Selective Ef cacy of Culture Media Recommended for Isolation and Enumeration of Fusarium spp.
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1 207 Journal of Food Protection, Vol. 67, No. 1, 2004, Pages Copyright q, International Association for Food Protection Research Note Selective Ef cacy of Culture Media Recommended for Isolation and Enumeration of Fusarium spp. M. R. BRAGULAT, E. MARTÍNEZ, G. CASTELLÁ, AND F. J. CABAÑES* Departament de Sanitat i d Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, E Bellaterra, Barcelona, Spain MS : Received 30 May 2003/Accepted 1 August 2003 ABSTRACT Selective culture media, such as Nash and Snyder medium (NS), dichloran-chloramphenicol peptone agar (DCPA), modi ed Czapek-Dox agar (MCz), Czapek Dox iprodione dichloran agar (CZID), potato dextrose iprodione dichloran agar (PDID), or malachite green agar (MGA 2.5), have been developed for isolating and enumerating Fusarium spp. from natural samples. However, some of these culture media are not very selective because they allow the growth of many other fungal species. In this study, a comparison of the selective ef cacy of these culture media, using different strains of Fusarium spp. (F. anthophilum, F. culmorum, F. dlamini, F. graminearum, F. napiforme, F. nygamai, F. oxysporum, F. proliferatum, F. semitectum, F. solani, F. subglutinans, and F. verticillioides) and natural samples has been carried out. Among the six recommended selective culture media assayed, no statistical differences were detected in colony counts of the Fusarium spp. strains tested, although the colony diameters in MGA 2.5 were signi cantly lower than in NS, MCz, DCPA, CZID, and PDID media. With natural samples, MGA 2.5 performs as a potent selective medium for Fusarium spp., whereas the other recommended selective media allow the growth of many other different fungal species including Zygomycetes and yeasts. Ideally, a selective culture medium for the isolation and enumeration of a speci c group of fungi from natural samples should support the recovery of all viable propagules of this group of fungi and inhibit the development of other undesired fungal species and bacteria. It would be an advantage if these culture media facilitate the identi cation of desired species. On the other hand, the stability, solubility, and relative toxicity of the fungal inhibitor added to the culture medium are important factors to take into account for its usefulness and safety. Some selective culture media have been developed for isolating and enumerating Fusarium spp. from natural samples. Nash and Snyder medium (NS) (13) with pentachloronitrobenzene (PCNB) as fungal inhibitor is one of the most widely employed. Several modi cations of this media (8 10, 15) are also recommended for these purposes. However, PCNB has been reported to be carcinogenic (17), and other antifungal compounds have been assayed such as dichloran in dichloran-chloramphenicol peptone agar (DCPA) (2) or in modi ed Czapek-Dox agar (MCz) (6), iprodione in Czapek Dox iprodione dichloran agar (CZID) (1) or in potato dextrose iprodione dichloran agar (PDID) (19), and malachite green agar (MGA 2.5) (7). The aim of this work was to assess differences among the recommended culture media for isolation and enumeration of different Fusarium spp. The selective ef - cacy of these recommended selective media was also assayed with the use of natural samples. * Author for correspondence. Tel: ; Fax: ; javier.cabanes@uab.es. MATERIAL AND METHODS Strains. In total, 29 strains belonging to 12 Fusarium spp. were included in this study: F. anthophilum (Institute of Plant Genetics, Poland [KF] 391, KF 461), F. culmorum (Spanish Type Culture Collection [CECT] 2158, Culture Collection of Veterinary Faculty of Barcelona, Spain [CCFVB] 85, CCFVB 110), F. dlamini (CCFVB 88, International Mycological Institute, Egham, London [IMI] ), F. graminearum (CECT 2150, CCFVB 98, CCFVB 101), F. napiforme (IMI ), F. nygamai (IMI ), F. oxysporum (CECT 2871, CCFVB 82), F. proliferatum (CCFVB 210, CCFVB 221, CCFVB 224), F. semitectum (CCFVB 49, CCFVB 80, CCFVB 129), F. solani (CECT 2129, CCFVB 230, CCFVB 232), F. subglutinans (CCFVB 203, CCFVB 222, CCFVB 227), and F. verticillioides (South African Research Council Collection [MCR] 826, CCFVB 235, CCFVB 236). Culture media. Recommended selective culture media for Fusarium spp. used were NS (13) (15 g peptone [Biolife, Milano, Italy], 1 g KH 2 PO 4 [Panreac, Barcelona, Spain], 0.5 g MgSO 4 7H 2 O [Panreac], 20 g agar [Biolife], g PCNB [Sigma, St. Louis, Mo.], 1 liter distilled water), MCz (6) (20 g glucose [Panreac], 1 g yeast extract [Difco, Detroit, Mich.], 0.5 g KH 2 PO 4, 2 g NaNO 3 [Panreac], 0.5 g MgSO 4 7H 2 O, 0.01 g FeSO 4 [Panreac], 20 g agar, g dichloran [2,6-dichloro-4-nitroaniline; TCI, Tokyo, Japan], 1 liter distilled water), DCPA (2) (15 g peptone, 0.5 g KH 2 PO 4, 0.5 g MgSO 4 7H 2 O, 20 g agar, 2 mg dichloran, 1 liter distilled water), CZID (1) (35 g Czapek-Dox broth [Difco], g CuSO 4 5H 2 O [Panreac], 0.01 g ZnSO 4 7H 2 O [Panreac], 20 g agar, g dichloran, g iprodione [Rovral, 50% iprodione, Rhone-Poulenc Agro, Madrid, Spain], 1 liter distilled water), PDID (19) (24 g potato dextrose broth [Difco], g CuSO 4 5H 2 O, 0.01 g ZnSO 4 7H 2 O, 20 g agar, g dichloran,
2 208 BRAGULAT ET AL. TABLE 1. Mean values of colony diameters (CD, mm), a colony counts (CFU), b and conidia counts (CC) b of strains of each Fusarium spp. tested on six recommended selective media after 7 days of incubation Mean values for each culture medium c Species (no. of strains) NS MCz DCPA CZID PDID MGA 2.5 F. anthophilum (2) F. culmorum (3) F. dlamini (2) F. graminearum (3) F. napiforme (1) F. nygamai (1) F. oxysporum (2) F. proliferatum (3) F. semitectum (3) F. solani (3) F. subglutinans (3) F. verticillioides (3) 40.0/46.8/ /45.6/ /45.3/ /79.7/ /35.5/ /56.3/ /60.8/ /54.5/ /55.7/ /24.8/ /56.2/ /36.0/ /37.7/ /28.3/ /46.7/ /53.8/ /40.0/ /42.7/ /59.6/ /59.0/ /42.5/ /26.1/ /55.9/ /34.1/ /43.2/ /25.6/ /50.0/ /82.8/ /2.0/ /54.7/ /55.5/ /55.8/ /49.0/ /24.3/ /59.6/ /29.8/ /41.5/ /29.6/ /39.0/ /66.6/ /30.3/ /52.0/ /65.5/ /56.0/ /38.7/ /24.5/ /48.9/ /31.9/ /42.2/ /37.3/ /47.0/ /78.1/ /38.0/ /52.0/ /65.2/ /61.9/ /46.9/ /24.5/ /56.4/ /35.9/ /28.2/ /8.9/ /42.7/ /45.4/ /43.7/ /55.3/ /70.5/ /56.2/ /29.7/ /12.6/ /59.6/ /36.2/1.4 Mean 37.4 A/51.1/ B/44.0/ BC/44.8/ C/44.6/ C/49.7/ D/38.3/2.0 a Signi cant differences (P, 0.01). Mean values that are not followed by the same letter differ signi cantly. b No signi cant differences (CFU, P ; CC, P ). c NS, Nash and Snyder medium (13); MCz, modi ed Czapek-Dox medium (6); DCPA, dichloran chloramphenical peptone agar medium (2); CZID, Czapek Dox iprodione dichloran agar (1); PDID, potato dextrose iprodione dichloran agar (19); MGA 2.5, malachite green agar 2.5 (7) g iprodione, 1 liter distilled water), and MGA 2.5 (7) (15 g peptone, 1 g KH 2 PO 4, 0.5 g MgSO 4 7H 2 O, 20 g agar, g malachite green oxalate [Panreac], 1 liter distilled water). Comparison of recommended selective media for Fusarium spp. with pure cultures. Six recommended selective media were used: NS (13) without streptomycin, DCPA (2) without chloramphenicol, MCz (6), CZID (1), PDID (19), and MGA 2.5 (7). Potato dextrose agar was used as control medium. These culture media were inoculated with pure cultures of the strains of Fusarium spp. tested. Conidial suspensions were prepared from cultures grown on potato dextrose agar (Difco) for 7 days at 288C. After incubation, spores were harvested by adding 3 ml of sterile % Tween 80 (ICN, Aurora, Ill.) solution to the culture vessels and gently dislodging the conidia with a amed wire loop. The spore suspensions were then aseptically ltered through sterile gauze to remove mycelial debris, and the volumes were adjusted so that suspensions contained approximately 10 5 spores per ml as determined by a counting chamber. At least three plates per medium were used for each strain using a 10-ml calibrated Nicrom loop. Three inoculation points were applied to each plate. For each colony, two diameters were averaged to give the mean diameter for that colony measured at right angles to one another. Diameters were measured after 7 days at 288C. Also, three plates per medium were inoculated by the surface-spread method. Plates were incubated at 288C, and colony diameters and colony counts were made after 3, 5, and 7 days of incubation. In addition, morphological characteristics and measurement of sporulation were determined. Colonies were examined after 7 days of incubation for overall appearance and color, as well as the production of macroconidia, microconidia, and chlamydospores. Conidia counts were made by placing a 1-cm 2 plug from the center of each colony into 3 ml of distilled sterile water, stirring to dislodge the conidia, and 10 ml were applied on a glass slide. Ten elds were observed with a microscope and the average of a number of conidia per eld was determined. No distinction was made between macro- and microconidia. Comparison of recommended selective media for Fusarium spp. using natural samples. Fifty-six naturally contaminated samples examined were cereals (n 5 30), including cereal maize, wheat, and oats, and different animal feedstuffs (n 5 26). The samples were obtained from agricultural cooperatives and factories. The quantitative enumeration of fungal propagules was done on solid media by the surface-spread method. Serial dilutions in saline water (0.9%) were made and 0.1-ml aliquots were inoculated on three plates of malt extract agar (MEA), NS, MCz, DCPA, CZID, PDID, and MGA 2.5 with 100 ppm chloramphenicol (Boehringer-Mannheim, Mannheim, Germany) and 50 ppm streptomycin (Boehringer-Mannheim) and incubated at 288C for 5 to 7 days. MEA (malt extract [Biolife] 20 g, peptone 1 g, glucose 20 g, agar 20 g, distilled water 1 liter) was used as the control medium. Total counts of samples (CFU/g) were determined after 3, 5, and 7 days of incubation. On the last day of incubation, counts for Fusarium spp. (CFU/g) were recorded. Colonies were transferred to slants to ensure precise counting and then to plates for identi cation. The isolates belonging to the genus Fusarium were identi ed to species level (14). Statistical analysis. Data were statistically analyzed by a one-way analysis of variance test, and the signi cant differences observed were studied by a Newman-Keuls test. All statistical analyses were performed by SPSS software 8.0 (SPSS Inc., Chicago, Ill.). RESULTS Mean of values of colony diameters, colony counts, and conidia counts of strains of each Fusarium spp. tested on the six recommended selective media (MGA 2.5, NS, DCPA, MCz, CZID, and PDID) after 7 days of incubation are summarized in Table 1. Colony diameters in MGA 2.5 were signi cantly lower than in NS, MCz, DCPA, CZID, and PDID. No statistical differences were found either in
3 SELECTIVE MEDIA FOR FUSARIUM SPP. 209 TABLE 2. Mean values of colony counts a of Fusarium spp. and other fungal species of the natural samples (n 5 56) Mean values for each culture medium b MEA NS MCz DCPA CZID PDID MGA 2.5 Fusarium spp. c 29.1 (17.9) d Other species e A (82.1) 27.7 (18.2) A (81.8) 30.7 (16.5) A (83.4) 29.2 (18.5) A (81.5) 27.4 (16.7) A (83.3) 26.5 (16.9) A (83.1) 19.7 (98.0) 0.4 B (2.0) a CFU/g b NS, Nash and Snyder medium (13); MCz, modi ed Czapek-Dox medium (6); DCPA, dichloran chloramphenicalpeptone agar medium (2); CZID, Czapek Dox iprodione dichloran agar (1); PDID, potato dextrose iprodione dichloran agar (19); MGA 2.5, malachite green agar 2.5 (7). c No statistical differences were detected (P ). d % total count. e Species other than Fusarium spp. Mean values that are not followed by the same letter differ signi cantly (P, 0.01). the colony counts or the conidia counts in the six culture media assayed. Mean values of both Fusarium spp. and other fungal species counts from the natural samples analyzed are shown in Table 2. There were no signi cant differences in Fusarium spp. counts among the different media used, although the mean value of Fusarium spp. colony counts on MGA 2.5 was lower than on the rest of culture media assayed. However, signi cant differences were detected in the other species counts (other than Fusarium spp.). In a few cases, very few colonies belonging to Aspergillus, Acremonium, Penicillium, and Scopulariopsis grew restrictedly in some dishes containing MGA 2.5 (mean CFU/g, range 0 to CFU/g). Nevertheless, in the rest of the selective culture media assayed, many colonies of species belonging to different fungal genera (Acremonium, Alternaria, Aphanocladium, Aspergillus, Cladosporium, Penicillium, Scopulariopsis, Zygomycetes, and yeasts) developed in much higher counts than in MGA 2.5, the mean values being greater than CFU/g and similar to those obtained in the nonselective culture medium used as the control culture medium (MEA) (Figs. 1 and 2). DISCUSSION Various attempts have been made to improve selective Fusarium spp. isolation media (20). Effects of different compounds on growth, isolation, or enumeration of Fusarium spp. have been studied. The most widely used is the NS, which includes the common soil fungicide PCNB, as a selective agent that partially inhibits many fungal contaminants but allows the normal development of a few selected fungi, including Fusarium spp. Many modi cations of this medium have appeared, all containing various concentrations of PCNB and streptomycin and other supplementary antifungal agents such as benomyl (9) or oxgall in Komada s medium (10) and in Papaviza s medium (15). Mc- Mullen and Stack (11) did not obtain differences in the recovery of Fusarium spp. between Komada (10) and NS media. However, all these media contain PCNB, reported as a carcinogen (17). Some other selective agents used in Fusarium isolation media are dichloran (2 ppm) in MCz and DCPA, or a mixture of dichloran and iprodione (2 and 3 ppm, respectively) in CZID (1) and in PDID (19). However all of them allow growth in higher counts of other fungal species (3, 12, 18). This fact prompted us to investigate the effect of some dyes that are currently used in microbiology in staining procedures in selective media for bacteria or as ph indicators on various fungi in order to nd a range of dye concentrations that restrict growth of rapidly spreading fungi, while allowing satisfactory growth of other test fungi, FIGURE 1. Plates from a natural sample containing no Fusarium spp. propagules. In MEA, NS, CZID, and PDID, different fungal species (e.g., Aspergillus, Penicillium) were developed, whereas in MGA 2.5, no fungal growth was observed because there were no Fusarium spp. in the sample.
4 210 BRAGULAT ET AL. FIGURE 2. Plates from a natural sample containing Fusarium spp. propagules. In MEA, NS, CZID, and PDID, different fungal species (e.g., Acremonium, Alternaria, Fusarium, Penicillium) developed, whereas in MGA 2.5, only Fusarium spp. developed. * Colonies of Fusarium spp. or in order to select growth of a given fungal species (4, 5). The results obtained in these investigations on the effect of some dyes on the colony enumeration of various fungi in pure and mixed cultures (5) showed that malachite green at 1 ppm performed mainly as a strong inhibitor of spreading molds, allowing only adequate colony development and recoveries of both Fusarium and Aspergillus strains tested. Malachite green was used in Singh-Nene medium (16), but the concentration used by these authors was too high (15 to 20 ppm) to allow germination of Fusarium spores. We optimized the concentration of the dye malachite green to 2.5 ppm in the culture medium in such a way that this medium allowed only the growth of Fusarium spp. and could be used both as a selective isolation and colony enumeration medium for species belonging to this genus (7). With pure cultures, no statistical differences were detected in the colony counts of the different culture media used, although the strongest colony diameter reductions were detected in MGA 2.5. A higher colony diameter reduction in CZID and PDID than in DCPA has been described (18). In our study, the differences in diameter values found in these media were not statistically signi cant. Moreover, MGA 2.5 supports good growth of all the common fusaria, which produce well-formed colonies with good sporulation. An important consideration is that conidia are generally characteristic of those formed on standard identi cation media, so many isolates of Fusarium can be identi ed directly from MGA 2.5 plates. Macroscopic morphological characteristics of Fusarium spp. colonies were maintained in MGA 2.5. Although colony color was more enhanced in media with potato (PDID) and Czapek as the basal media (MCz and CZID) than in media with peptone as the basal medium (DCPA, NS, and MGA 2.5), subcultures were not necessary to identify these species in all media tested. Some of these observations are in concordance with other authors (6, 18, 19). We also assayed these selective media on natural samples, and no signi cant differences in Fusarium colony counts were found. The MGA 2.5 medium was completely selective for Fusarium spp. (Figs. 1 and 2), whereas the remaining media allowed the growth of many other fungal species, as other authors have reported (3, 12, 18). MGA 2.5 is a very useful medium for the isolation and enumeration of Fusarium spp., maintaining the morphological characteristics of this fungal genus and allowing identi cation to genus level without subculturing. This medium with added antimicrobial agents is also very useful for isolating Fusarium species from naturally contaminated samples. ACKNOWLEDGMENTS This study was supported by grants ALI C04-02 from the Comisio n Interministerial de Ciencia y Tecnolog a and SGR00079 from the DURSI, Generalitat de Catalunya, Spain. Fusarium strains from CECT, KF, and MCR were kindly provided by J. Uruburu, J. Chelkowski, and J. P. Rheeder, respectively. REFERENCES Abildgren, M. P., F. Lund, U. Thrane, and S. Elmholt CzapekDox agar containing iprodione and dicloran as a selective medium for the isolation of Fusarium species. Lett. Appl. Microbiol. 5: Andrews, S., and J. I. Pitt Selective medium for the isolation of Fusarium species and dematiaceous Hypomycetes from cereals. Appl. Environ. Microbiol. 51: Arino, A. A., and L. B. Bullerman Fungal colonization of corn grown in Nebraska in relation to year, genotype and growing conditions. J. Food Prot. 57: Bragulat, M. R., M. L. Abarca, M. T. Bruguera, and F. J. Caban es Dyes as fungal inhibitors: effect on colony diameter. Appl. Environ. Microbiol. 57: Bragulat, M. R., M. L. Abarca, G. Castella, and F. J. Caban es Dyes as fungal inhibitors: effect on colony enumeration. J. Appl. Bacteriol. 79: Bullerman, L. B., and D. I. West Comparison of several media and methods for detection and enumeration of toxigenic Fusarium species, p In R. A. Samson, A. D. Hocking, J. I. Pitt, and A. D. King (ed.), Modern methods in food mycology. Elsevier, Amsterdam. Castella, G., M. R. Bragulat, M. V. Rubiales, and F. J. Caban es Malachite green agar, a new selective medium for Fusarium spp. Mycopathologia 137: Elad, Y., and I. Chet Improved selective media for isolation of Trichoderma spp. or Fusarium spp. Phytoparasitica 11: Hall, R Benomyl increases the selectivity of the Nash-Snyder
5 medium for Fusarium solani f. sp. phaseoli. Can. J. Plant Pathol. 3: Komada, H Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Rev. Plant Prot. Res. 8: McMullen, M. P., and R. W. Stack Effects of isolation techniques and media on the differential isolation of Fusarium species. Phytopathology 73: Munimbazi, C., and L. B. Bullerman Molds and mycotoxins in foods from Burundi. J. Food Prot. 59: Nash, S. M., and W. C. Snyder Quantitative estimations by plate counts of propagules of the bean root rot Fusarium in eld soils. Phytopathology 52: Nelson, P. E., T. A. Tousson, and W. F. O. Marasas Fusarium species: an illustrated manual for identi cation. The Pennsylvania State University Press, University Park. Papavizas, G. C Evaluation of various media and antimicro- SELECTIVE MEDIA FOR FUSARIUM SPP bial agents for isolation of Fusarium from soil. Phytopathology 57: Singh, R. S., and Y. L. Nene Malachite green in synthetic medium for the isolation of Fusarium spp. from plant tissues. Naturwissenschaften 52:94. Sweet, D. V Registry of toxic effects of chemical substances. U.S. Department of Health and Human Services, Cincinnati. Thrane, U Comparison of three selective media for detecting Fusarium species in food: a collaborative study. Int. J. Food Microbiol. 29: Thrane, U., O. Filtenborg, J. C. Frisvad, and F. Lund Improved methods for detection and identi cation of toxigenic Fusarium species, p In R. A. Samson, A. D. Hocking, J. I. Pitt, and A. D. King (ed.), Modern methods in food mycology. Elsevier, Amsterdam. Tsao, P. H Selective media for isolation of pathogenic fungi. Ann. Rev. Phytopathol. 8:
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