State University, University Park, PA, U.S.A. 16802. E-mail: [email protected] Dr Lorelei L. Norvell, Pacific Northwest Mycology Service, 6720 NW Skyline Blvd, Portland, OR, U.S.A. 97229-1309. E-mail: [email protected] Dr Erast Parmasto, Institute of Zoology & Botany, 181 Riia Street, Tartu, Estonia EE-51014. E-mail: [email protected] Prof. dr Alan J.L. Phillips, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta de Torre, 2829-516 Caparica, Portugal. E-mail: [email protected] Dr Amy Y. Rossman, Rm 304, Bldg 011A, Systematic Mycology & Microbiology Laboratory, Beltsville, MD, U.S.A. 20705. E-mail: [email protected] Dr Keith A. Seifert, Research Scientist / Biodiversity (Mycology and Botany), Agriculture & Agri-Food Canada, KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, Canada K1A OC6. E-mail: [email protected] Prof. dr Jeffrey K. Stone, Department of Botany & Plant Pathology, Cordley 2082, Oregon State University, Corvallis, OR, U.S.A. 97331-2902. E-mail: [email protected] Dr Richard C. Summerbell, 27 Hillcrest Park, Toronto, Ont. M4X 1E8, Canada. E-mail: [email protected] Copyright 2008 CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. You are free to share — to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by- nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author"s moral rights. Publication date: 18 December 2008 Published and distributed by CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. Internet: www.cbs.knaw.nl. E-mail: [email protected]. ISBN/EAN : 978-90-70351-73-1 Online ISSN : 1872-9797 Print ISSN : 0166-0616 Cover: Images of various habitats on black yeast-like fungi. Top from left to right: flying foxes at temple of Chachoengsao province, Thailand, the hypothesized natural niche of Exophiala dermatitidis. Saltpans at Sečovlje, Slovenia, the natural habitat of Hortaea werneckii. Gas station, The Netherlands, human- made habitat of Cladophialophora immunda. Bottom from left to right: rock formations in the McMurdo Dry Valley, Antarctica, one of the natural habitats of Recurvomyces mirabilis. Human foot with lesions of Coniosporium epidermidis. Sea ice from Kongsvegen glacier in Spitsbergen, natural habitat of Aureobasidium pullulans var. subglaciale. Black fungal extremes edited by G. S. de Hoog CBS Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands M. Grube Institute of Plant Sciences, Karl-Franzens-University, Holteigasse 6, 010 Graz, Austria CBS Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences PREFACE The terms "black fungi" or "dematiaceous fungi" are practical tags that recall the early days of mycological classification. At the beginning of the 19th century the grouping of anamorphic fungi relied on characters that were easy to observe with minimal optical equipment, such as colour mycelial. Since these times, and till today, hyphomycetes producing olive-grey, brown or black pigment in their cell wall or conidia are classified as "dematiaceous fungi" (referring to the meanwhile obsolete genus Dematium, originally introduced for black, clumpy fungi). The dark pigments are presumed to be DHN-like (dihydroxynaphthalene) melanins, although biochemical and structural characterisation has not always been achieved and may involve various precursor molecules. It has now become clear that black fungi do not comprise a single phylogenetic lineage, but stem from divergent branches of the fungal tree of life. The lineages share production of melanin-like pigments, which has had profound evolutionary consequences for these groups. In human- and phytopathogenic fungi melanins are linked to increased virulence. Melanins also provide protection from a broad range of environmental stress conditions. With their adaptive potential to uncommon habitats, black fungi have raised increasing interest of mycologists in medical sciences as well as in environmental ecology. It has become clear that a comprehensive understanding of black fungal evolution, ecology and functionality requires a synergic interdisciplinary approach, supported by a cooperative effort among specialists. A first step to bundle the interests in black fungi and to create a common forum was the foundation of a Working Group "Black Yeasts" under auspices of the International Society for Human and Animal Mycology (ISHAM). A small-scale meeting was held in Graz, Austria (May 30–June 1, 2006), and focused on the extremophilic ecology of black fungi. The growing interest in the topic was reflected in the second workshop held in Utrecht, The Netherlands (April 26–28, 2007), jointly with the ISHAM-affiliated Working Group on "Chromoblastomycosis", with 55 participants from 19 countries. The workshops helped to further establish the scientific network among fundamental scientists, clinicians and workers in applied fields. Oral contributions at the Utrecht workshop covered such diverse topics as human infections, diseases on cold-blooded animals, fungi growing in lichens or on rock under extreme climatic conditions, fungal use in bioremediation of polluted environments, and black yeasts in drinking water, but also susceptibility testing, and molecular evolution. Nearly all contributions included new material and quickly the idea was born that this information would be valuable to be published in a coherent fashion. For the majority of the medical papers we refer to the journal "Medical Mycology", issue 46(1), 2009. The present issue of Studies in Mycology entitled "Black Fungal Extremes" reveals unexpected types of ecology, such as growth in Arctic glaciers, Mediterranean rock, in lichens, in pure acid, and in nearly saturated salt solutions. Other papers investigate the evolutionary origins of black fungi, expression of relevant genes, medical aspects, and technical advances in culturing techniques. This interdisciplinary blend of approaches gives an insight in current research on black fungi. We hope that the present issue will attract the interest of more mycologists, who will join in our initiative to shed more light on the fascinating biology of extremophilic and pathogenic black fungi. The Editors November 2008 The papers in this issue of Studies in Mycology emerged from a workshop organised by the Working Groups on Black Yeasts and on Chromoblastomycosis, under auspices of the non-profit organisation “International Society for Human and Animal Mycology” (ISHAM). All authors report no conflicts of interest. The authors alone are responsible for the content and writing of the papers. PREFACE The terms "black fungi" or "dematiaceous fungi" are practical tags that recall the early days of mycological classification. At the beginning of the 19th century the grouping of anamorphic fungi relied on characters that were easy to observe with minimal optical equipment, such as colour mycelial. Since these times, and till today, hyphomycetes producing olive-grey, brown or black pigment in their cell wall or conidia are classified as "dematiaceous fungi" (referring to the meanwhile obsolete genus Dematium, originally introduced for black, clumpy fungi). The dark pigments are presumed to be DHN-like (dihydroxynaphthalene) melanins, although biochemical and structural characterisation has not always been achieved and may involve various precursor molecules. It has now become clear that black fungi do not comprise a single