Phylogeny, Identification and Nomenclature of the Genus Aspergillus

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Phylogeny, Identification and Nomenclature of the Genus Aspergillus available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 78: 141–173. Phylogeny, identification and nomenclature of the genus Aspergillus R.A. Samson1*, C.M. Visagie1, J. Houbraken1, S.-B. Hong2, V. Hubka3, C.H.W. Klaassen4, G. Perrone5, K.A. Seifert6, A. Susca5, J.B. Tanney6, J. Varga7, S. Kocsube7, G. Szigeti7, T. Yaguchi8, and J.C. Frisvad9 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, NL-3584 CT Utrecht, The Netherlands; 2Korean Agricultural Culture Collection, National Academy of Agricultural Science, RDA, Suwon, South Korea; 3Department of Botany, Charles University in Prague, Prague, Czech Republic; 4Medical Microbiology & Infectious Diseases, C70 Canisius Wilhelmina Hospital, 532 SZ Nijmegen, The Netherlands; 5Institute of Sciences of Food Production National Research Council, 70126 Bari, Italy; 6Biodiversity (Mycology), Eastern Cereal and Oilseed Research Centre, Agriculture & Agri-Food Canada, Ottawa, ON K1A 0C6, Canada; 7Department of Microbiology, Faculty of Science and Informatics, University of Szeged, H-6726 Szeged, Hungary; 8Medical Mycology Research Center, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8673, Japan; 9Department of Systems Biology, Building 221, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark *Correspondence: R.A. Samson, [email protected] Abstract: Aspergillus comprises a diverse group of species based on morphological, physiological and phylogenetic characters, which significantly impact biotechnology, food production, indoor environments and human health. Aspergillus was traditionally associated with nine teleomorph genera, but phylogenetic data suggest that together with genera such as Polypaecilum, Phialosimplex, Dichotomomyces and Cristaspora, Aspergillus forms a monophyletic clade closely related to Penicillium. Changes in the International Code of Nomenclature for algae, fungi and plants resulted in the move to one name per species, meaning that a decision had to be made whether to keep Aspergillus as one big genus or to split it into several smaller genera. The International Commission of Penicillium and Aspergillus decided to keep Aspergillus instead of using smaller genera. In this paper, we present the arguments for this decision. We introduce new combinations for accepted species presently lacking an Aspergillus name and provide an updated accepted species list for the genus, now containing 339 species. To add to the scientific value of the list, we include information about living ex-type culture collection numbers and GenBank accession numbers for available representative ITS, calmodulin, β-tubulin and RPB2 se- quences. In addition, we recommend a standard working technique for Aspergillus and propose calmodulin as a secondary identification marker. Key words: Fungal identification, Phylogeny, Media, Nomenclature. Taxonomic novelties: New names: Aspergillus baarnensis Samson, Visagie & Houbraken, Aspergillus chinensis Samson, Visagie & Houbraken, Aspergillus delacroxii Samson, Visagie & Houbraken, Aspergillus jaipurensis Samson, Visagie & Houbraken, Aspergillus solicola Samson, Visagie & Houbraken; New combinations: Aspergillus arxii (Fort & Guarro) Houbraken, Visagie & Samson, Aspergillus assulatus (S.B. Hong, Frisvad & Samson) Houbraken, Visagie & Samson, Aspergillus astellatus (Fennell & Raper) Houbraken, Visagie & Samson, Aspergillus australensis (Samson, S.B. Hong & Varga) Houbraken, Visagie & Samson, Aspergillus caninus (Sigler, Deanna A. Sutton, Gibas, Summerb. & Iwen) Houbraken, Tanney, Visagie & Samson, Aspergillus capsici (J.F.H. Beyma) Houbraken, Visagie & Samson, Aspergillus cejpii (Milko) Samson, Varga, Visagie & Houbraken, Aspergillus chlamydosporus (Gene & Guarro) Houbraken, Tanney, Visagie & Samson, Aspergillus denticulatus (Samson, S.B. Hong & Frisvad) Samson, S.B. Hong, Visagie & Houbraken, Aspergillus desertorum (Samson & Mouch.) Samson, Visagie & Houbraken, Aspergillus ferenczii (Varga & Samson) Samson, Varga, Visagie & Houbraken, Aspergillus galapagensis (Frisvad, S.B. Hong & Samson) Samson, Frisvad & Houbraken, Aspergillus inflatus (Stolk & Malla) Samson, Frisvad, Varga, Visagie & Houbraken, Aspergillus insolitus (G. Sm.) Houbraken, Visagie & Samson, Aspergillus papuensis (Samson, S.B. Hong & Varga) Samson, S.B. Hong & Varga, Aspergillus pisci (A.D. Hocking & Pitt) Houbraken, Visagie & Samson, Aspergillus pluriseminatus (Stchigel & Guarro) Samson, Visagie & Houbraken, Aspergillus sclerotialis (W. Gams & Breton) Houbraken, Tanney, Visagie & Samson, Aspergillus shendaweii (Yaguchi, Abliz & Y. Horie) Samson, Visagie & Houbraken, Aspergillus similis (Y. Horie, Udagawa, Abdullah & Al-Bader) Samson, Visagie & Houbraken, Aspergillus tsunodae (Yaguchi, Abliz & Y. Horie) Samson, Visagie & Houbraken. Published online 11 September 2014; http://dx.doi.org/10.1016/j.simyco.2014.07.004. Hard copy: June 2014. INTRODUCTION teleomorph genera were traditionally linked to Aspergillus ana- morphs (Pitt et al. 2000), one of these being Eurotium Link: Fr. Aspergillus is a diverse genus with high economic and social typified by Eurotium herbariorum (Wiggers: Fr.) Link. The others impact. Species occur worldwide in various habitats and they are were Chaetosartorya Subram., Emericella Berk., Fennellia B.J. known to spoil food, produce mycotoxins and are frequently Wiley & E.G. Simmons, Hemicarpenteles A.K. Sarbhoy & Elphick reported as human and animal pathogens. Furthermore, many (now considered to belong in Penicillium; Visagie et al. 2014a), species are used in biotechnology for the production of various Neosartorya Malloch & Cain, Petromyces Malloch & Cain, metabolites such as antibiotics, organic acids, medicines or Sclerocleista Subram. (now considered distinct from Aspergillus; enzymes, or as agents in many food fermentations. The clas- Houbraken & Samson 2011) and Stilbothamnium Henn. Neo- sification and identification of Aspergillus has been based on petromyces Frisvad & Samson and Neocarpenteles Udagawa & phenotypic characters but in the last decades was strongly Uchiy. were introduced more recently by Frisvad & Samson influenced by molecular and chemotaxonomic characterisation. (2000) and Udagawa & Uchiyama (2002). Thom & Raper Micheli (1729) introduced the name Aspergillus, with Haller (1945) and Raper & Fennell (1965) published major mono- (1768) validating the genus and Fries (1832) sanctioning the graphic treatments on the genus Aspergillus and respectively generic name. Aspergillus glaucus (L.) Link [= Mucor glaucus accepted 89 and 150 species. They also disregarded tele- L. ≡ Monilia glauca (L.) Pers.] is the generic type. In total, nine omorphic names, contrary to the prevailing nomenclatural code, Studies in Mycology Peer review under responsibility of CBS-KNAW Fungal Biodiversity Centre. Copyright © 2014, CBS-KNAW Fungal Biodiversity Centre. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/3.0/). 141 SAMSON ET AL. using only the name Aspergillus. The List of “Names in Current purpureus, Neosartorya fischeri (= A. fischeri), Eurotium rubrum Use” (NCU) for the family Trichocomaceae (Pitt & Samson 1993) (= A. ruber) and A. fumigatus form a well-supported clade (98 % accepted 185 anamorphic Aspergillus names and 72 associated bootstrap value, bs) indicating the close relationship among teleomorphic names. Pitt et al. (2000) updated this list, accepting these species. Furthermore, A. ruber, A. fumigatus and 184 Aspergillus and 70 associated teleomorphic names. Both A. fischeri were placed together on a branch with moderate lists were mainly based on the morphological species concept statistical support (77 % bs), indicating that Aspergillus is current at that time. However, the move towards a polyphasic monophyletic. Similar results were found by Ogawa et al. (1997); species concept incorporating morphology, extrolite data and in their phylogeny based on 18S rDNA data, E. rubrum, most importantly phylogenetic data, meant that this list quickly N. fischeri and A. fumigatus also formed a well-supported clade became out-dated. This is not only because new species were (99 % bs), distinct from Penicillium and Monascus. Tamura et al. described since the late 1990's, but was also a reflection that (2000) determined the relationships within Aspergillus using 18S many species previously considered synonyms based on rDNA. Using a larger sample size, data indicate that Aspergillus morphology were shown to be phylogenetically distinct. Old is monophyletic, but the overall resolution was limited. names were thus often re-introduced as accepted, distinct spe- Peterson (2008) studied the phylogenetic relationships within cies. As such, we consider updating the list of accepted species Aspergillus. A phylogeny based on 5.8S rDNA, 28S rDNA and to be crucial for the taxonomic and nomenclatural stability of the RPB2 sequences resolved Aspergillus into three main Aspergillus. clades, but the relationship among these clades was not statis- The infrageneric classification of the genus Aspergillus is tically supported. These clades roughly corresponded with the traditionally based on morphological characters. Raper & Fennell subgenera of Aspergillus, with one clade including the subgenera (1965) divided the genus in 18 groups. The classification into Circumdati and Fumigati, one representing subgenus Nidulantes groups does not have any nomenclatural status and therefore and another containing members of subgenus Aspergillus. Gams et al. (1985) introduced names of
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