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CHAPTER FOUR Modern Taxonomy of Biotechnologically Important Aspergillus and Penicillium Species Jos Houbraken1, Ronald P. de Vries, Robert A. Samson CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands 1Corresponding author: e-mail address: [email protected] Contents 1. Introduction 200 2. One Fungus, One Name 202 2.1 Dual nomenclature 202 2.2 Single-name nomenclature 203 2.3 Implications for Aspergillus and Penicillium taxonomy 203 3. Classification and Phylogenetic Relationships in Trichocomaceae, Aspergillaceae, and Thermoascaceae 205 4. Taxonomy of Penicillium Species and Phenotypically Similar Genera 209 4.1 Penicillium and Talaromyces 209 4.2 Rasamsonia 215 4.3 Thermomyces 216 5. Taxonomy of Aspergillus Species 219 5.1 Phylogenetic relationships among Aspergillus species 219 5.2 Aspergillus section Nigri 219 5.3 Aspergillus section Flavi 224 6. Character Analysis 225 7. Modern Taxonomy and Genome Sequencing 227 7.1 Identity of genome-sequenced strains 230 7.2 Selection of strains 231 7.3 Recommendations for strain selection 231 8. Identification of Penicillium and Aspergillus Strains 233 9. Mating-Type Genes 234 9.1 Aspergillus 236 9.2 Penicillium 238 9.3 Other genera 239 10. Conclusions 240 Acknowledgments 240 References 241 # Advances in Applied Microbiology, Volume 86 2014 Elsevier Inc. 199 ISSN 0065-2164 All rights reserved. http://dx.doi.org/10.1016/B978-0-12-800262-9.00004-4 200 Jos Houbraken et al. Abstract Taxonomy is a dynamic discipline and name changes of fungi with biotechnological, industrial, or medical importance are often difficult to understand for researchers in the applied field. Species belonging to the genera Aspergillus and Penicillium are com- monly used or isolated, and inadequate taxonomy or uncertain nomenclature of these genera can therefore lead to tremendous confusion. Misidentification of strains used in biotechnology can be traced back to (1) recent changes in nomenclature, (2) new tax- onomic insights, including description of new species, and/or (3) incorrect identifica- tions. Changes in the recent published International Code of Nomenclature for Algae, Fungi and Plants will lead to numerous name changes of existing Aspergillus and Pen- icillium species and an overview of the current names of biotechnological important species is given. Furthermore, in (biotechnological) literature old and invalid names are still used, such as Aspergillus awamori, A. foetidus, A. kawachii, Talaromyces emersonii, Acremonium cellulolyticus, and Penicillium funiculosum. An overview of these and other species with their correct names is presented. Furthermore, the biotechnologically important species Talaromyces thermophilus is here combined in Thermomyces as Th. dupontii. The importance of Aspergillus, Penicillium, and related genera is also illustrated by the high number of undertaken genome sequencing projects. A number of these strains are incorrectly identified or atypical strains are selected for these projects. Rec- ommendations for correct strain selection are given here. Phylogenetic analysis shows a close relationship between the genome-sequenced strains of Aspergillus, Penicillium, and Monascus. Talaromyces stipitatus and T. marneffei (syn. Penicillium marneffei) are closely related to Thermomyces lanuginosus and Th. dupontii (syn. Talaromyces thermophilus), and these species appear to be distantly related to Aspergillus and Pen- icillium. In the last part of this review, an overview of heterothallic reproduction in Asper- gillus and Penicillium is given. The new insights in the taxonomy of Aspergillus, Penicillium, and related genera will help to interpret the results generated with compar- ative genomics studies or other studies dealing with evolution of, for example, enzymes, mating-type loci, virulence genes, and secondary metabolite biosynthetic gene clusters. 1. INTRODUCTION Aspergillus and Penicillium are two of the most economically important genera of fungi. These genera belong to the Aspergillaceae, a family belonging to the order Eurotiales (class Eurotiomycetes,phylumAscomycota)(Houbraken & Samson, 2011). Species belonging to this family have diverse physiological properties. Some species grow at extremely low water activities due to high sugar or salt concentrations, while others can grow at low (psychrotolerant) or high temperatures (thermotolerant), low-acidity levels, and/or low oxygen levels. Aspergillaceae are predominantly saprobic and are commonly occurring in soil; however, some are known to have a positive or negative impact on Taxonomy of Aspergillus and Penicillium 201 human activities. Positive impacts include the use of these fungi in food fermentations. For example, Penicillium camemberti and Penicillium roqueforti are used in cheese production and Penicillium nalgiovense in the production of surface ripened sausages. In Asia, a larger variation of fungal fermented foods occurs and, for instance, Aspergillus oryzae and Aspergillus sojae are used in the production of miso, sake, and soy sauce, and black Aspergilli for the produc- tion of awamori liquors and Puerh tea (Mogensen, Varga, Thrane, & Frisvad, 2009; Perrone et al., 2011). Members of Aspergillaceae also produce various bioactive extrolites (¼secondary metabolites). Some of these extrolites are known as pharmaceuticals and examples are penicillin (antibiotic, Penicillium rubens), griseofulvin (antifungal, Penicillium griseofulvum), mycophenolic acid (immunosuppressant, Penicillium brevicompactum), and lovastatin (cholesterol- lowering agent, Aspergillus terreus). Other industrial applications include the production of organic acids and enzymes. Aspergilli, in particular, are known for their production of these compounds. Citric and gluconic acid are pro- duced by Aspergillus niger, itaconic acid by A. terreus and especially members of Aspergillus section Nigri and A. oryzae arewidelyusedinextracellular enzyme production (either as donor or production organism). Less frequently exploited species for enzyme production include Aspergillus melleus, A. sojae, Talaromyces funiculosus (syn. Penicillium funiculosum), Penicillium multicolor, Rasamsonia emersonii (syn. Talaromyces emersonii), Thermoascus aurantiacus,and Thermomyces lanuginosus (van Dijck, 2008). Besides the positive interactions mentioned above, also negative aspects are linked to this family. Some species produce extrolites that can be regarded as mycotoxins and examples of regu- lated mycotoxins produced by Aspergillus and Penicillium species in food and/or feed are aflatoxins, patulin, ochratoxin, citrinin, and fumonisin (Samson, Houbraken, Thrane, Frisvad, & Andersen, 2010). In addition, Aspergillus species especially can cause a wide spectrum of diseases includ- ing mycotoxicosis, and noninvasive and invasive infections in immune- compromised patients. Aspergillus fumigatus is the principal etiological agent, but several other Aspergillus species are reported as causal agent of asper- gillosis. Other adverse responses are hypersensitivity reactions (e.g., asthma, extrinsic allergic alveolitis) due to exposure to fungal fragments. Aspergillus and Penicillium are typical indoor fungi and are among the most frequently encountered genera in indoor environments (Flannigan, Samson, & Miller, 2011; Gravesen, Nielsen, Iversen, & Nielsen, 1999). These fungi produce high quantities of dry spores which can become airborne easily, resulting in exposure of humans to high spore concentrations in the air of indoor environments. 202 Jos Houbraken et al. Naming and classifying our surroundings, especially living organisms, has likely been taking place as long as mankind has been able to communicate. The primary aim of taxonomy is to provide a classification that can be used for a wide range of purposes. It is traditionally divided into three fields: (1) classification, that is, the orderly arrangement of groups; (2) nomenclature, that is, the naming of the groups defined under 1, and (3) identification of unknown organisms, that is, the process of determining whether an organ- ism belongs to one of the groups defined in 1, and labeled in 2 (Moore, Mihaylova, Vandamme, Krichevsky, & Dijkshoorn, 2010; Schleifer & Tru¨per, 2006). Taxonomy is a dynamic discipline but inadequate taxonomy or uncertain nomenclature can lead to tremendous confusion. The recently published International Code of Nomenclature for Algae, Fungi and Plants deleted dual nomenclature, giving anamorph names the same priority as teleomorph names, leading to several name changes (Norvell, 2011). The impact of these new nomenclatural rules on the taxonomy of biotechnologically important Aspergillus and Penicillium is addressed in this chapter and the latest develop- ments regarding the phylogeny and classification of species belonging to these genera are given. The importance of Aspergillus, Penicillium, and related genera is also illustrated by the high number of genome sequencing projects undertaken. Correct species identification and the use of valid names are the first crucial steps in these projects and in this paper we identify the currently genome-sequenced strains according to the latest taxonomic schemes. 2. ONE FUNGUS, ONE NAME 2.1. Dual nomenclature Pleomorphism in fungi was first demonstrated by Tulasne (1851) and shortly after de Bary (1854) demonstrated that Eurotium herbariorum had an Aspergil- lus anamorph, while Brefeld (1874) showed with illustrations the connection between Eupenicillium and Penicillium. In spite of the trend to apply the ana- morphic name to all
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  • Development of Aspergillus Niger

    Development of Aspergillus Niger

    Studies in Mycology 74 (March 2013) Development of Aspergillus niger Jan Dijksterhuis and Han Wösten, editors CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences Development of Aspergillus niger STUDIES IN MYCOLOGY 74, 2013 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 dr hc Robert A. Samson, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] LAYOUT EDITOR Manon van den Hoeven-Verweij, CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] SCIENTIFIC EDITORS Prof. dr Dominik Begerow, Lehrstuhl für Evolution und Biodiversität der Pflanzen, Ruhr-Universität Bochum, Universitätsstr. 150, Gebäude ND 44780, Bochum, Germany. E-mail: [email protected] Prof. dr Uwe Braun, Martin-Luther-Universität, Institut für Biologie, Geobotanik und Botanischer Garten, Herbarium, Neuwerk 21, D-06099 Halle, Germany. E-mail: [email protected] Dr Paul Cannon, CABI and Royal Botanic Gardens, Kew, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, U.K. E-mail: [email protected] Prof. dr Lori Carris, Associate Professor, Department of Plant Pathology, Washington State University, Pullman, WA 99164-6340, U.S.A. E-mail: [email protected] Prof.