Relationship between cyclopiazonic acid production and gene expression in Penicillium griseofulvum under dry-cured ham processing environmental conditions
- 25 Downloads
Cyclopiazonic acid (CPA)-producing Penicillium griseofulvum is usually found on the dry-cured ham surface during its ripening. The objective of this work was to evaluate the effect of temperature and water activity (aw) of dry-cured ham processing on growth, CPA production, and temporal relative expression of genes involved in CPA biosynthesis on dry-cured meat-based media. P. griseofulvum CECT 2919 grew faster than P. griseofulvum IBT 14319 in all conditions tested, although no growth occurred at 0.85 aw. Besides, the dry-cured ham-based medium favoured CPA synthesis for both strains compared to the meat-based medium. For the strain CECT 2919, the expression of the mfs-1 and pks-nrps genes were stimulated at 0.90 and 0.95 aw, respectively, while the dmaT gene expression was inhibited during the incubation time. By contrast, the strain IBT 14319 showed that the dmaT gene expression was stimulated at 0.90 aw, while the pks-nrps and mfs-1 genes were repressed throughout incubation time. In conclusion, it is necessary to reduce aw on the surface of the hams below 0.85 during ripening before to increase temperature to reduce growth of P. griseofulvum and CPA production. This information may be useful to design preventive and corrective actions to minimise risks associated with the presence of CPA in dry-cured ham.
KeywordsPenicillium griseofulvum Cyclopiazonic acid Growth CPA biosynthetic genes Dry-cured ham
The authors acknowledge the technical support provided by the Facility of Innovation and Analysis in Animal Source Foodstuffs of SAIUEx (financed by UEx, Junta de Extremadura, MICINN, FEDER, and FSE).
This work has been funded by the Spanish Ministry of Economy and Competitiveness, Government of Extremadura, and FEDER (AGL2013-45729-P, AGL2016-80209-P, GR15108). B. Peromingo is recipient of a pre-doctoral fellowship (BES-2014-069484) and Dr. A. Rodríguez was supported by a Juan de la Cierva-Incorporación senior research fellowship (IJCI-2014-20666), both from the Spanish Ministry of Economy and Competitiveness.
Compliance with ethical standards
Conflict of interest
The authors declare that there are no conflicts of interest.
- Banani H, Marcet-Houben M, Ballester AR, Abbruscato P, González-Candelas L, Gabaldón T, Spadaro D (2016) Genome sequencing and secondary metabolism of the postharvest pathogen Penicillium griseofulvum. BMC Genomics 17(19). https://doi.org/10.1186/s12864-015-2347-x
- Berni E, Cacchioli C, Diaferia C, Spotti E (2007) Microbial surface colonization in Nebrodi salame. Proceedings of the 6th International Symposium on the Mediterranean Pig. Messina, Capo d’Orlando, pp 253–257Google Scholar
- Berni E, Cacchioli C, Diaferia C (2012) Characterization of surface mycoflora in Nebrodi hams. De Pedro E.J. (ed.), Cabezas A.B. (ed.) 7th International Symposium on the Mediterranean Pig. Zaragoza. CIHEAM (pp. 437–440). (Options Méditerranéennes: Série A. Séminaires Méditerranéens; n. 101)Google Scholar
- Frisvad JC, Smedsgaard J, Larsen TO, Samson RA (2004) Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol 49:201–241Google Scholar
- Kato N, Tokuoka M, Shinohara Y, Kawatani M, Uramoto M, Seshime Y, Fujii I, Kitamoto K, Takahashi T, Takahashi S, Koyama Y, Osada H (2011) Genetic safeguard against mycotoxin cyclopiazonic acid production in Aspergillus oryzae. Chem Bio Chem 12:1376–1382. https://doi.org/10.1002/cbic.201000672 CrossRefGoogle Scholar
- Lazzaro I, Susca A, Mula G, Ritieni A, Ferracane R, Marruecos A, Battilani P (2012) Effects of temperature and water activity on FUM2 and FUM21 gene expression and fumonisin B production in Fusarium verticillioides. Eur J Plant Pathol 134:685–695. https://doi.org/10.1007/s10658-012-0045-y CrossRefGoogle Scholar
- Le Bars J (1979) Cyclopiazonic acid production by Penicillium camemberti Thom and natural occurrence of this mycotoxin in cheese. Appl Environ Microbiol 38:1052–1055Google Scholar
- Medina A, Gilbert MK, Mack BM, O’Brian GR, Rodríguez A, Bhatnagar D, Payne G, Magan N (2017) Interactions between water activity and temperature on the Aspergillus flavus transcriptome and aflatoxin B1 production. Int J Food Microbiol 256: 36–44. https://doi.org/10.1016/j.ijfoodmicro.2017.05.020
- Ostry V, Polster M (1989) Detection of cyclopiazonic acid and its producers in food. Vet Med 34:421–430Google Scholar
- Peromingo B, Rodríguez A, Bernáldez V, Delgado J, Rodríguez M (2016) Effect of temperature and water activity on growth and aflatoxin production by Aspergillus flavus and Aspergillus parasiticus on cured meat model systems. Meat Sci 122:76–83. https://doi.org/10.1016/j.meatsci.2016.07.024 CrossRefGoogle Scholar
- Pleadin J, Staver MM, Vahčić N, Kovacevi N, Milone S, Saftić L, Scortichini G (2015) Survey of aflatoxin B1 and ochratoxin A occurrence in traditional meat products coming from Croatian households and markets. Food Control 52:71–77. https://doi.org/10.1016/j.foodcont.2014.12.027 CrossRefGoogle Scholar
- Riley RT, Goeger DE, Yoo H, Showker JL (1992) Comparison of three tetramic acids and their ability to alter membrane function in cultured skeletal muscle cells and sarcoplasmic reticulum vesicles. Toxicol Appl Pharmacol 114:261–267. https://doi.org/10.1016/0041-008X(92)90076-5 CrossRefGoogle Scholar
- Rodríguez A, Rodríguez M, Luque MI, Justesen AF, Córdoba JJ (2012a) A comparative study of DNA extraction methods to be used in real-time PCR based quantification of ochratoxin A-producing molds in food products. Food Control 25:666–672. https://doi.org/10.1016/j.foodcont.2011.12.010 CrossRefGoogle Scholar
- Rodríguez A, Medina A, Córdoba JJ, Magan N (2014) The influence of salt (NaCl) on ochratoxin A biosynthetic genes, growth and ochratoxin a production by three strains of Penicillium nordicum on a dry-cured ham-based medium. Int J Food Microbiol 178:113–119. https://doi.org/10.1016/j.ijfoodmicro.2014.03.007 CrossRefGoogle Scholar