Skip to main content
Log in

Isolation and Identification of Aspergillus Section Nigri, and Genotype Associated with Ochratoxin A and Fumonisin B2 Production in Garlic Marketed in Brazil

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The garlic contains sulfur bioactive compounds responsible for medicinal properties. The decrease of these compounds due to inadequate storage conditions reduces the beneficial properties and favors infection by microorganisms. Several studies have shown high frequency of garlic infected with Aspergillus section Nigri that potentially produce mycotoxin. Garlic samples were collected in markets of Brazil and a total of 32 samples (of 36) had the fungal infection with predominant genus Aspergillus (50.3%), Penicillium (34.7%), and Fusarium (11%). A total of 63% (649/1031) of infection with Aspergillus section Nigri, of which 60 isolates were selected for analysis of genetic variability that resulted in 4 clusters. Representatives of clusters were identified by the calmodulin gene. Isolates from cluster I were subdivided into A-I and identified as A. niger (16 isolates) and the isolates of clusters B-I, II, and III were identified as A. welwitschiae (43 isolates). Besides, an isolate of the IV-cluster was identified by A. luchuensis. Further, we used the multiplex PCR to verify genotypes of 59 isolates, and none of these had OTA production-associated genotype. Moreover, 19 A. welwitschiae and 15 A. niger were FB2 production-associated genotype. Our study is the first report to the incidence of garlic infection in Brazil and to show that A. welwitschiae causes most of these infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Fao (2016) Production and trade statistics

  2. Randle WM, Lancaster JE (2002) Sulphur compounds in alliums in relation to flavour quality. In: Rabinowitch HD, Currah L (ed) Allium crop science: recent advances. CAB Int., Wallingford, p 329–356.

    Chapter  Google Scholar 

  3. Lanzotti V, Scala F, Bonanomi G (2014) Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochem Rev 13:769–791

    Article  CAS  Google Scholar 

  4. Banerjee SK, Mukherjee PK, Maulik SK (2003) Garlic as an antioxidant: the good, the bad and the ugly. Phytother Res 17:97–106

    Article  CAS  Google Scholar 

  5. Amagase H (2006) Clarifying the real bioactive constituents of garlic. J Nutr 136:7165–7255

    Article  Google Scholar 

  6. Alorainy MS (2011) Evaluation of antimicrobial activity of garlic (Allium sativum) against E. coli O 157: H 7. J Agric Vet Sci 4:149–457

    Google Scholar 

  7. Chen S, Shen X, Cheng S, Li P, Du J, Chang Y, Meng H (2013) Evaluation of garlic cultivars for polyphenolic content and antioxidant properties. PLoS ONE 8:e79730

    Article  Google Scholar 

  8. Kumar R, Chhatwal S, Arora S, Sharma S, Singh J, Singh N, Khurana A (2013) Antihyperglycemic, antihyperlipidemic, anti-inflammatory and adenosine deaminase-lowering effects of garlic in patients with type 2 diabetes mellitus with obesity. Diabetes Metab Syndr Obes 6:49–56

    Article  CAS  Google Scholar 

  9. Borlinghaus J, Albrecht F, Gruhlke MCH, Nwachukwu ID, Slusarenko AJ (2014) Allicin: chemistry and biological properties. Molecules 19:12591–12618

    Article  Google Scholar 

  10. Capasso A (2014) Antioxidant action and therapeutic efficacy of Allium sativum L. Molecules 18:690–700

    Article  Google Scholar 

  11. Rahman MS (2007) Allicin and other functional active components in garlic: health benefits and bioavailability. Int J Food Prop 10:245–268

    Article  CAS  Google Scholar 

  12. Shadkchan Y, Shemesh E, Mirelman D, Miron T, Rabinkov A, Wilchek M, Osherov N (2004) Efficacy of allicin, the reactive molecule of garlic, in inhibiting Aspergillus spp. in vitro, and in a murine model of disseminated aspergillosis. J Antimicrob Chemother 53:832–836

    Article  CAS  Google Scholar 

  13. Irkin R, Korukluoglu M (2007) Control of Aspergillus niger with garlic, onion and leek extracts. Afr J Biotechnol 6:384–387

    Google Scholar 

  14. Irkin R, Korukluoglu M (2009) Control of some filamentous fungi and yeasts by dehydrated Allium extracts. J Verbrauch Lebensm 4:3–6

    Article  Google Scholar 

  15. Guevara-Figuero T, López-Hernández L, Lopez MG, Dufoo HMD, Vázquez-Barrios ME, Guevara-Olvera L, Mercado-Silva EM (2015) Conditioning garlic ‘‘seed” cloves at low temperature modifies plant growth, sugar, fructan content, and sucrose fructosyltransferase (1-SST) expression. Sci Hortic 189:150–158

    Article  Google Scholar 

  16. Fei MLI, Tong LI, Wei LI, De Yang L (2015) Changes in antioxidant capacity, levels of soluble sugar, total polyphenol, organosulfur compound and constituents in garlic clove during storage. Ind Crops Prod 69:137–142

    Article  CAS  Google Scholar 

  17. MacDonald S, Castle LA (1996) UK retail survey of aflatoxin in herbs and spices and their fate during cooking. Food Addt Contam 13:121–128

    Article  CAS  Google Scholar 

  18. Patel S, Hazel CM, Winterton AGM, Mortby E (1996) Survey of ethnic foods for mycotoxins. Food Addt Contam 13:833–841

    Article  CAS  Google Scholar 

  19. Gnonlonfin GJB, Adjovi YC, Tokpo AF, Agbekponou ED, Ameyapoh Y, De Souza C, Brimer L, Sanni A (2013) Mycobiota and identification of aflatoxin gene cluster in marketed spices in West Africa. Food Control 34:115–120

    Article  CAS  Google Scholar 

  20. Toma FM, Abdulla NQF (2013) Isolation and identification of fungi from spices and medicinal plants. Res J Environm Ear Sci 5:131–138

    Google Scholar 

  21. Tancinová D, Mokrý M, Barboráková Z, Masková Z (2014) Mycobiota of spices and aromatic herbs. Potravinarstvo Sci J Food Ind 8:172–177

    Google Scholar 

  22. Ghangaonkar NM (2013) Incidence of mycoflora on garlic (Allium sativum L.) bulbs. Int Res J Biol Sci 2:44–64

    Google Scholar 

  23. Fontenele LM dos S, Azevedo MLX, Cardoso-Filho FC, Muratori MCS, Sá LRS, Pereira MMG (2015) Qualidade microbiológica do alho (Allium sativum) produzido e comercializado em mercados públicos. Rev Inst Adolfo Lutz 74

  24. Oh JY, Mannaa M, Han GD, Chun SC, Kim KD (2016) First report of Aspergillus awamori as a fungal pathogen of garlic (Allium sativum L.). Crop Prot 85:65–70

    Article  Google Scholar 

  25. Abarca ML, Bragulat MR, Castellá G, Cabañes FJ (1994) Ochratoxin A production by strains of Aspergillus niger var. niger. Appl Environ Microbiol 60:2650–2652

    Article  CAS  Google Scholar 

  26. Frisvad JC, Smedsgaard J, Samson RA, Larsen TO, Thrane U (2007) Fumonisin B2 production by Aspergillus niger. J Agric Food Chem 55:9727–9732

    Article  CAS  Google Scholar 

  27. Varga J, Baranyi N, Chandrasekaran M, Vágvolgyi C (2015) Mycotoxin producers in the Aspergillus genus: an update. Acta Biol Szeged 59:151–167

    Google Scholar 

  28. Perrone G, Stea G, Epifani F, Varga J, Frisvad JC, Samson RA (2011) Aspergillus niger contains the cryptic phylogenetic species Aspergillus awamori. Fungal Biol 115:1138–1150

    Article  CAS  Google Scholar 

  29. Orlandelli RC, Specian V, Felber AC, Pamphile JA (2012) Enzimas de interesse industrial: produção por fungos e aplicações. SaBios 7:97–109

    Google Scholar 

  30. Hong SB, Lee M, Kim DH, Varga J, Frisvad JC, Perrone G, Gomi K, Yamada O, Machida M, Houbraken J, Samson RA (2013) Aspergillus luchuensis, an industrially important black Aspergillus in East Asia. PLoS ONE 8:e63769

    Article  CAS  Google Scholar 

  31. Samson RA, Visagie CM, Houbraken J (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173

    Article  CAS  Google Scholar 

  32. Abbas HK, Wilkinson JR, Zablotowicz RM, Accinelli C, Abel CA, Bruns HA, Weaver MA (2009) Ecology of Aspergillus flavus, regulation of aflatoxin production, and management strategies to reduce aflatoxin contamination of corn. Toxin Ver 28:142–153

    Article  CAS  Google Scholar 

  33. Massi FP, Sartori D, de Souza FL, Iamanaka BT, Taniwaki MH, Vieira MLC, Fungaro MHP (2016) Prospecting for the incidence of genes invoved in ochratoxin and fumonisin biosynthesis in Brazilian strains of Aspergillus niger and Aspergillus welwitschiae. Int J Food Microbiol 221:19–28

    Article  CAS  Google Scholar 

  34. Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, New York

    Book  Google Scholar 

  35. Azevedo ACS, Furlaneto MC, Soza-Gomez DR, Fungaro MHP (2000) Molecular characterization of Paecilomyces fumosoroseus (Deuteromycotina Hyphomycetes) isolates. Sci Agríc 57:729–732

    Article  Google Scholar 

  36. Fungaro MHP, Vieira MLC, de Azevedo JL (1996) Diversity among soil and insect isolates of Metarhizium anisopliae var. anisopliae detected by RAPD. Appl Microbiol 61:1323–1330

    Google Scholar 

  37. Hong SB, Cho HS, Shin HD, Frisvad JC, Samson RA (2006) Novel Neosartorya species isolated from soil in Korea. Int J Syst Evol Microbiol 56:477–486

    Article  CAS  Google Scholar 

  38. Hile AG, Shan Z, Block E (2004) Aversion of European starlings (Sturnus vulgaris) to garlic oil treated granules: garlic oil as na avian repellent. Garlic oil analysis by nuclear magnetic resonance spectroscopy. J Agric Food Chem 52:2192–2196

    Article  CAS  Google Scholar 

  39. Myhammad MT, Abdullahi A, Jafaru S, Lema SY (2016) A Survey of mycoflora of garlic cloves (Allium sativum L.) in Sokoto metropolis. Niger Ann Biol Sci 4:1–5

    Google Scholar 

  40. Susca A, Proctor RH, Butchko RAE, Haidukowski M, Stea G, Logrieco A, Moretti A (2014) Variation in the fumonisin biosynthetic gene cluster in fumonisin-producing and nonproducing black aspergilli. Fungal Genet Biol 73:39–52

    Article  CAS  Google Scholar 

  41. Palumbo JD, O’Keeffe TL, Gorski L (2013) Multiplex PCR analysis of fumonisin biosynthetic genes in fumonisin-nonporducing Aspergillus niger and A. awamori strains. Mycologia 105:277–284

    Article  CAS  Google Scholar 

  42. Gherbawy Y, Elhariry H, Kocsubé S, Bahobial A, El Deeb B, Altalhi A, Varga J, Vágvölgyi C (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

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by Coordenadoria de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniele Sartori.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vanzela, D.O.A., Massi, F.P., de Oliveira, A.L.M. et al. Isolation and Identification of Aspergillus Section Nigri, and Genotype Associated with Ochratoxin A and Fumonisin B2 Production in Garlic Marketed in Brazil. Curr Microbiol 77, 1150–1158 (2020). https://doi.org/10.1007/s00284-020-01915-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-01915-6

Navigation