Species identification of Aspergillus section Flavi isolates from Portuguese almonds using phenotypic, including MALDI-TOF ICMS, and molecular approaches

Journal of Applied Microbiology

Volumn 111, Issue 4, 2011, Pages 877-892

  Rodrigues, P ^a,b   Santos, C ^a   Venancio A ^a   Lima, N ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

Author keywords

Aflatoxins; Calmodulin gene; Cyclopiazonic acid; Food mycology; Fungal polyphasic identification; Mycotoxins

Indexed keywords

ASPERGILLUS; CALMODULIN; DESORPTION; GENES; MASS SPECTROMETRY; SPECTRUM ANALYSIS;

ASPERGILLUS SECTION FLAVI; CALMODULIN GENE; CYCLOPIAZONIC ACID; FOOD MYCOLOGIES; FUNGAL POLYPHASIC IDENTIFICATION; MALDI-TOF; MOLECULAR APPROACH; PARASITICUS; POLYPHASIC; SPECIES IDENTIFICATION;

MYCOTOXINS;

CALMODULIN; MYCOTOXIN; PROTEIN;

DECIDUOUS TREE; DESORPTION; FUNGUS; GENOTYPE; IDENTIFICATION KEY; INDUCTIVELY COUPLED PLASMA METHOD; IONIZATION; MICROMORPHOLOGY; MOLECULAR ANALYSIS; MULTIVARIATE ANALYSIS; PHENOTYPE; PROTEIN; SPECTRAL ANALYSIS; TAXONOMY; TOXIN;

ALMOND; ARTICLE; ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS PARASITICUS; ASPERGILLUS TAMARII; CLADISTICS; FINGER DERMATOGLYPHICS; FUNGUS ISOLATION; GENE SEQUENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROMORPHOLOGY; MOLECULAR GENETICS; NONHUMAN; PHYLOGENETIC TREE; SPECIES IDENTIFICATION;

ASPERGILLUS; ASPERGILLUS FLAVUS; ASPERGILLUS PARASITICUS; ASPERGILLUS TAMARII;

EID: 80052792324     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05116.x     Document Type: Article

References (62)

1. Abarca, M.L., Bragulat, M.R., Bruguera, M.T. and Cabañes, F.J. (1988) Comparison of some screening methods for aflatoxigenic moulds. Mycopathologia 104, 75-79.
2. Akaike, H. (1973) Information theory and an extension of the maximum likelihood principle. In Second International Symposium on Information Theory ed. Petrov, B.N. and Csaki, F., pp. 267-281. Budapest, Hungary: Akademiai Kiado.
3. Batista, P.P., Santos, J.F., Oliveira, N.T., Pires, A.P.D., Motta, C.M.S. and Lima, E.A.L.A. (2008) Genetic characterization of Brazilian strains of Aspergillus flavus using DNA markers. Genet Mol Res 7, 706-717.
4. Blaney, B.J., Kelly, M.A., Tyler, A.L. and Connole, M.D. (1989) Aflatoxin and cyclopiazonic acid production by Queensland isolates of Aspergillus flavus and Aspergillus parasiticus. Aust J Agr Res 40, 395-400.
5. Cotty, P.J. and Cardwell, K.F. (1999) Divergence of West African and North American communities of Aspergillus section Flavi. Appl Environ Microbiol 65, 2264-2266.
6. Criseo, G., Racco, C. and Romeo, O. (2008) High genetic variability in non-aflatoxigenic A. flavus strains by using Quadruplex PCR-based assay. Int J Food Microbiol 125, 341-343.
7. Davies, N.D., Iyer, S.K. and Diener, U.L. (1987) Improved method of screening for aflatoxin with a coconut agar medium. Appl Environ Microbiol 53, 1593-1595.
8. Doster, M.A., Michailides, T.J. and Morgan, D.P. (1996) Aspergillus species and mycotoxins in figs from California orchards. Plant Dis 80, 484-489.
9. Frisvad, J.C. (1989) The use of high-performance liquid chromatography and diode array detection in fungal chemotaxonomy based on profiles of secondary metabolites. Bot J Linn Soc 99, 81-95.
10. Frisvad, J.C., Skouboe, P. and Samson, R.A. (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.
11. Garber, R.K. and Cotty, P.J. (1997) Formation of sclerotia and aflatoxins in developing cotton bells infected by the S strain of Aspergillus flavus and potential for biocontrol with an atoxigenic strain. Phytopathology 87, 940-945.
12. Geiser, D.M., Dorner, J.W., Horn, B.W. and Taylor, J.W. (2000) The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae. Fungal Genet Biol 31, 169-179.
13. Geiser, D.M., Klich, M.A., Frisvad, J.C., Peterson, S.W., Varga, J. and Samson, R.A. (2007) The current status of species recognition and identification in Aspergillus. Stud Mycol 59, 1-10.
14. Gerrits van den Ende, A.H.G. and de Hoog, G.S. (1999) Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Stud Mycol 43, 151-162.
15. Giorni, P., Magan, N., Pietri, A., Bertuzzi, T. and Battilani, P. (2007) Studies on Aspergillus section Flavi isolated from maize in northern Italy. Int J Food Microbiol 113, 330-338.
16. Goto, T., Wicklow, D.T. and Ito, Y. (1996) Aflatoxin and cyclopiazonic acid production by a Sclerotium-producing Aspergillus tamarii strain. Appl Environ Microbiol 62, 4036-4038.
17. Hong, S.-B., Go, S.-J., Shin, H.-D., Frisvad, J.C. and Samson, R.A. (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97, 1316-1329.
18. Horn, B. (1997) Aspergillus caelatus, a new species in section Flavi. Mycotaxon 56, 185-191.
19. Horn, B.W., Greene, R.L., Sobolev, V.S., Dorner, J.W. and Powell, J.H. (1996) Association of morphology and mycotoxin production with vegetative compatibility groups in Aspergillus flavus, A. parasiticus, and A. tamarii. Mycologia 88, 574-587.
20. Huelsenbeck, J.P. and Ronquist, F. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
21. Ito, Y., Peterson, S.W., Wicklow, D.T. and Goto, T. (2001) Aspergillus pseudotamarii, a new aflatoxin producing species in Aspergillus section Flavi. Mycol Res 105, 233-239.
22. Johnsson, P., Lindblad, M., Thim, A.M., Jonsson, N., Vargas, E.A., Medeiros, N.L., Brabet, C., Quaresma de Araújo, M. and Olsen, M. (2008) Growth of aflatoxigenic moulds and aflatoxin formation in Brazil nuts. World Mycotoxin J 1, 127-137.
23. Kallow, W., Santos, I.M., Erhard, M., Serra, R., Venâncio, A. and Lima, N. (2006) Aspergillus ibericus: a new species of section Nigri characterised by MALDI-TOF MS. In Proceedings of 8th International Mycological Congress ed. Meyer, W. and Pearce, C. pp. 189-193. Bologna: Medimond S.r.l.
24. Kemptner, J., Marchetti-Deschmann, M., Mach, R., Druzhinina, I.S., Kubicek, C.P. and Allmaier, G. (2009) Evaluation of matrix-assisted laser desorption/ionization (MALDI) preparation techniques for surface characterization of intact Fusarium spores by MALDI linear time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 23, 877-884.
25. Klich, M.A. (2002) Identification of Common Aspergillus Species. The Netherlands: CBS.
26. Klich, M.A. and Pitt, J.L. (1988) Differentiation of Aspergilus flavus and A. parasiticus and other closely related species. Trans Br Mycol Soc 91, 99-108.
27. Kozakiewicz, Z. (1989) Aspergillus Species on Stored Products. Wallingford: CAB International.
28. Larsen, T.O., Smedsgaard, J., Nielsen, K.F., Hansen, M.E. and Frisvad, J.C. (2005) Phenotypic taxonomy and metabolite profiling in microbial drug discovery. Nat Prod Rep 22, 672-693.
29. Lee, C.-Z., Liou, G.-Y. and Yuan, G.-F. (2004) Comparison of Aspergillus flavus and Aspergillus oryzae by amplified fragment length polymorphism. Bot Bull Acad Sin 45, 61-68.
30. Li, D.M., Horie, Y., Wang, Y. and Li, R. (1998) Three new Aspergillus species isolated from clinical sources as a causal agent of human aspergillosis. Mycoscience 39, 299-305.
31. Li, T.-Y., Liu, B.-H. and Chen, Y.-C. (2000) Characterization of Aspergillus spores by matrix assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 14, 2393-2400.
32. Maroco, J. (2003) Análise Estatística com utilização do SPSS, 2nd edn. Lisbon, Portugal: Edições Sílabo, Lda.
33. Marvin, L.F., Roberts, M.A. and Fay, L.B. (2003) Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in clinical chemistry. Clin Chim Acta 337, 11-21.
34. McAlpin, C.E., Wiclow, D.T. and Platis, C.E. (1998) Genotypic diversity of Aspergillus parasiticus in an Illinois corn field. Plant Dis 82, 1132-1136.
35. O'Donnell, K., Nirenberg, H.I., Aoki, T. and Cigelnik, E. (2000) A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience 41, 61-78.
36. Olsen, M., Johnsson, P., Möller, T., Paladino, R. and Lindblad, M. (2008) Aspergillus nomius, an important aflatoxin producer in Brazil nuts? World Mycotoxin J 1, 123-126.
37. Peterson, S.W. (2000) Phylogenetic relationships in Aspergillus based on rDNA sequence analysis. In Integration of Modern Taxonomic Methods for Penicillium and Aspergillus Classification ed. Samson, R.A. and Pitt, J.I. pp. 323-355. Amsterdam: Harwood Academic Publishers.
38. Peterson, S.W. (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100, 205-226.
39. Peterson, S.W., Ito, Y., Horn, B.W. and Goto, T. (2001) Aspergillus bombycis, a new aflatoxigenic species and genetic variation in its sibling species, A. nomius. Mycologia 93, 689-703.
40. Pildain, M.B., Frisvad, J.C., Vaamonde, G., Cabral, D., Varga, J. and Samson, R.A. (2008) Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Int J Syst Evol Microbiol 58, 725-735.
41. Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 25, 1253-1256.
42. Raper, K.B. and Fennell, D.I. (1965) The Genus Aspergillus. Baltimore, MD: Williams & Wilkins.
43. Rigó, K., Varga, J., Toth, B., Teren, J., Mesterhazy, A. and Kozakiewicz, Z. (2002) Evolutionary relationships within Aspergilus section Flavi based on sequences of the intergenic transcribed spacer regions and the 5.8S rRNA gene. J Gen Appl Microbiol 48, 9-16.
44. Rodrigues, P., Venâncio, A., Kozakiewicz, Z. and Lima, N. (2009) A polyphasic approach to the identification of aflatoxigenic and non-aflatoxigenic strains of Aspergillus Section Flavi isolated from Portuguese almonds. Int J Food Microbiol 129, 187-193.
45. Rokas, A., Payne, G., Fedorova, N.D., Baker, S.E., Machida, M., Yu, J., Georgianna, D.R., Dean, R.A. et al. (2007) What can comparative genomics tell us about species concepts in the genus Aspergillus? Stud Mycol 59, 11-17.
46. Saito, M. and Tsuruta, O. (1993) A new variety of Aspergillus flavus from tropical soil in Thailand and its aflatoxin productivity. Proc Jpn Assoc Mycotoxicol 37, 31-36.
47. Samson, R.A. (1979) A compilation of the Aspergilli described since 1965. Stud Mycol 18. The Netherlands: CBS.
48. Samson, R.A. and Varga, J. (2009) What is a species in Aspergillus? Med Mycol 47(Suppl. 1), S13-S20.
49. Samson, R.A., Hoekstra, E.S. and Frisvad, J.C. (eds) (2004) Introduction to Food- and Airborne Fungi, 7th edn. Wageningen: CBS.
50. Samson, R.A., Noonim, P., Meijer, M., Houbraken, J., Frisvad, J.C. and Varga, J. (2007) Diagnostic tools to identify black aspergilli. Stud Mycol 59, 129-145.
51. Santos, C., Paterson, R.R.M., Venâncio, A. and Lima, N. (2010) Filamentous fungal characterizations by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Appl Microbiol 108, 375-385.
52. Serra, R., Cabañes, F.J., Perrone, G., Castellá, G., Venâncio, A., Mulè, G. and Kozakiewicz, Z. (2006) Aspergillus ibericus: a new species of section Nigri isolated from grapes. Mycologia 98, 295-306.
53. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
54. Tanaka, K., Waki, H., Ido, Y., Akita, S. and Yoshida, Y. (1988) Protein and polymer analyses up to m/z 100000 by laser ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 2, 151-153.
55. Tavaré, L. (1986) Some probabilistic and statistical problems on the analysis of DNA sequences. Lec Math Life Sci 17, 57-86.
56. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties, and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
57. Tran-Dinh, N., Pitt, J.I. and Carter, D.A. (1999) Molecular genotype analysis of natural toxigenic and nontoxigenic isolates of Aspergillus flavus and A. parasiticus. Mycol Res 103, 1485-1490.
58. Vaamonde, G., Patriarca, A., Pinto, V.F., Comeria, R. and Degrossi, C. (2003) Variability of aflatoxin and cyclopiazonic acid production by Aspergillus section Flavi from different substrates in Argentina. Int J Food Microbiol 88, 79-84.
59. Varga, J., Due, M., Frisvad, J.C. and Samson, R.A. (2007a) Taxonomic revision of Aspergillus section Clavati based on molecular, morphological and physiological data. Stud Mycol 59, 89-106.
60. Varga, J., Frisvad, J.C. and Samson, R.A. (2007b) Polyphasic taxonomy of Aspergillus section Candidi based on molecular, morphological and physiological data. Stud Mycol 59, 75-88.
61. Wicklow, D.T., McAlpin, C.E. and Platis, C.E. (1998) Characterization of the Aspergillus flavus population within an Illinois maize field. Mycol Res 102, 263-268.
62. Zalar, P., Frisvad, J.C., Gunde-Cimerman, N., Varga, J. and Samson, R.A. (2008) Four new species of Emericella from the Mediterranean region of Europe. Mycologia 100, 779-795.