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New species in Aspergillus section Fumigati from reclamation sites in Wyoming (U.S.A.) and revision of A. viridinutans complex

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Abstract

The Aspergillus viridinutans complex includes morphologically similar, soil-inhabiting species. Although its species boundaries have not been fully defined, many isolates from the complex have been isolated as opportunistic human and animal pathogens. In the present study, these species were dominant in spoil sites subjected to various types of reclamation management after coal mining. These species were characterised using two different PCR-fingerprinting methods, sequence data from the β-tubulin (benA) and calmodulin (caM) genes, macro- and micromorphology (optical and scanning electron microscopy), maximum growth temperatures and mating experiments. In addition, RNA polymerase II gene (RPB2), actin (act1) and ITS sequences were deposited for the ex-type isolates of newly described species. The mating experiment results, phylogenetic analyses and ascospore morphology suggested the presence of five species in the A. viridinutans complex. Aspergillus aureolus (syn. Neosartorya aureola) was the only homothallic species. Three species, A. felis, A. udagawae (syn. N. udagawae) and A. wyomingensis sp. nov., were heterothallic and their morphologically distinguishable teleomorph was induced by systematic mating experiments. Aspergillus viridinutans s. str. seems to be a very rare species and was represented only by the ex-type isolate in which the MAT1-1 locus was amplified. Aspegillus viridinutans and A. aureolus were typified in accordance with the rules of the new botanical code. Other species outside the A. viridinutans complex isolated from the reclamation sites were A. fumigatiaffinis and A. lentulus as well as two new sister species, A. brevistipitatus sp. nov. and A. conversis sp. nov. which were closely related each to other and to N. papuensis. Both new species are phylogenetically distant from all anamorphic species and resemble A. brevipes, A. duricaulis and A. unilateralis in micromorphology and are distinguishable from each other by the slower growth of A. conversis on all tested media. Interestingly, no isolate from the reclamation sites represented A. fumigatus s. str. which is usually reported as the dominant species from the section Fumigati in soil.

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References

  • Alcazar-Fuoli L, Mellado E, Aslastruey-Izquierdo A, Cuenca-Estrella M, Rodriguez-Tudela JL (2008) Aspergillus section Fumigati: antifungal susceptibility patterns and sequence-based identification. Antimicrob Agents Chemother 52:1244–1251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Atlas RM (2010) Handbook of microbiological media, 4th edn. CRC Press, Washington

    Book  Google Scholar 

  • Balajee SA, Gribskov JL, Hanley E, Nickle D, Marr KA (2005) Aspergillus lentulus sp. nov., a new sibling species of A. fumigatus. Eukaryot Cell 4:625–632

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Balajee SA, Nickle D, Varga J, Marr KA (2006) Molecular studies reveal frequent misidentification of Aspergillus fumigatus by morphotyping. Eukaryot Cell 5:1705–1712

    Article  CAS  PubMed Central  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barrs VR, Halliday C, Martin P, Wilson B, Krockenberger M, Gunew M, Bennett S, Koehlmeyer E, Thompson A, Fliegner R (2012) Sinonasal and sino-orbital aspergillosis in 23 cats: aetiology, clinicopathological features and treatment outcomes. Vet J 191:58–64

    Article  CAS  PubMed  Google Scholar 

  • Barrs VR, van Doorn TM, Houbraken J, Kidd SE, Martin P, Pinheiro MD, Richardson M, Varga J, Samson RA (2013) Aspergillus felis sp. nov., an emerging agent of invasive aspergillosis in humans, cats and dogs. PLoS One 8:e64871

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brygoo Y, Caffier V, Carlier J, Fabre JV, Fernandez D, Giraud T, Mourichon X, Neema C, Notteghem JL, Pope C (1998) Reproduction and population structure in phytopathogenic fungi. In: Bridge P, Couteaudier Y, Clarkson J (eds) Molecular variability of fungal pathogens. CAB International, Wallingford, pp 133–148

    Google Scholar 

  • Coelho D, Silva S, Vale-Silva L, Gomes H, Pinto E, Sarmento A, Pinheiro MD (2011) Aspergillus viridinutans: an agent of adult chronic invasive aspergillosis. Med Mycol 49:755–759

    PubMed  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 JC, Samson RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium: a guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49:1–173

    Google Scholar 

  • Ganjegunte GK, Wick AF, Stahl PD, Vance GF (2009) Accumulation and composition of total organic carbon in reclaimed coal mine lands. Land Degrad Develop 20:156–175

    Article  Google Scholar 

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

    Google Scholar 

  • Gyotoku H, Izumikawa K, Ikeda H, Takazono T, Morinaga Y, Nakamura S, Imamura Y, Nishino T, Miyazaki T, Kakeya H, Yamamoto Y, Yanagihara K, Yasuoka A, Yaguchi T, Ohno H, Miyzaki Y, Kamei K, Kanda T, Kohno S (2012) A case of bronchial aspergillosis caused by Aspergillus udagawae and its mycological features. Med Mycol 50:631–636

    Article  CAS  PubMed  Google Scholar 

  • Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97:1316–1329

    Article  CAS  PubMed  Google Scholar 

  • Hong SB, Shin HD, Hong J, Frisvad JC, Nielsen PV, Varga J, Samson RA (2008) New taxa of Neosartorya and Aspergillus in Aspergillus section Fumigati. Antonie Leeuwenhoek 93:87–98

    Article  PubMed Central  PubMed  Google Scholar 

  • Hong SB, Kim D-H, Park I-C, Samson RA, Shin HD (2010a) Isolation and identification of Aspergillus section Fumigati strains from arable soil in Korea. Microbiology 38:1–6

    CAS  Google Scholar 

  • Hong SB, Kim DH, Park IC, Choi YJ, Shin HD, Samson R (2010b) Re-identification of Aspergillus fumigatus sensu lato based on a new concept of species delimitation. J Microbiol 48:607–615

    Article  PubMed  Google Scholar 

  • Horie Y, Miyaji M, Nishimura K, Franco MF, Coelho KLR (1995) New and interesting species of Neosartorya from Brazilian soil. Mycoscience 36:199–204

    Article  Google Scholar 

  • Horie Y, Abliz P, Fukushima K, Okada K, Takaki GMC (2003) Two new species of Neosartorya from Amazonian soil, Brazil. Mycoscience 44:397–402

    Article  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

    Article  CAS  PubMed Central  PubMed  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 aetiological agents revealed among 178 clinical Aspergillus strains obtained from Czech patients and characterised by molecular sequencing. Med Mycol 50:601–610

    Article  CAS  PubMed  Google Scholar 

  • Hubka V, Kolařík M, Kubátová A, Peterson SW (2013a) Taxonomical revision of the genus Eurotium and transfer of species to Aspergillus. Mycologia 105:912–937

    Article  PubMed  Google Scholar 

  • Hubka V, Peterson SW, Frisvad JC, Yaguchi T, Kubátová A, Kolařík M (2013b) Aspergillus waksmanii sp. nov. and Aspergillus marvanovae sp. nov., two closely related species in section Fumigati. Int J Syst Evol Microbiol 63:783–789

    Article  CAS  PubMed  Google Scholar 

  • Kano R, Itamoto K, Okuda M, Inokuma H, Hasegawa A, Balajee SA (2008) Isolation of Aspergillus udagawae from a fatal case of feline orbital aspergillosis. Mycoses 51:360–361

    Article  CAS  PubMed  Google Scholar 

  • Kano R, Shibahashi A, Fujino Y, Sakai H, Mori T, Tsujimoto H, Yanai T, Hasegawa A (2013) Two cases of feline orbital aspergillosis due to Aspergillus udagawae and A. viridinutans. J Vet Med Sci 75:7–10

    Article  PubMed  Google Scholar 

  • Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Katz ME, Dougall AM, Weeks K, Cheetham BF (2005) Multiple genetically distinct groups revealed among clinical isolates identified as atypical Aspergillus fumigatus. J Clin Microbiol 43:551–555

    Article  CAS  PubMed Central  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 (2002) Biogeography of Aspergillus species in soil and litter. Mycologia 94:21–27

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Kwon-Chung KJ, Kim SJ (1974) A second heterothallic Aspergillus. Mycologia 56:628–638

    Article  Google Scholar 

  • Larsen TO, Smedsgaard J, Nielsen KF, Hansen MAE, Samson RA, Frisvad JC (2007) Production of mycotoxins by Aspergillus lentulus and other medically important and closely related species in section Fumigati. Med Mycol 45:225–232

    Article  CAS  PubMed  Google Scholar 

  • Marvanová L (1999) Biodiversity of soil micromycetes of meadows in surroundings of localities Lanžhot-soutok and Lednice-Nejdek. In: Vizárová G (ed) Ďugová O. Proceedings from the workshop Life in Soil II, Bratislava, pp 102–104

    Google Scholar 

  • McLennan EI, Tucker SC, Thrower LB (1954) New soil fungi from Australian heathland: Aspergillus, Penicillium, Spegazzinia. Aust J Bot 2:355–364

    Google Scholar 

  • McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, van Prud’homme Reine WF, Smith GF, Wiersema JH, Turland NJ (2012) International code of nomenclature for algae, fungi, and plants (Melbourne Code): adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Koeltz Scientific Books, Koenigstein

    Google Scholar 

  • Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, Heitman J (2003) Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and α isolates. Infect Immun 71:4831–4841

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  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

    Article  PubMed  Google Scholar 

  • Paden JW (1968) A new variety of Aspergillus fischeri. Mycopathol Mycol Appl 36:161–164

    Article  CAS  PubMed  Google Scholar 

  • Peláez T, Álvarez-Pérez S, Mellado E, Serrano D, Valerio M, Blanco JL, Garcia ME, Muñoz P, Cuenca-Estrella M, Bouza E (2013) Invasive aspergillosis caused by cryptic Aspergillus species: a report of two consecutive episodes in a patient with leukaemia. J Med Microbiol 62:474–478

    Article  PubMed  Google Scholar 

  • Peterson SW (1992) Neosartorya pseudofischeri sp. nov. and its relationship to other species in Aspergillus section Fumigati. Mycol Res 96:547–554

    Article  Google Scholar 

  • Pitt JI, Samson RA (2000) Types of Aspergillus and Penicillium and their teleomorphs in current use. In: Samson RA, Pitt JI (eds) Integration of modern taxonomic methods for Penicillium and Aspergillus. Harwood Academic Publishers, Amsterdam, pp 51–72

    Google Scholar 

  • Posteraro B, Mattei R, Trivella F, Maffei A, Torre A, Carolis E, Posteraro P, Fadda G, Sanguinetti M (2011) Uncommon Neosartorya udagawae fungus as a causative agent of severe corneal infection. J Clin Microbiol 49:2357–2360

    Article  PubMed Central  PubMed  Google Scholar 

  • Rai JN, Agarwal SC, Tewari JP (1971) Fungal microflora of usar soils of India. J Ind Bot Soc 50:63–74

    Google Scholar 

  • Rana S, Stahl PD, Ingram LJ, Wick AF (2007) Soil microbial community composition in reclaimed soil under different vegetation in Wyoming minelands. American Society of Mining and Reclamation Meeting, Gillette

    Google Scholar 

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

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Samson RA (1989) Filamentous fungi in food and feed. In: Moss MO, Jarvis B, Skinner FA (eds) Society for applied bacteriology symposium series no. 18. Filamentous fungi in foods and feeds. Blackwell Scientific Publications, Oxford, pp 27S–35S

    Google Scholar 

  • Samson RA, Gams W (1985) Typification of the species of Aspergillus and associated teleomorphs. In: Samson RA, Pitt JI (eds) Advances in Penicillium and Aspergillus systematics. Plenum Press, New York, pp 31–54

    Google Scholar 

  • Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (1996) Introduction to foodborne fungi. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • Samson RA, Hong S, Peterson SW, Frisvad JC, Varga J (2007a) Polyphasic taxonomy of Aspergillus section Fumigati and its teleomorph Neosartorya. Stud Mycol 59:147–203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samson RA, Noonim P, Meijer M, Houbraken J, Frisvad JC, Varga J (2007b) Diagnostic tools to identify black aspergilli. Stud Mycol 59:129–145

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samson RA, Varga J, Meijer M, Frisvad JC (2011) New taxa in Aspergillus section Usti. Stud Mycol 69:81–97

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shigeyasu C, Yamada M, Nakamura N, Mizuno Y, Sato T, Yaguchi T (2012) Keratomycosis caused by Aspergillus viridinutans: an Aspergillus fumigatus-resembling mold presenting distinct clinical and antifungal susceptibility patterns. Med Mycol 50:525–528

    Article  PubMed  Google Scholar 

  • Smith G (1952) Aspergillus brevipes n. sp. Trans Brit Mycol Soc 35:241–242

    Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Sugui JA, Vinh DC, Nardone G, Shea YR, Chang YC, Zelazny AM, Marr KA, Holland SM, Kwon-Chung KJ (2010) Neosartorya udagawae (Aspergillus udagawae), an emerging agent of aspergillosis: how different is it from Aspergillus fumigatus? J Clin Microbiol 48:220–228

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swilaiman SS, O’Gorman CM, Balajee SA, Dyer PS (2013) Discovery of a sexual cycle in Aspergillus lentulus, a close relative of A. fumigatus. Eukaryot Cell 12:962–969

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takada M, Udagawa SI (1985) A new species of heterothallic Neosartorya. Mycotaxon 24:395–402

    Google Scholar 

  • Takada M, Horie Y, Abliz P (2001) Two new heterothallic Neosartorya from African soil. Mycoscience 42:361–367

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Tomoda H, Kim YK, Nishida H, Masuma R, Omura S (1994) Pyripyropenes, novel inhibitors of acyl-CoA: cholesterol acyltransferase produced by Aspergillus fumigatus. I. Production, isolation, and biological properties. J Antibiot 47:148–153

    Article  CAS  PubMed  Google Scholar 

  • Tournas V (1994) Heat-resistant fungi of importance to the food and beverage industry. Crit Rev Microbiol 20:243–263

    Article  CAS  PubMed  Google Scholar 

  • Varga J, Tóth B, Rigó K, Debets F, Kozakiewicz Z (2000) Genetic variability within the Aspergillus viridinutans species. Folia Microbiol 45:423–428

    Article  CAS  Google Scholar 

  • Vinh DC, Shea YR, Jones PA, Freeman AF, Zelazny A, Holland SM (2009a) Chronic invasive aspergillosis caused by Aspergillus viridinutans. Emerg Infect Dis 15:1292–1294

    Article  PubMed  Google Scholar 

  • Vinh DC, Shea YR, Sugui JA, Parrilla-Castellar ER, Freeman AF, William Campbell J, Pittaluga S, Jones PA, Zelazny A, Kleiner D, Kwon-Chung KJ, Holland SM (2009b) Invasive aspergillosis due to Neosartorya udagawae. Clin Infect Dis 49:102–111

    Article  PubMed  Google Scholar 

  • Wick AF, Stahl PD, Rana S, Ingram LJ (2007) Recovery of reclaimed soil structure and function in relation to plant community composition. In: Barnhisel RO (ed) 2007 National Meeting of the American Society of Mining and Reclamation, Gillette, WY, 30 Years of SMCRA and Beyond June 2–7, 2007, Lexington, pp 941–957

  • Wong SM, Musza LL, Kydd GC, Kullnig R, Gillum AM, Cooper R (1993) Fiscalins: new sibstamce P inhibitors produced by the fungus Neosartorya fischeri. Taxonomy, fermentation, structures, and biological properties. J Antibiot 46:545–553

    Article  CAS  PubMed  Google Scholar 

  • Yaguchi T, Horie Y, Tanaka R, Matsuzawa T, Ito J, Nishimura K (2007) Molecular phylogenetics of multiple genes on Aspergillus section Fumigati isolated from clinical specimens in Japan. Jap J Med Mycol 48:37–46

    Article  CAS  Google Scholar 

  • Yaguchi T, Imanishi Y, Matsuzawa T, Hosoya K, Hitomi J, Nakayama M (2012) Method for identifying heat-resistant fungi of the genus Neosartorya. J Food Protect 75:1806–1813

    Article  Google Scholar 

  • Yun S-H, Arie T, Kaneko I, Yoder OC, Turgeon BG (2000) Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 31:7–20

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Karel Tajovský, Václav Pižl and Jan Frouz (ISB BC AS CR, v.v.i.) for sampling in the Belle Ayr Mine research sites and Janos Varga for providing the ex-type isolate of A. felis. This study was supported by the project ME 08085 KONTAKT Soil organisms in spoils after brown coal mining in the U.S.A. and Europe: a bioindication potential and a role in pedogenesis. This research was also partially supported by the Ministry of Education, Youth and Sports (CZ.1.07/2.3.00/20.0055 and CZ.1.07/2.3.00/30.0003). Molecular genetics analyses were supported by the project GAUK 607812.

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  1. Biology Centre AS CR, v.v.i., Institute of Soil Biology, Na Sádkách 7, 370 05, České Budějovice, Czech Republic

    Alena Nováková

  2. Laboratory of Physiology and Genetics of Fungi, Institute of Microbiology AS CR, v.v.i, Vídeňská 1083, 142 20, Prague 4, Czech Republic

    Vit Hubka, Zuzana Dudová & Miroslav Kolařík

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

    Vit Hubka, Zuzana Dudová, Alena Kubátová & Miroslav Kolařík

  4. Medical Mycology Research Center, Chiba University, 1-8-1, Inohana, Chuo-ku, Chiba, 260-8673, Japan

    Tetsuhiro Matsuzawa & Takashi Yaguchi

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  1. Alena Nováková
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  2. Vit Hubka
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Nováková, A., Hubka, V., Dudová, Z. et al. New species in Aspergillus section Fumigati from reclamation sites in Wyoming (U.S.A.) and revision of A. viridinutans complex. Fungal Diversity 64, 253–274 (2014). https://doi.org/10.1007/s13225-013-0262-5

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