Variation in fumonisin and ochratoxin production associated with differences in biosynthetic gene content in Aspergillus niger and A. welwitschiae isolates from multiple crop and geographic origins

Frontiers in Microbiology

Volumn 7, Issue SEP, 2016, Pages

  Susca, Antonia ^a   Proctor, Robert H ^b   Morelli, Massimiliano ^c   Haidukowski, Miriam ^a   Gallo, Antonia ^a   Logrieco, Antonio F ^a   Moretti, Antonio ^a  

^a INSTITUTE OF SCIENCES OF FOOD PRODUCTION   (Italy)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^c INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

Aspergillus niger; Aspergillus welwitschiae; Biosynthetic gene cluster; Fum cluster; Fumonisin; Ochratoxin; Ota cluster

Indexed keywords

FUMONISIN; MYCOTOXIN; OCHRATOXIN;

ARTICLE; ASPERGILLUS NIGER; BIOSYNTHETIC GENE; DENSITY GRADIENT CENTRIFUGATION; DNA EXTRACTION; DNA SEQUENCE; FUNGAL STRAIN; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; GENE; GENE DELETION; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION;

EID: 84992730962     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01412     Document Type: Article

References (40)

1. Abbas, H. K., Zablotowicz, R. M., Bruns, H. A., and Abel, C. A. (2006). Biocontrol of aflatoxin in corn by inoculation with non-aflatoxigenic Aspergillus flavus isolates. Biocontrol. Sci. Technol. 16, 437-449. doi: 10.1080/09583150500532477
2. Alexander, N. J., Proctor, R. H., and McCormick, S. P. (2009). Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins in Fusarium. Toxin Rev. 28, 198-215. doi: 10.1080/15569540903092142
3. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Millwer, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
4. Andersen, M. R., Salazar, M. P., Schaap, P. J., van de Vondervoort, P. J. I., Culley, D., Thykaer, J, et al. (2011). Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res. 21, 885-897. doi: 10.1101/gr.112169.110
5. Baker, S. E. (2006). Aspergillus niger genomics: past, present and into the future. Med. Mycol. 44, S17-S21. doi: 10.1080/13693780600921037
6. Battilani, P., Barbano, C., Marin, S., Sanchis, V., Kozakiewicz, Z., and Magan, N. (2006). Mapping of Aspergillus section Nigri in Southern Europe and Israel based on geostatistical analysis. Int. J. Food Microbiol. 111, S72-S82. doi: 10.1016/j.ijfoodmicro.2006.03.014
7. Brakhage, A. A. (2013). Regulation of fungal secondary metabolism. Nat. Rev. Microbiol. 11, 21-32. doi: 10.1038/nrmicro2916
8. Brown, D. W., Butchko, R. A. E., Busman, M., and Proctor, R. H. (2007). The Fusarium verticillioides FUM gene cluster encodes a Zn(II)2Cys6 protein that affects FUM gene expression and fumonisin production. Eukaryot. Cell 6, 1210-1218. doi: 10.1128/EC.00400-06
9. Dorner, J. W., and Horn, B. W. (2007). Separate and combined applications of nontoxigenic Aspergillus flavus and A. parasiticus for biocontrol of aflatoxin in peanuts. Mycopathologia 163, 215-223. doi: 10.1007/s11046-007-9004-0
10. Ferracin, L. M., Fier, C. B., Vieira, M. L. C., Monteiro-Vitorello, C. B., Varani Ade, M., Rossi, M. M., et al. (2012). Strain-specific polyketide synthase genes of Aspergillus niger. Int. J. Food Microbiol. 155, 137-145. doi: 10.1016/j.ijfoodmicro.2012.01.020
11. Frisvad, J. C., Larsen, T. O., Thrane, U., Meijer, M., Varga, J., Samson, R. A., et al. (2011). Fumonisin and ochratoxin production in industrial Aspergillus niger strains. PLoS ONE 6:e23496. doi: 10.1371/journal.pone.0023496
12. Frisvad, J. C., Smedsgaard, J., Samson, R. A., Larsen, T. O., and Thrane, U. (2007). Fumonisin B2 production by Aspergillus niger. J. Agric. Food Chem. 55, 9727-9732. doi: 10.1021/jf0718906
13. Gallo, A., Bruno, K. S., Solfrizzo, M., Perrone, G., Mulè, G., Visconti, A., et al. (2012). New insight into the ochratoxin A biosynthetic pathway through deletion of a nonribosomal peptide synthetase gene in Aspergillus carbonarius. Appl. Environ. Microbiol. 78, 8208-8218. doi: 10.1128/AEM.02508-12
14. Gallo, A., Knox, B. P., Bruno, K. S., Solfrizzo, M., Baker, S. E., and Perrone, G. (2014). Identification and characterization of the polyketide synthase involved in ochratoxin A biosynthesis in Aspergillus carbonarius. Int. J. Food Microbiol. 179, 10-17. doi: 10.1016/j.ijfoodmicro.2014.03.013
15. Gallo, A., Perrone, G., Solfrizzo, M., Epifani, F., Abbas, A., Dobson, A. D., et al. (2009). Characterisation of a pks gene which is expressed during ochratoxin A production by Aspergillus carbonarius. Int. J. Food Microbiol. 129, 8-15. doi: 10.1016/j.ijfoodmicro.2008.10.022
16. Geisen, R., Schmidt-Heydt, M., and Karolewiez, A. (2006). A gene cluster of the ochratoxin A biosynthetic genes in Penicillium. Mycotoxin Res. 22, 134-141. doi: 10.1007/BF02956777
17. Gherbawy, Y., Elhariry, H., Kocsube, S., Bahobial, A., Deeb, B. E., Altalhi, A., et al. (2015). Molecular characterization of black Aspergillus species from onion and their potential for ochratoxin A and fumonisin B2 production. Foodborne Pathog. Dis. 12, 414-423. doi: 10.1089/fpd.2014.1870
18. Gil-Serna, J, Vázquez, C, González-Jaén, M. T., and Patiño, B. (2015). Clustered array of ochratoxin A biosynthetic genes in Aspergillus steynii and their expression patterns in permissive conditions. Int. J. Food Microbiol. 214, 102-108. doi: 10.1016/j.ijfoodmicro.2015.07.020
19. Hong, S. B., Lee, M., Kim, D. H., Varga, J., Frisvad, J. C., Perrone, G., et al. (2013). Aspergillus luchuensis, an industrially important black Aspergillus in East Asia. PLoS ONE 8:e63769. doi: 10.1371/journal.pone.0063769
20. Keller, N. P., Turner, G., and Bennett, J. W. (2005). Fungal secondary metabolism-from biochemistry to genomics. Nat. Rev. Microbiol. 3, 937-947. doi: 10.1038/nrmicro1286
21. Kozakiewicz, Z. (1989). Aspergillus Species on Stored Products. Mycological Papers, Vol. 161, Wallingford, CT: CABI Publishing.
22. Massi, F. P., Sartori, D, de Souza Ferranti, L., Iamanaka, B. T., Taniwaki, M. H., Vieira, M. L., et al. (2016). Prospecting for the incidence of genes involved in ochratoxin and fumonisin biosynthesis in Brazilian strains of Aspergillus niger and Aspergillus welwitschiae. Int. J. Food Microbiol. 221, 19-28. doi: 10.1016/j.ijfoodmicro.2016.01.010
23. Medina, C., Mateo, R., López-Ocaña, L., Valle-Algarra, F. M., and Jiménez, M. (2005). Study on Spanish grape mycobiota and ochratoxin A production by isolates of Aspergillus tubingensis and other members of Aspergillus section Nigri. Appl. Environ. Microbiol. 71, 4696-4702. doi: 10.1128/AEM.71.8.4696-4702.2005
24. Mogensen, J. M., Frisvad, J. C., Thrane, U., and Nielsen, K. F. (2010). Production of Fumonisin B2 and B4 by Aspergillus niger on grapes and raisins. J. Agric. Food. Chem. 58, 954-958. doi: 10.1021/jf903116q
25. Nordberg, H., Cantor, M., Dusheyko, S., Hua, S., Poliakov, A., Shabalov, I., et al. (2014). The genome portal of the department of energy joint genome institute: 2014 updates. Nucleic Acids Res. 42, D26-D31. doi: 10.1093/nar/gkt1069
26. 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. doi: 10.1007/BF02464387
27. Palumbo, J. D., O'Keeffe, T. L., and Gorski, L. (2013). Multiplex PCR analysis of fumonisin biosynthetic genes in fumonisin-nonproducing Aspergillus niger and A. awamori strains. Mycologia 105, 277-284. doi: 10.3852/11-418
28. Pel, H. J., de Winde, J. H., Archer, D. B., Dyer, P. S., Hofmann, G., Schaap, P. J., et al. (2007). Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 25, 221-231. doi: 10.1038/nbt1282
29. Perrone, G., Stea, G., Epifani, F., Varga, J., Frisvad, J. C., and Samson, R. A. (2011). Aspergillus niger contains the cryptic phylogenetic species A. awamori. Fungal Biol. 115, 1138-1150. doi: 10.1016/j.funbio.2011.07.008
30. Proctor, R. H., Desjardins, A. E., Plattner, R. D., and Hohn, T. M. (1999). A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27, 100-112. doi: 10.1006/fgbi.1999.1141
31. Qi, T. F., Renaud, J. B., McDowell, T., Seifert, K. A., Yeung, K. K., and Sumarah, M. W. (2016). Diversity of mycotoxin-producing black aspergilli in Canadian vineyards. J. Agric. Food Chem. 64, 1583-1589. doi: 10.1021/acs.jafc.5b05584
32. Raeder, U., and Broda, P. (1985). Rapid preparation of DNA from filamentous fungi. Lett. Appl. Microbiol. 1, 17-20. doi: 10.1111/j.1472-765X.1985.tb01479.x
33. Storari, M., Dennert, F. G., Bigler, L., Gessler, C., and Broggini, G. A. L. (2012). Isolation of mycotoxins producing black aspergilli in herbal teas available on the Swiss market. Food Control 26, 157-161. doi: 10.1016/j.foodcont.2012.01.026
34. Susca, A., Moretti, A., Stea, G., Villani, A., Haidukowski, M., Logrieco, A., et al. (2014b). Comparison of species composition and fumonisin production in Aspergillus section Nigri populations in maize kernels from USA and Italy. Int. J. Food Microbiol. 188, 75-82. doi: 10.1016/j.ijfoodmicro.2014.06.031
35. Susca, A., Perrone, G., Cozzi, G., Stea, G., Logrieco, A. F., and Mulè, G. (2013). Multilocus sequence analysis of Aspergillus Sect. Nigri in dried vine fruits of worldwide origin. Int. J. Food Microbiol. 165, 163-168. doi: 10.1016/j.ijfoodmicro.2013.04.027
36. Susca, A., Proctor, R. H., Butchko, R. A, Haidukowski, M., Stea, G., Logrieco, A. F., et al. (2014a). Variation in the fumonisin biosynthetic gene cluster in fumonisin-producing and nonproducing black aspergilli. Fungal Genet. Biol. 73, 39-52. doi: 10.1016/j.fgb.2014.09.009
37. Susca, A., Proctor, R. H., Mulè, G., Stea, G., Ritieni, A., Logrieco, A., et al. (2010). Correlation of mycotoxin fumonisin B2 production and presence of the fumonisin biosynthetic gene fum8 in Aspergillus niger from Grape. J. Agric. Food Chem. 58, 9266-9272. doi: 10.1021/jf101591x
38. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
39. Varga, J., Frisvad, J. C., Kocsubé, S., Brankovics, B., Tóth, B., Szigeti, G., et al. (2011). New and revisited species in Aspergillus section Nigri. Stud. Mycol. 69, 1-17. doi: 10.3114/sim.2011.69.01
40. Varga, J., Kocsubé, S., Suri, K., Szigeti, G., Szekeres, A., Varga, M., et al. (2010). Fumonisin contamination and fumonisin producing black Aspergilli in dried vine fruits of different origin. Int. J. Food Microbiol. 143, 143-149. doi: 10.1016/j.ijfoodmicro.2010.08.008