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A reappraisal of Aspergillus section Nidulantes with descriptions of two new sterigmatocystin-producing species

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Abstract

Aspergillus section Nidulantes is a speciose group of microscopic fungi whose species are important in indoor air quality, food spoilage, mycotoxin production and human pathogenicity. We assembled as many species from the section as possible with either type specimens or protologues for analysis. DNA sequences were obtained from up to four loci to conduct phylogenetic analysis of sect. Nidulantes and other species in subgenus Nidulantes. Comparisons of phenetic characters were made. Our goal was to recognize monophyletic taxa for section Nidulantes as well as the other taxa in the subgenus. Phylogenetic analysis indicated that sections Versicolores and Aenei formed subclades in the larger clade containing the type species of section Nidulantes. In order to maintain monophyly in section Nidulantes, we synonymized sects. Versicolores and Aenei with sect. Nidulantes. In place of sections, we have identified six subclades in sect. Nidulantes that also have shared phenetic character sets that allow for easier morphological identification of species. Earlier reports showed that standard β-tubulin primers can occasionally amplify the tubC gene rather than the benA gene they were designed for. We show that codon usage analysis can easily distinguish between these paralogues, and we provide primer pair options to allow benA amplifications. Two new sect. Nidulantes species are described from European caves, A. croceus (Spain) and A. askiburgiensis (Czech Republic). The analysis of exometabolites showed that both species are able to produce the mycotoxin sterigmatocystin and some additional compounds.

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References

  • Abad-Diaz-De-Cerio A, Fernandez-Molina JV, Ramirez-Garcia A, Sendino J, Hernando FL, Pemán J, Garaizar J, Rementeria A (2013) The aspHS gene as a new target for detecting Aspergillus fumigatus during infections by quantitative real-time PCR. Med Mycol 51:545–554. doi:10.3109/13693786.2012.756989

    Article  CAS  PubMed  Google Scholar 

  • Atlas RM (2010) Handbook of microbiological media. CRC Press, Boca Raton

    Book  Google Scholar 

  • Balajee SA, Kano R, Baddley JW, Moser SA, Marr KA, Alexander BD, Andes D, Kontoyiannis DP, Perrone G, Peterson S, Brandt ME, Pappas PG, Chiller T (2009) Molecular identification of Aspergillus species collected for the transplant-associated infection surveillance network. J Clin Microbiol 47:3138–3141. doi:10.1128/JCM.01070-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barchiesi F, Mazzocato S, Mazzanti S, Gesuita R, Skrami E, Fiorentini A, Singh N (2015) Invasive aspergillosis in liver transplant recipients: epidemiology, clinical characteristics, treatment, and outcomes in 116 cases. Liver Transpl 21:204–212. doi:10.1002/lt.24032

    Article  PubMed  Google Scholar 

  • Bennetzen JL, Hall BD (1982) Codon selection in yeast. J Biol Chem 257:3026–3031

    CAS  PubMed  Google Scholar 

  • Berkeley M (1857) Introduction to cryptogamic botany. Bailliere, London

    Book  Google Scholar 

  • Bills GF, Yue Q, Chen L, Li Y, An Z, Frisvad JC (2016) Aspergillus mulundensis sp. nov., a new species for the fungus producing the antifungal echinocandin lipopeptides, mulundocandins. J Antibiot 69:141–148. doi:10.1038/ja.2015.1105

    Article  CAS  PubMed  Google Scholar 

  • Buttner MP, Stetzenbach LD (1991) Evaluation of four aerobiological sampling methods for the retrieval of aerosolized Pseudomonas syringae. Appl Environ Microbiol 57:1268–1270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charles MP, Noyal MJ, Easow JM (2011) Invasive pulmonary aspergillosis caused by Aspergillus versicolor in a patient on mechanical ventilation. Australas Med J 4:632–634. doi:10.4066/AMJ.2011.905

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen AJ, Jiao X, Hu Y, Lu X, Gao W (2015) Mycobiota and mycotoxins in traditional medicinal seeds from China. Toxins 7:3858–3875. doi:10.3390/toxins7103858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiu YL, Liaw SJ, Wu VC, Hsueh PR (2005) Peritonitis caused by Aspergillus sydowii in a patient undergoing continuous ambulatory peritoneal dialysis. J Infect 51:e159–e161. doi:10.1016/j.jinf.2004.12.008

    Article  PubMed  Google Scholar 

  • Christensen M, States JS (1982) Aspergillus nidulans group: Aspergillus navahoensis, and a revised synoptic key. Mycologia 74:226–235. doi:10.2307/3792888

    Article  Google Scholar 

  • Crous PW, Wingfield MJ, Le Roux JJ, Richardson DM, Strasberg D, Shivas RG, Alvarado P, Edwards J, Moreno G, Sharma R, Sonawane MS, Tan YP, Alte´s A, Barasubiye T, Barnes CW, Blanchette RA, Boertmann D, Bogo A, Carlavilla JR, Cheewangkoon R, Daniel R, de Beer ZW, de Jesús Yáñez-Morales M, Duong TA, Fernández-Vicente J, Geering ADW, Guest DI, Held BW, Heykoop M, Hubka V, Ismail AM, Kajale SC, Khemmuk W, Kolarřík M, Kurli R, Lebeuf R, Lévesque CA, Lombard L, Magista D, Manjón JL, Marincowitz S, Mohedano JM, Nováková A, Oberlies NH, Otto EC, Paguigan ND, Pascoe IG, Pérez-Butrón JL, Perrone G, Rahi P, Raja HA, Rintoul T, Sanhueza RMV, Scarlett K, Shouche YS, Shuttleworth LA, Taylor PWJ, Thorn RG, Vawdrey LL, Solano-Vidal R, Voitk A, Wong PTW, Wood AR, Zamora JC, Groenewald JZ (2015) Fungal planet description sheets: 371–399. Persoonia: 264–327. doi:10.3767/003158515X690269

  • David H, Özçelik İŞ, Hofmann G, Nielsen J (2008) Analysis of Aspergillus nidulans metabolism at the genome-scale. BMC Genom 9:163. doi:10.1186/1471-2164-9-163

    Article  CAS  Google Scholar 

  • Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi, 2nd edn. IHW-Verlag, Eching

    Google Scholar 

  • Fennell DI, Raper KB (1955) New species and varieties of Aspergillus. Mycologia 47:68–89

    Article  Google Scholar 

  • Frisvad J, Gravesen S (1994) Penicillium and Aspergillus from Danish homes and working places with indoor air problems: identification and mycotoxin determination. In: Samson R, Flannigan B, Flannigan M, Verhoeff A, Adan O, Hoekstra E (eds) Health implications of fungi in indoor environments: air quality monographs, vol 2. Pergamon Press, Oxford, pp 281–290

    Google Scholar 

  • Frisvad JC, Larsen TO (2015) Chemodiversity in the genus Aspergillus. Appl Microbiol Biotechnol 99:7859–7877. doi:10.1007/s00253-015-6839-z

    Article  CAS  PubMed  Google Scholar 

  • Frisvad JC, Samson RA (2004) Emericella venezuelensis, a new species with stellate ascospores producing sterigmatocystin and aflatoxin B1. Syst Appl Microbiol 27:672–680. doi:10.1078/0723202042369910

    Article  CAS  PubMed  Google Scholar 

  • Frisvad JC, Thrane U (1987) Standardized high-performance liquid chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone retention indices and UV-VIS spectra (diode array detection). J Chromatogr A 404:195–214

    Article  CAS  Google Scholar 

  • Frisvad JC, Samson RA, Smedsgaard J (2004) Emericella astellata, a new producer of aflatoxin B1, B2 and sterigmatocystin. Lett Appl Microbiol 38:440–445. doi:10.1111/j.1472-765X.2004.01520.x

    Article  CAS  PubMed  Google Scholar 

  • Frisvad JC, Skouboe P, Samson RA (2005) Taxonomic comparison of three different groups of aflatoxin producers and a new efficient producer of aflatoxin B1, sterigmatocystin and 3-O-methylsterigmatocystin, Aspergillus rambellii sp. nov. Syst Appl Microbiol 28:442–453. doi:10.1016/j.syapm.2005.02.012

    Article  CAS  PubMed  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Batürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MÁ, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115. doi:10.1038/nature04341

    Article  CAS  PubMed  Google Scholar 

  • Gams W, Christensen M, Onions AH, Pitt JI, Samson RA (1985) Infrageneric taxa of Aspergillus. In: Samson RA, Pitt JI (eds) Advances in Penicillium and Aspergillus systematics. Plenum Press, New York, pp 55–62

    Google Scholar 

  • Garrett SD (1981) Soil fungi and soil fertility: an introduction to soil mycology, 2nd edn. Pergamon Press, Oxford

    Google Scholar 

  • Geiser DM, Taylor JW, Ritchie KB, Smith GW (1998) Cause of sea fan death in the West Indies. Nature 394:137–138. doi:10.1038/28079

    Article  CAS  Google Scholar 

  • Geiser DM, Klich MA, Frisvad JC, Peterson SW, Varga J, Samson RA (2007) The current status of species recognition and identification in Aspergillus. Stud Mycol 59:1–10. doi:10.3114/sim.2007.59.01

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gugnani HC, Vijayan VK, Tyagi P, Sharma S, Stchigel AM, Guarro J (2004) Onychomycosis due to Emericella quadrilineata. J Clin Microbiol 42:914–916. doi:10.1128/JCM.42.2.914-916.2004

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hong S-B, Kim D-H, Samson RA (2015) Aspergillus associated with meju, a fermented soybean starting material for traditional soy sauce and soybean paste in Korea. Mycobiology 43:218–224. doi:10.5941/MYCO.2015.43.3.218

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoog GS de, Guarro J, Gené J, Figueras MJ (2009) Atlas of clinical fungi, 3rd. CD-ROM ed. CBS-KNAW Fungal Biodiversity Centre, Utrecht

    Google Scholar 

  • Horie Y (1980) Ascospore ornamentation and its application to the taxonomic re-evaluation in Emericella. Trans Mycol Soc Japan 21:483–493

    Google Scholar 

  • Horie Y (1996) New and interesting species of Emericella from Chinese soil. Mycoscience 37:323–329. doi:10.1007/BF02461304

    Article  Google Scholar 

  • Horie Y (1998) Emericella appendiculata, a new species from Chinese soil. Mycoscience 39:161–165. doi:10.1007/BF02464054

    Article  Google Scholar 

  • Horie Y (2000) Emericella qinqixianii, a new species from desert soil in China. Mycoscience 41:183–187. doi:10.1007/BF02464329

    Article  Google Scholar 

  • Horie Y, Miyaji M, Nishimura K, Franco MF, Coelho KIR (1996) New and interesting species of Emericella from Brazilian soil. Mycoscience 37:137–144. doi:10.1007/BF02461338

    Article  Google Scholar 

  • Horn BW, Olarte RA, Peterson SW, Carbone I (2013) Sexual reproduction in Aspergillus tubingensis from section Nigri. Mycologia 105:1153–1163. doi:10.3852/13-101

    Article  CAS  PubMed  Google Scholar 

  • Houbraken J, Samson RA (2011) Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud Mycol 70:1–51. doi:10.3114/sim.2011.70.01

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houbraken J, Due M, Varga J, Meijer M, Frisvad JC, Samson RA (2007) Polyphasic taxonomy of Aspergillus section Usti. Stud Mycol 59:107–128. doi:10.3114/sim.2007.59.12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houbraken J, Spierenburg H, Frisvad JC (2012) Rasamsonia, a new genus comprising thermotolerant and thermophilic Talaromyces and Geosmithia species. Antonie Leeuwenhoek 101:403–421. doi:10.1007/s10482-011-9647-1

    Article  CAS  PubMed  Google Scholar 

  • Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Adv Appl Microbiol 86:199–249

    Article  PubMed  Google Scholar 

  • Hsiue H-C, Wu T-H, Chang T-C, Hsiue Y-C, Huang Y-T, Lee P-I, Hsueh P-R (2012) Culture-positive invasive aspergillosis in a medical center in Taiwan, 2000–2009. Eur J Clin Microbiol Infect Dis 31:1319–1326. doi:10.1007/s10096-011-1445-1

    Article  PubMed  Google Scholar 

  • Hubka V, Kolařík M (2012) β-tubulin paralogue tubC is frequently misidentified as the benA gene in Aspergillus section Nigri taxonomy: primer specificity testing and taxonomic consequences. Persoonia 29:1–10. doi:10.3767/003158512X658123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubka V, Kubatova A, Mallatova N, Sedlacek P, Melichar J, Skorepova M, Mencl K, Lyskova P, Sramkova B, Chudickova M, Hamal P, Kolarik M (2012) Rare and new etiological agents revealed among 178 clinical Aspergillus strains obtained from Czech patients and characterised by molecular sequencing. Med Mycol 50:601–610. doi:10.3109/13693786.2012.667578

    Article  CAS  PubMed  Google Scholar 

  • Hubka V, Kolařík M, Kubátová A, Peterson SW (2013) Taxonomical revision of Eurotium and transfer of species to Aspergillus. Mycologia 105:912–937. doi:10.3852/12-151

    Article  PubMed  Google Scholar 

  • Hubka V, Lyskova P, Frisvad JC, Peterson SW, Skorepova M, Kolarik M (2014) Aspergillus pragensis sp. nov. discovered during molecular re-identification of clinical isolates belonging to Aspergillus section Candidi. Med Mycol 52:565–576. doi:10.1093/mmy/myu022

    Article  CAS  PubMed  Google Scholar 

  • Hubka V, Nissen C, Jensen R, Arendrup M, Cmokova A, Kubatova A, Skorepova M (2015a) Discovery of a sexual stage in Trichophyton onychocola, a presumed geophilic dermatophyte isolated from toenails of patients with a history of T. rubrum onychomycosis. Med Mycol 53:798–809. doi:10.1093/mmy/myv044

    Article  PubMed  Google Scholar 

  • Hubka V, Novakova A, Kolarik M, Jurjevic Z, Peterson SW (2015b) Revision of Aspergillus section Flavipedes: seven new species and proposal of section Jani sect. nov. Mycologia 107:169–208. doi:10.3852/14-059

    Article  PubMed  Google Scholar 

  • Hubka V, Nováková A, Samson R, Houbraken J, Frisvad J, Sklenář F, Varga J, Kolařík M (2016) Aspergillus europaeus sp. nov., a widely distributed soil-borne species related to A. wentii (section Cremei). Pl Syst Evol 302:641–650. doi:10.1007/s00606-00016-01293-00607

    Article  CAS  Google Scholar 

  • Ikemura T (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Molec Biol 151:389–409. doi:10.1016/0022-2836(81)90003-6

    Article  CAS  PubMed  Google Scholar 

  • Ismail M, Abdel-Sater M, Zohri A (1995) A synoptic key to species of the Aspergillus nidulellus-Emericella assemblage common to Egypt. Mycotaxon 53:391–405

    Google Scholar 

  • Jurjević Ž, Peterson SW, Horn BW (2012) Aspergillus section Versicolores: nine new species and multilocus DNA sequence based phylogeny. IMA Fungus 3:59–79. doi:10.5598/imafungus.2012.03.01.07

    Article  PubMed  PubMed Central  Google Scholar 

  • Jurjević Ž, Peterson SW, Solfrizzo M, Peraica M (2013) Sterigmatocystin production by nine newly described Aspergillus species in section Versicolores grown on two different media. Mycotoxin Res 29:141–145. doi:10.1007/s12550-013-0160-4

    Article  PubMed  CAS  Google Scholar 

  • Jurjević Ž, Kubátová A, Kolařík M, Hubka V (2015) Taxonomy of Aspergillus section Petersonii sect. nov. encompassing indoor and soil-borne species with predominant tropical distribution. Pl Syst Evol 301:2441–2462. doi:10.1007/s00606-015-1248-4

    Article  CAS  Google Scholar 

  • Kakkar R, Mehrotra B (1971) Induced production of cleistothecia in Aspergillus unguis. Cell Molec Life Sci 27:710–711. doi:10.1007/BF02136978

    Article  CAS  Google Scholar 

  • Kane S, Pinto JM, Dadzie CK, Dawis MAC (2014) Aspergilloma caused by Aspergillus versicolor. Pediatr Infect Dis J 33:891. doi:10.1097/INF.0000000000000360

    Article  PubMed  Google Scholar 

  • Kelly KL (1964) Inter-society color council—National bureau of standards color name charts illustrated with centroid colors. US Government Printing Office, Washington

    Google Scholar 

  • Klich MA (1993) Morphological studies of Aspergillus section Versicolores and related species. Mycologia 85:100–107. doi:10.2307/3760484

    Article  Google Scholar 

  • Klich MA (2009) Health effects of Aspergillus in food and air. Toxicol Ind Health 25:657–667. doi:10.1177/0748233709348271

    Article  PubMed  Google Scholar 

  • Kozakiewicz Z (1989) Aspergillus species on stored products. Mycol Pap 161:1–188

    Google Scholar 

  • Kreisel H, Schauer F (1987) Methoden des mykologishen Laboratoriums. VEB Gustav Fischer Verlag, Jena

    Google Scholar 

  • Lacey J (1994) Aspergilli in feeds and seeds. In: Powell K, Renwick A, Peberdy J (eds) The genus Aspergillus. Springer, Berlin, pp 73–92

    Chapter  Google Scholar 

  • Lewis RE, Cahyame-Zuniga L, Leventakos K, Chamilos G, Ben-Ami R, Tamboli P, Tarrand J, Bodey GP, Luna M, Kontoyiannis DP (2013) Epidemiology and sites of involvement of invasive fungal infections in patients with haematological malignancies: a 20-year autopsy study. Mycoses 56:638–645. doi:10.1111/myc.12081

    Article  PubMed  Google Scholar 

  • Lloyd AT, Sharp PM (1991) Codon usage in Aspergillus nidulans. Mol Gen Genet 230:288–294. doi:10.1007/BF00290679

    Article  CAS  PubMed  Google Scholar 

  • Lockhart SR, Zimbeck AJ, Baddley JW, Marr KA, Andes DR, Walsh TJ, Kauffman CA, Kontoyiannis DP, Ito JI, Pappas PG (2011) In vitro echinocandin susceptibility of Aspergillus isolates from patients enrolled in the Transplant-associated Infection Surveillance Network. Antimicrob Agents Chemother 55:3944–3946. doi:10.1128/AAC.00428-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínková N, Bačkor P, Bartonička T, Blažková P, Červený J, Falteisek L, Gaisler J, Hanzal V, Horáček D, Hubálek Z, Jahelková H, Kolařík M, Korytár L, Kubátová A, Lehotská B, Lehotský R, Lučan RK, Májek O, Matějů J, Řehák Z, Šafář J, Tájek P, Tkadlec E, Uhrin M, Wagner J, Weinfurtová D, Zima J, Zukal J, Horáček I (2010) Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE 5:e13853. doi:10.1371/journal.pone.0013853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsuzawa T, Tanaka R, Horie Y, Hui Y, Abliz P, Yaguchi T (2012) The correlation among molecular phylogenetics, morphological data, and growth temperature of the genus Emericella, and a new species. Mycoscience 53:433–445. doi:10.1007/s10267-012-0188-x

    Article  Google Scholar 

  • May GS, Tsang MLS, Smith H, Fidel S, Morris NR (1987) Aspergillus nidulans β-tubulin genes are unusually divergent. Gene 55:231–243. doi:10.1016/0378-1119(87)90283-6

    Article  CAS  PubMed  Google Scholar 

  • McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J (2012) International code of nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress, Melbourne, Australia, July 2011. Regnum Vegetabile 154, Koeltz Scientific Books, Königstein

  • Negri C, Gonçalves S, Xafranski H, Bergamasco M, Aquino V, Castro P, Colombo A (2014) Cryptic and rare Aspergillus species in Brazil: prevalence in clinical samples and in vitro susceptibility to triazoles. J Clin Microbiol 52:3633–3640. doi:10.1128/JCM.01582-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nováková A (2009) Microscopic fungi isolated from the Domica Cave system (Slovak Karst National Park, Slovakia). A review. Int J Speleol 38:71–82. doi:10.5038/1827-806X.38.1.8

    Article  Google Scholar 

  • Nováková A, Hubka V, Saiz-Jimenez C, Kolarik M (2012a) Aspergillus baeticus sp. nov. and Aspergillus thesauricus sp. nov., two species in section Usti from Spanish caves. Int J Syst Evol Microbiol 62:2778–2785. doi:10.1099/ijs.0.041004-0

    Article  PubMed  Google Scholar 

  • Nováková A, Šimonovičová A, Kubátová A (2012b) List of cultivable microfungi recorded from soils, soil related substrates and underground environment of the Czech and Slovak Republics. Mycotaxon 119:1–186

    Article  Google Scholar 

  • Nováková A, Hubka V, Dudová Z, Matsuzawa T, Kubátová A, Yaguchi T, Kolařík M (2014a) New species in Aspergillus section Fumigati from reclamation sites in Wyoming (USA) and revision of A. viridinutans complex. Fungal Diversity 64:253–274. doi:10.1007/s13225-013-0262-5

    Article  Google Scholar 

  • Nováková A, Hubka V, Sáiz-Jiménez C (2014b) Microscopic fungi isolated from cave air and sediments in the Nerja Cave—preliminary results. In: Sáiz-Jiménez C (ed) The conservation of subterranean cultural heritage. CRC Press, Leiden, pp 239–245

    Google Scholar 

  • O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molec Phylogen Evol 7:103–116. doi:10.1006/mpev.1996.0376

    Article  Google Scholar 

  • O’Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471–474. doi:10.1038/nature07528

    Article  PubMed  CAS  Google Scholar 

  • Peden JF (1999) Analysis of codon usage. PhD thesis. University of Nottingham, Nottingham

  • Perri P, Campa C, Incorvaia C, Parmeggiani F, Lamberti G, Costagliola C, Sebastiani A (2005) Endogenous Aspergillus versicolor endophthalmitis in an immuno-competent HIV-positive patient. Mycopathologia 160:259–261. doi:10.1007/s11046-005-6871-0

    Article  PubMed  Google Scholar 

  • Peterson SW (1995) Phylogenetic analysis of Aspergillus sections Cremei and Wentii, based on ribosomal DNA sequences. Mycol Res 99:1349–1355. doi:10.1016/S0953-7562(09)81220-3

    Article  CAS  Google Scholar 

  • Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205–226. doi:10.3852/mycologia.100.2.205

    Article  CAS  PubMed  Google Scholar 

  • Peterson SW, Jurjević Ž (2013) Talaromyces columbinus sp. nov., and genealogical concordance analysis in Talaromyces clade 2a. PLoS ONE 8:e78084. doi:10.1371/journal.pone.0078084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson SW, Varga J, Frisvad JC, Samson RA (2008) Phylogeny and subgeneric taxonomy of Aspergillus. In: Varga J, Samson RA (eds) Aspergillus in the genomic era. Wageningen Academic Publishers, Wageningen, pp 33–56

    Google Scholar 

  • Pitt JI, Hocking AD (2009) Aspergillus and related teleomorphs. In: Pitt J, Hocking A (eds) Fungi and food spoilage, 3rd edn. Springer, London, pp 275–337

    Chapter  Google Scholar 

  • Pitt JI, Samson RA (1993) Species names in current use in the Trichocomaceae (Fungi, Eurotiales). In: Greuter W (ed) NCU-2: names in current use in the families Trichocomaceae, Cladoniaceae, Pinaceae, and Lemnaceae. Koeltz Scientific Books, Königstein, pp 13–57

    Google Scholar 

  • Pitt JI, Taylor JW (2014) Aspergillus, its sexual states, and the new International Code of Nomenclature. Mycologia 105:1051–1062. doi:10.3852/14-060

    Article  Google Scholar 

  • Polacheck I, Nagler A, Okon E, Drakos P, Plaskowitz J, Kwon-Chung KJ (1992) Aspergillus quadrilineatus, a new causative agent of fungal sinusitis. J Clin Microbiol 30:3290–3293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rank C, Nielsen KF, Larsen TO, Varga J, Samson RA, Frisvad JC (2011) Distribution of sterigmatocystin in filamentous fungi. Fungal Biol 115:406–420. doi:10.1016/j.funbio.2011.02.013

    Article  CAS  PubMed  Google Scholar 

  • Raper KB, Fennell DI (1965) The genus Aspergillus. Williams and Wilkins Co., Baltimore

    Google Scholar 

  • Rippon JW (1988) Medical mycology. The pathogenic fungi and the pathogenic actinomycetes. Saunders, Philadelphia

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rotoli M, Sascaro G, Cavalieri S (2001) Aspergillus versicolor infection of the external auditory canal successfully treated with terbinafine. Dermatology 202:143. doi:10.1159/000051618

    Article  CAS  PubMed  Google Scholar 

  • Roy K, Mukhopadhyay T, Reddy G, Desikan K, Ganguli B (1987) Mulundocandin, a new lipopeptide antibiotic. I. Taxonomy, fermentation, isolation and characterization. J Antibiot 40:275–280. doi:10.7164/antibiotics.40.275

    Article  CAS  PubMed  Google Scholar 

  • Sabino R, Veríssimo C, Parada H, Brandão J, Viegas C, Carolino E, Clemons KV, Stevens DA (2014) Molecular screening of 246 Portuguese Aspergillus isolates among different clinical and environmental sources. Med Mycol 52:519–529. doi:10.1093/mmy/myu006

    Article  CAS  PubMed  Google Scholar 

  • Samson RA (1979) A compilation of the Aspergilli described since 1965. Stud Mycol 18:1–40

    Google Scholar 

  • Samson RA, Mouchacca J (1974) Some interesting species of Emericella and Aspergillus from Egyptian desert soil. Antonie Leeuwenhoek 40:121–131. doi:10.1007/BF00394559

    Article  CAS  PubMed  Google Scholar 

  • Samson RA, Mouchacca J (1975) Additional notes on species of Aspergillus, Eurotium and Emericella from Egyptian desert soil. Antonie Leeuwenhoek 41:343–351. doi:10.1007/BF02565069

    Article  CAS  PubMed  Google Scholar 

  • Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS KNAW Biodiversity Center, Utrecht

    Google Scholar 

  • Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHV, Perrone G, Seifert KA, Tanney JB, Varga J, Yaguchi T, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173. doi:10.1016/j.simyco.2014.07.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schönborn C, Schmoranzer H (1970) Untersuchungen über schimmelpilzinfektionen der zehennägel. Mycoses 13:253–272. doi:10.1111/j.1439-0507.1970.tb01260.x

    Article  Google Scholar 

  • Schwab CJ, Straus DC (2004) The roles of Penicillium and Aspergillus in sick building syndrome. Adv Appl Microbiol 55:215–238. doi:10.1016/S0065-2164(04)55008-6

    Article  CAS  PubMed  Google Scholar 

  • Segal BH, Romani LR (2009) Invasive aspergillosis in chronic granulomatous disease. Med Mycol 47:S282–S290. doi:10.1080/13693780902736620

    Article  CAS  PubMed  Google Scholar 

  • Seyedmousavi S, Guillot J, Arné P, de Hoog GS, Mouton JW, Melchers WJ, Verweij PE (2015) Aspergillus and aspergilloses in wild and domestic animals: a global health concern with parallels to human disease. Med Mycol 53:765–797. doi:10.1093/mmy/myv067

    Article  PubMed  Google Scholar 

  • Sharma D, Capoor M, Ramesh V, Gupta S, Shivaprakash M, Chakrabarti A (2015) A rare case of onychomycosis caused by Emericella quadrilineata (Aspergillus tetrazonus). Indian J Med Microbiol 33:314–316. doi:10.4103/0255-0857.153561

    Article  CAS  PubMed  Google Scholar 

  • Shields RK, Nguyen MH, Shullo MA, Silveira FP, Kwak EJ, Abdel Massih RC, Toyoda Y, Bermudez CA, Bhama JK, Kormos RL (2012) Invasive aspergillosis among heart transplant recipients is rare but causes rapid death due to septic shock and multiple organ dysfunction syndrome. Scand J Infect Dis 44:982–986. doi:10.3109/00365548.2012.705018

    Article  PubMed  PubMed Central  Google Scholar 

  • Stchigel A, Guarro J (1997) A new species of Emericella from Indian soil. Mycologia 89:937–941. doi:10.2307/3761114

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro T, Izumikawa K, Tashiro M, Takazono T, Morinaga Y, Yamamoto K, Imamura Y, Miyazaki T, Seki M, Kakeya H (2011) Diagnostic significance of Aspergillus species isolated from respiratory samples in an adult pneumology ward. Med Mycol 49:581–587. doi:10.3109/13693786.2010.548084

    PubMed  Google Scholar 

  • Thom C, Church MB (1926) The Aspergilli. Williams and Wilkins, Baltimore

    Google Scholar 

  • Thom C, Raper KB (1945) A manual of the Aspergilli. Williams and Wilkins, Baltimore

    Google Scholar 

  • Todd RB, Davis MA, Hynes MJ (2007) Genetic manipulation of Aspergillus nidulans: Meiotic progeny for genetic analysis and strain construction. Nat Protocols 2:811–821. doi:10.1038/nprot.2007.112

    Article  CAS  PubMed  Google Scholar 

  • Torres-Rodríguez JM, Madrenys-Brunet N, Siddat M, López-Jodra O, Jimenez T (1998) Aspergillus versicolor as cause of onychomycosis: report of 12 cases and susceptibility testing to antifungal drugs. J Eur Acad Dermatol Venereol 11:25–31. doi:10.1111/j.1468-3083.1998.tb00949.x

    Article  PubMed  Google Scholar 

  • Tsang C-C, Hui TW, Lee K-C, Chen JH, Ngan AH, Tam EW, Chan JF, Wu AL, Cheung M, Brian P (2016) Genetic diversity of Aspergillus species isolated from onychomycosis and Aspergillus hongkongensis sp. nov., with implications to antifungal susceptibility testing. Diagn Microbiol Infect Dis 84:125–134. doi:10.1016/j.diagmicrobio.2015.10.027

    Article  CAS  PubMed  Google Scholar 

  • Uhrin GB, Jensen RH, Korup E, Grønlund J, Hjort U, Moser C, Arendrup MC, Schønheyder HC (2015) Recurrent prosthetic valve endocarditis caused by Aspergillus delacroxii (formerly Aspergillus nidulans var. echinulatus). Med Mycol Case Rep 10:21–23. doi:10.1016/j.mmcr.2015.12.005

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanderwolf KJ, Malloch D, McAlpine DF, Forbes GJ (2013) A world review of fungi, yeasts, and slime molds in caves. Int J Speleol 42:77–96. doi:10.5038/1827-806X.42.1.9

    Article  Google Scholar 

  • Varga J, Frisvad JC, Samson RA (2010) Aspergillus sect. Aenei sect. nov., a new section of the genus for A. karnatakaensis sp. nov. and some allied fungi. IMA Fungus 1:197–205

    Article  PubMed  PubMed Central  Google Scholar 

  • Varga J, Frisvad JC, Kocsubé S, Brankovics B, Tóth B, Szigeti G, Samson RA (2011a) New and revisited species in Aspergillus section Nigri. Stud Mycol 69:1–17. doi:10.3114/sim.2011.69.01

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varga J, Frisvad JC, Samson RA (2011b) Two new aflatoxin producing species, and an overview of Aspergillus section Flavi. Stud Mycol 69:57–80. doi:10.3114/sim.2011.69.05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verweij PE, Varga J, Houbraken J, Rijs AJMM, VerduynLunel FM, Blijlevens NMA, Shea YR, Holland SM, Warris A, Melchers WJG, Samson RA (2008) Emericella quadrilineata as cause of invasive aspergillosis. Emerg Infect Dis 14:566–572. doi:10.3201/eid1404.071157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visagie C, Houbraken J, Frisvad JC, Hong S-B, Klaassen C, Perrone G, Seifert K, Varga J, Yaguchi T, Samson R (2014a) Identification and nomenclature of the genus Penicillium. Stud Mycol 78:343–371. doi:10.1016/j.simyco.2014.09.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visagie CM, Hirooka Y, Tanney JB, Whitfield E, Mwange K, Meijer M, Amend AS, Seifert KA, Samson RA (2014b) Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Stud Mycol 78:63–139. doi:10.1016/j.simyco.2014.07.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visagie CM, Varga J, Houbraken J, Meijer M, Kocsube S, Yilmaz N, Fotedar R, Seifert KA, Frisvad JC, Samson RA (2014c) Ochratoxin production and taxonomy of the yellow aspergilli (Aspergillus section Circumdati). Stud Mycol 78:1–61. doi:10.1016/j.simyco.2014.07.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Mu X, Li R (2013) Invasive pulmonary aspergillosis due to Emericella nidulans var. echinulata, successfully cured by voriconazole and micafungin. J Clin Microbiol 51:1327–1329. doi:10.1128/JCM.02487-12

    Article  PubMed  PubMed Central  Google Scholar 

  • Zalar P, Frisvad JC, Gunde-Cimerman N, Varga J, Samson RA (2008) Four new species of Emericella from the Mediterranean region of Europe. Mycologia 100:779–795. doi:10.3852/08-078

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Ministry of Education, Youth and Sports of the Czech Republic (SVV project) and by the project “BIOCEV—Biotechnology and Biomedicine Centre of the Academy of Sciences and Charles University” (CZ.1.05/1.1.00/02.0109) from the European Regional Development Fund. Molecular genetic analyses were supported by the projects of Charles University Grant Agency (GAUK 1130214). The survey in European caves was supported through a grant from the Czech Science Foundation (Grant No. P506-12-1064). Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer. Prof Karol Marhold’s consultation on nomenclatural issues is gratefully acknowledged. We thank Dr M. Chudíčková and A. Gabrielová, for their invaluable assistance in laboratory, and Dr Ž. Jurjević for valuable comments.

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Authors and Affiliations

  1. Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, 128 01, Prague 2, Czech Republic

    Vit Hubka, František Sklenář, Alena Kubátová & Miroslav Kolařík

  2. Institute of Microbiology AS CR, v.v.i., Vídeňská 1083, 142 20, Prague 4, Czech Republic

    Vit Hubka, Alena Nováková, František Sklenář & Miroslav Kolařík

  3. Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, 1815 North University Street, Peoria, IL, 61604, USA

    Stephen W. Peterson

  4. DTU Systems Biology, Technical University of Denmark, Søltofts Plads, Bldg. 221, 2800, Kgs. Lyngby, Denmark

    Jens C. Frisvad

  5. University of Nagasaki, 1-1-1 Manabino, Nagayo-cho, Nishi-Sonogi-gun, Nagasaki, 851-2195, Japan

    Tetsuhiro Matsuzawa

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Online Resource 1. Alignment of partial β-tubulin, calmodulin and RPB2 genes (coding regions only) used for reconstruction of tree on Fig. 1.

Online Resource 2. Alignment of ITS rDNA, β-tubulin, calmodulin and RPB2 genes used for reconstruction of tree on Fig. 2.

Online Resource 3. Alignment of partial β-tubulin gene used for reconstruction of tree on Fig. 3.

Online Resource 4. Alignment of partial β-tubulin gene used for reconstruction of tree on Fig. 4.

Online Resource 5. Alignment of partial calmodulin gene used for reconstruction of tree on Fig. 4.

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Hubka, V., Nováková, A., Peterson, S.W. et al. A reappraisal of Aspergillus section Nidulantes with descriptions of two new sterigmatocystin-producing species. Plant Syst Evol 302, 1267–1299 (2016). https://doi.org/10.1007/s00606-016-1331-5

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