Aspergillus is one of the economically most important fungal genera. Recently, the ICN adopted the single name nomenclature which has forced mycologists to choose one name for fungi (e.g. Aspergillus, Fusarium, Penicillium, etc.). Previously two proposals for the single name nomenclature in Aspergillus were presented: one attributes the name "Aspergillus" to clades comprising seven different teleomorphic names, by supporting the monophyly of this genus; the other proposes that Aspergillus is a non-monophyletic genus, by preserving the Aspergillus name only to species belonging to subgenus Circumdati and maintaining the sexual names in the other clades. The aim of our study was to test the monophyly of Aspergilli by two independent phylogenetic analyses using a multilocus phylogenetic approach. One test was run on the publicly available coding regions of six genes (RPB1, RPB2, Tsr1, Cct8, BenA, CaM), using 96 species of Penicillium, Aspergillus and related taxa. Bayesian (MrBayes) and Ultrafast Maximum Likelihood (IQ-Tree) and Rapid Maximum Likelihood (RaxML) analyses gave the same conclusion highly supporting the monophyly of Aspergillus. The other analyses were also performed by using publicly available data of the coding sequences of nine loci (18S rRNA, 5,8S rRNA, 28S rRNA (D1-D2), RPB1, RPB2, CaM, BenA, Tsr1, Cct8) of 204 different species. Both Bayesian (MrBayes) and Maximum Likelihood (RAxML) trees obtained by this second round of independent analyses strongly supported the monophyly of the genus Aspergillus. The stability test also confirmed the robustness of the results obtained. In conclusion, statistical analyses have rejected the hypothesis that the Aspergilli are non-monophyletic, and provided robust arguments that the genus is monophyletic and clearly separated from the monophyletic genus Penicillium. There is no phylogenetic evidence to split Aspergillus into several genera and the name Aspergillus can be used for all the species belonging to Aspergillus i.e. the clade comprising the subgenera Aspergillus, Circumdati, Fumigati, Nidulantes, section Cremei and certain species which were formerly part of the genera Phialosimplex and Polypaecilum. Section Cremei and the clade containing Polypaecilum and Phialosimplex are proposed as new subgenera of Aspergillus. The phylogenetic analysis also clearly shows that Aspergillus clavatoflavus and A. zonatus do not belong to the genus Aspergillus. Aspergillus clavatoflavus is therefore transferred to a new genus Aspergillago as Aspergillago clavatoflavus and A. zonatus was transferred to Penicilliopsis as P. zonata. The subgenera of Aspergillus share similar extrolite profiles indicating that the genus is one large genus from a chemotaxonomical point of view. Morphological and ecophysiological characteristics of the species also strongly indicate that Aspergillus is a polythetic class in phenotypic characters.

CBS KNAW Fungal Biodiversity Centre Utrecht The Netherlands

Department of Biotechnology and Biomedicine Technical University of Denmark Kongens Lyngby Denmark

Department of Botany Charles University Prague Prague Czech Republic

Dept of Microbiology Faculty of Science and Informatics University of Szeged Szeged Hungary

Institute of Sciences of Food Production National Research Council Bari Italy

Korean Agricultural Culture Collection National Institute of Agricultural Science 166 Nongsaengmyeong ro Iseo myeon Wanju gun Jeollabuk do 55365 Republic of Korea

Zobrazit více v PubMed

Aberer A.J., Krompass D., Stamatakis A. Pruning rogue taxa improves phylogenetic accuracy: an efficient algorithm and webservice. Systematic Biology. 2013;62:162–166. PubMed PMC

Anisimova M., Gil M., Dufayard J.F. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology. 2011;60:685–699. PubMed PMC

Bhat B., Harrison S.M., Lamont H.M. The biosynthesis of the mould metabolites roquefortine and aszonalenin from L-[2,4,5,6,7-2H5]tryptophan. Tetrahedron. 1993;49:10663–10668.

Borchsenius F. FastGap 1.2. Department of Biosciences, Aarhus University, Denmark. 2009. http://www.aubot.dk/FastGap_home.htm Published online at:

Borg I., Groenen P. Springer-Verlag; Heidelberg: 1997. Modern multidimensional scaling.

Chang J.M., Di Tommaso P., Lefort V. TCS: a web server for multiple sequence alignment evaluation and phylogenetic reconstruction. Nucleic Acids Reserch. 2015;43:W3–W6. PubMed PMC

Chernomor O.A., von Haeseler A., Minh B.Q. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology. 2016 PubMed PMC

Darriba D., Taboada G.L., Doallo R. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods. 2012;30:772. PubMed PMC

El Kady I., El Maraghy S., Zsohri A.N. Mycotoxin producing potential of some isolates of Aspergillus flavus and Eurotium groups from meat products. Microbiological Research. 1994;149:297–307. PubMed

Fan Z., Sun Z.-H., Liy Z. Dichotocejpins A-C; new diketopiperazines from a deep-sea derived fungus Dichotomomyces cejpii FS110. Marine Drugs. 2016;14 PubMed PMC

Frisvad J.C., Larsen T.O. Chemodiversity in the genus Aspergillus. Applied Microbiology and Biotechnology. 2015;99:7859–7877. PubMed

Frisvad J.C., Larsen T.O. Extrolites of Aspergillus fumigatus and other pathogenic species in Aspergillus section Fumigati. Frontiers in Microbiology. 2016;6 PubMed PMC

Frisvad J.C., Samson R.A. Emericella venezuelensis, a new species with stellate ascospores producing sterigmatocystin and aflatoxin B1. Systematic and Applied Microbiology. 2004;27:672–680. PubMed

Frisvad J.C., Thrane U. Standardized high-performance liquid chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone indices and UV–VIS spectra (diode-array detection) Journal of Chromatography. 1987;404:195–214. PubMed

Frisvad J.C., Rank C., Nielsen K.F. Metabolomics of Aspergillus fumigatus. Medical Mycology. 2009;47:S53–S71. PubMed

Greiner K., Peršoh D., Weig A. Phialosimplex salinarum, a new species of Eurotiomycetes from a hypersaline habitat. IMA Fungus. 2014;5:161–172. PubMed PMC

Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology. 2003;52:696–704. PubMed

Guindon S., Dufayard J.F., Lefort V. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology. 2010;59:307–321. PubMed

Harms H., Rempel V., Kehraus S. Indoloterpenes from a marine-derived fungal strain of Dichotomomyces cejpii with antagonistic activity at GRR18 and cannabinoid receptors. Journal of Natural Products. 2014;77:673–677. PubMed

Harms H., Orlikova B., Seungwon J. Epipolythiodiketopiperazines from the marine derived fungus Dichotomomyces cejpii with NF-κB inhibitory potential. Marine Drugs. 2015;13:4949–4966. PubMed PMC

Harms H., Kehraus S., Nesaei-Mosaferan D. Ab-42 lowering agents from the marine-derived fungus Dichotomomyces cejpii. Steroids. 2015;104:182–188. PubMed

Hillis D.M., Heath T.A., St John K. Analysis and visualization of tree space. Systematic Biology. 2005;54:471–482. PubMed

Houbraken J., de Vries R.P., Samson R.A. Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Advances in Applied Microbiology. 2014;86:199–249. PubMed

Houbraken J., Samson R.A. Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Studies in Mycology. 2011;70:1–51. PubMed PMC

Houbraken J., Wang L., Lee H.B. New sections in Penicillium containing novel species producing patulin, pyripyropens or other bioactive compounds. Persoonia: Molecular Phylogeny and Evolution of Fungi. 2015;36:299–314. PubMed PMC

Hsieh H.-M., Ju Y.-M. Penicilliopsis pseudocordyceps, the holomorph of Pseudocordyceps seminicola, and notes on Penicilliopsis clavariaeformis. Mycologia. 2002;94:539–544. PubMed

Hubka V., Nováková A., Kolarík A. Revision of Aspergillus section Flavipedes: seven new species and proposal of section Jani sect. nov. Mycologia. 2014;107:169–208. PubMed

Jesenska Z., Pieckova E., Bernat D. Heat-resistance fungi in the soil. International Journal of Food Microbiology. 1992;16:209–214. PubMed

Jesenska Z., Pieckova E., Bernat D. Heat-resistance of fungi from soil. International Journal of Food Microbiology. 1993;19:187–192. PubMed

Jurjevic Ž., Kubátová A., Kolařík M. Taxonomy of Aspergillus section Petersonii sect. nov. encompassing indoor and soil-borne species with predominant tropical distribution. Plant Systematics and Evolution. 2015;301:2441–2462.

Katsube Y., Kimura Y., Hamasaki T. Structure of aszonapyrojne A monomethyl ether-1, a derivative of aszonapyrone A, produced by Aspergillus zonatus. Agricultural and Biological Chemistry. 1985;49:551–553.

Kepler R.M., Humber R.A., Bischoff J.F. Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia. 2014;106:811–829. PubMed

Kimura Y., Hamasaki T., Nakajima H. Structure of aszonalenin, a new metabolite of Aspergillus zonatus. Tetrahedron Letters. 1982;23:225–228.

Kimura Y., Hamasaki T., Isogai A. Structure of aszonapyrone, a new metabolite produced by Aspergillus zonatus. Agricultural and Biological Chemistry. 1982;46:1963–1965.

Kimura Y., Nishibe M., Nakajima H. Emeniveol; a new pollen growth inhibitor from the fungus, Emericella nivea. Tetrahedron Letters. 1992;33:6987–6990.

Kitahara N., Endo A. Xanthocillin X monomethyl ether, a potent inhibitor of prostaglandin biosynthesis. Journal of Antibiotics. 1981;34:1556–1561. PubMed

Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution. 2016;33:1870–1874. PubMed PMC

Lanfear R., Calcott B., Ho S.Y. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution. 2012;29:1695–1701. PubMed

Larsen T.O., Smedsgaard J., Nielsen K.F. Production of mycotoxins by Aspergillus lentulus and other medically important and closely related species in section Fumigati. Medical Mycology. 2007;45:225–232. PubMed

Lingoes J.C., Roskam E.E., Borg I. 2nd edn. Mathesis Press; Ann Arbor, Michigan: 1979. Geometric representations of relational data.

Löytynoja A. Phylogeny-aware alignment with PRANK. Methods in Molecular Biology. 2014;1079:155–170. PubMed

Ma Y-M., Liang X-A., Zhang H-C. Cytotoxic and antibiotic cyclic pentapeptide from an endophytic Aspergillus tamarii of Ficus carica. Journal of Agricultural and Food Chemistry. 2016;64:3789–3793. PubMed

Maddison W.P., Maddison D.R. Mesquite: a modular system for evolutionary analysis. Version 3.10. 2016. http://mesquiteproject.org

McNeill J., Barrie F.R., Buck W.R. International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) Regnum Vegetabile. 2012;154:208.

Micheli P.A. Nova plantarum genera; 1729.

Miller M.A., Pfeiffer W., Schwartz T. Gateway Computing Environments Workshop (GCE), IEEE. 2010. Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees; pp. 1–8.

Minh B.Q., Nguyen M.A.T., von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution. 2013;30:1188–1195. PubMed PMC

Nguyen L.T., Schmidt H.A., von Haeseler A. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution. 2015;32:268–274. PubMed PMC

Nielsen K.F., Månsson M., Rank C. Dereplication of microbial natural products by LC-DAD-TOFMS. Journal of Natural Products. 2011;74:2338–2348. PubMed

Nielsen K.F., Mogensen J.M., Johansen M. Review of secondary metabolites and mycotoxins from the Aspergillus niger group. Analytical and Bioanalytical Chemistry. 2009;395:1225–1242. PubMed

Nozawa K., Nakajima S., Kawai K. Isolation and structures of indoloditerpenes, possible biosynthetic intermediates to the tremorgenic mycotoxin, paxillin, from Emericella striata. Journal of the Chemical Society Perkin Transactions I. 1988;1988:2607–2610.

Ogata M., Ueda J., Hoshi M. A novel indole-diterpenoid, JBIR-03 with anti-MSRA activity from Dichotomomyces cejpii var. cejpii NBRC 103559. Journal of Antibiotics. 2007;60:645–648. PubMed

Peterson S.W. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia. 2008;100:205–226. PubMed

Peterson S.W., Jurjevic Z., Bills G.F. Genus Hamigera, six new species and multilocus DNA sequence based phylogeny. Mycologia. 2010;102:847–864. PubMed

Piñar G., Dalnodar D., Voiti C. Biodeterioration risk threatens the 3100 year old staircase of Hallstatt (Austria): possible involvement of halophilic microorganisms. PLOS ONE. 2016;11:e0148279. PubMed PMC

Piñar G., Tafer H., Sterflinger K. Amid the possible causes of a very famous foxing: molecular and microscopic insight into Leonardo da Vinci’s self-portrait. Environmental Microbiology Reports. 2015;7:849–859. PubMed PMC

Pitt J.I., Taylor J.W. Aspergillus, its sexual states, and the new International Code of Nomenclature. Mycologia. 2014;106:1051–1052. PubMed

Pitt J.I., Taylor J.W. (2441) Proposal to conserve the name Aspergillus (Fungi: Eurotiales: Trichocomaceae) with a conserved type to maintain also the name Eurotium. Taxon. 2016;65:631–632.

Qiao M.-F., Ji N.-Y., Liu X.-H. Asporyergosterol, a new steroid from an algicolous isolate of Aspergillus oryzae. Natural Products Communications. 2010;5:1575–1578. PubMed

Qiao M.-F., Ji N.-Y., Liu X.-H. Indoloterpenes from an algicolous isolate of Aspergillus oryzae. Bioorganic and Medicinal Chemistry Letters. 2010;20:5677–5680. PubMed

R Core Team . R Foundation for Statistical Computing; Vienna, Austria: 2016. R: a language and environment for statistical computing.https://www.R-project.org/

Rambaut A., Suchard M.A., Xie D. Tracer v. 1.6. 2014. http://beast.bio.ed.ac.uk/Tracer

Raper K.B., Fennell D.I. Williams & Wilkins; Baltimore: 1965. The genus Aspergillus.

Robinson D.F., Foulds L.R. Comparison of weighted labeled trees. Lecture Notes in Mathematics. 1979;748:119–126.

Robinson D.F., Foulds L.R. Comparison of phylogenetic trees. Mathematical Biosciences. 1981;53:131–147.

Rodrigues B.S.F., Sahm B.D.B., Jimenez P.C. Bioprospection of cytotoxic compounds in fungal strains recovered from sediments of the Brazilian coast. Chemistry & Biodiversity. 2015;12:432–442. PubMed

Ronquist F., Teslenko M., van der Mark P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology. 2012;61:539–542. PubMed PMC

Samson R.A., Houbraken J.A.M.P., Kuijpers A.F.A. New ochratoxin or sclerotium producing species in Aspergillus section Nigri. Studies in Mycology. 2004;50:45–61.

Samson R.A., Seifert K.A. The ascomycete genus Penicilliopsis and its anamorphs. In: Samson R.A., Pitt J.I., editors. Advances in Penicillium and Aspergillus systematic. Plenum Press; New York, USA: 1985. pp. 397–426.

Samson R.A., Visagie C.M., Houbraken J. Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology. 2014;78:141–173. PubMed PMC

Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics. 2001;17:1246–1247. PubMed

Sigler L., Sutton D.A., Gibas C.F.C. Phialosimplex, a new anamorphic genus associated with infections in dogs and having phylogenetic affinity to the Trichocomaceae. Medical Mycology. 2010;48:335–345. PubMed

Silvestro D., Michalak I. raxmlGUI: a graphical front-end for RAxML. Organisms Diversity and Evolution. 2012;12:335–337.

Slack G., Puniani E., Frisvad J.C. Secondary metabolites from Eurotium species, A. calidoustus and A. insuetus common in Canadian homes with a review of their chemistry and biological activities. Mycological Research. 2009;113:480–490. PubMed

Smedsgaard J. Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. Journal of Chromatography A. 1997;760:264–270. PubMed

Smith G. Polypaecilum gen. nov. Transactions of the British Mycological Society. 1961;44:437–440.

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. PubMed PMC

Stephens T.G., Bhattacharya D., Ragan M.A. PhySortR: a fast, flexible tool for sorting phylogenetic trees in R. PeerJ. 2016;4:e2038. PubMed PMC

Sukumaran J., Holder M.T. DendroPy: a Python library for phylogenetic computing. Bioinformatics. 2010;26:1569–1571. PubMed

Taylor J.W., Göker M., Pitt J.I. Choosing one name for pleomorphic fungi: the example of Aspergillus versus Eurotium, Neosartorya and Emericella. Taxon. 2016;65:593–601.

Throckmorton K., Wiemann P., Keller N.P. Evolution of chemical diversity in a group of non-reduced polyketide gene clusters: using phylogenetics to inform the search for novel natural products. Toxins. 2015;7:3572–3607. PubMed PMC

Vaidya G., Lohman D.J., Meier R. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics. 2011;27:171–180. PubMed

Varga J., Due M., Frisvad J.C. Taxonomic revision of Aspergillus section Clavati based on molecular, morphological and physiological data. Studies in Mycology. 2007;59:89–106. PubMed PMC

Varga J., Frisvad J.C., Samson R.A. Two new aflatoxin producing species, and an overview of Aspergillus section Flavi. Studies in Mycology. 2011;69:57–80. PubMed PMC

Vellinga E.C., Kuyper T.W., Ammirati J. Six simple guidelines for introducing new genera of fungi. IMA Fungus. 2015;6:65–68.

Visagie C.M., Houbraken J., Frisvad J.C. Identification and nomenclature of the genus Penicillium. Studies in Mycology. 2014;78:343–371. PubMed PMC

Wheeler K.A., Hocking A.D. Interactions among xerophilic fungi associated with dried salted fish. Journal of Applied Bacteriology. 1993;74:164–169. PubMed

Wheeler K.A., Hocking A.D., Pitt J.I. Influence of temperature on the water relations on Polypaecilum pisce and Basipetospora halophila, two halophilic fungi. Journal of General Microbiology. 1988;134:2255–2260.

Yilmaz N., Visagie C.M., Houbraken J. Polyphasic taxonomy of the genus. Talaromyces. Studies in Mycology. 2014;78:175–341. PubMed PMC

Young F.W., Hamer R.M. Erlbaum; New York: 1987. Multidimensional scaling: history, theory and applications.

Zhang N., Rossman A.Y., Seifert K. American Phytopathological Society; St. Paul: 2013. Impacts of the International Code of Nomenclature for algae, fungi and plants (Melbourne Code) on the scientific names of plant pathogenic fungi. Online. APSnet Feature.

Zuck K.M., Shipley S., Newman D.J. Induced production of N-formyl alkaloids from Aspergillus fumigatus by co-culture with Streptomyces peuceticus. Journal of Natural Products. 2011;74:1653–1657. PubMed

A review of recently introduced Aspergillus, Penicillium, Talaromyces and other Eurotiales species

A conceptual framework for nomenclatural stability and validity of medically important fungi: a proposed global consensus guideline for fungal name changes supported by ABP, ASM, CLSI, ECMM, ESCMID-EFISG, EUCAST-AFST, FDLC, IDSA, ISHAM, MMSA, and MSGERC

Reducing the number of accepted species in Aspergillus series Nigri

Re-examination of species limits in Aspergillus section Flavipedes using advanced species delimitation methods and description of four new species

Genetic Diversity, Ochratoxin A and Fumonisin Profiles of Strains of Aspergillus Section Nigri Isolated from Dried Vine Fruits

Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): An overview of families, genera, subgenera, sections, series and species

Unravelling species boundaries in the Aspergillus viridinutans complex (section Fumigati): opportunistic human and animal pathogens capable of interspecific hybridization

Phylogeny of xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section Restricti

Polyphasic taxonomy of Aspergillus section Aspergillus (formerly Eurotium), and its occurrence in indoor environments and food