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3) indicate that both the pcbC and the penDE genes are present in all the strains of P. griseofulvum and are absent in all the remaining strains belonging to other species. The presence of the penicillin gene cluster confirms that P. Similarly, the absence of the penicillin cluster in P. crustosum supports the conclusion that the antibacterial activity observed in these fungi is not due to penicillin. griseofulvum contained the whole pcbAB gene, as revealed by the hybridization signals appearing with the three probes C, D, and E (Fig. The Southern blot analyses performed with these five probes, along with additional Southern blots with other probes from the cluster, allowed us to elaborate on an Eco RI restriction map of the new penicillin gene cluster in P. griseofulvum by comparison with the previously described maps of P. 5, there is an Eco RI site in the penDE gene of the P. griseofulvum NRRL 991 strain which is absent in the other strains of P. In general most of the restriction sites are conserved between the three species, but it is striking that one of the Eco RI fragments inside pcbAB is about 160 bp larger in P. Presence of the genes pcbC and penDE in penicillin-producing strains and absence in nonproducing strains. Eco RI-digested genomic DNA from all the strains under study was electrophoresed ( lanes 1 to 34), transferred to a nylon membrane, and hybridized with probe A (corresponding to the pcbC gene) and probe B (corresponding to the penDE gene). griseofulvum NRRL 2300, NRRL 2152, NRRL 989, NRRL 994, NRRL 991, and NRRL 992; 11 and 12, P. roqueforti CONT1 (isolated from blue cheese) and NRRL 849; 13, Paecilomyces variotii NRRL 1775; 14 to 17, P. camemberti NRRL 874, NRRL 877, NRRL 876 (ex-type of P. commune NRRL 845 and CEC1 (isolated from cecina); 26, P. Presence of the gene pcbAB in penicillin-producing strains. Eco RI-digested genomic DNA from all the strains was electrophoresed (lanes 1 to 34); transferred to a nylon membrane; and hybridized with probes C, D, and E, which correspond to different portions of the pcbAB gene (Fig. Strain numbers are as indicated in the legend to Fig. verrucosum (lanes 21 and 22) there is a signal of 2.5 kb with probe C, which reveals the presence of the 3? end of the pcbAB gene in this species. With probes D and E, a signal of about 12.5 kb can be observed that corresponds also to the pcbAB gene (see text). Eco RI restriction map of the penicillin gene cluster in P. The five probes used in the Southern analysis are indicated as grey boxes below the maps of P. nalgiovense , together with the enzymes used to obtain the probes. Most Eco RI sites are conserved between the three species, except the site at the 5? end of the penDE gene, which is present only in P. griseofulvum NRRL 991, but in a slightly different position in each of these two strains. An Eco RI fragment inside the pcbAB gene (overlapping partially with probe D) shows a slightly larger size in P. A similar phenomenon occurs in the right part of the cluster, where the Eco RI fragment comprising the pcbC gene and most of the penDE gene is slightly larger in P. The existence of differences in the restriction map of P. griseofulvum NRRL 991 with respect to the rest of the P. griseofulvum strains prompted us to confirm by RAPD experiments that all of the P. griseofulvum collection strains had been correctly identified (Fig. The pattern of bands obtained with the primers used (see Materials and Methods) clearly indicated that all the strains belonged to the species P. griseofulvum ; therefore, the change in the restriction map of strain NRRL 991 is just a consequence of the genetic variability between P. RAPD analysis of seven strains previously classified as P. Primers and PCR conditions are indicated in Materials and Methods. The pattern of bands shown by the different strains clearly indicated that all of them belonged to the species P. griseofulvum NRRL 2300; 2, NRRL 991; 3, NRRL 992; 4, NRRL 994; 5, NRRL 989; 6, NRRL 2152; 7, P. verrucosum a striking result was obtained with probes C, D, and E. A 2.5-kb hybridization signal apparently belonging to the pcbAB gene was observed with probe C, which corresponds to the 3? end of pcbAB , whereas with probes D (adjacent to probe C) and E (corresponding to the 5? end of the gene) a signal of about 12.5 kb was found that did not coincide with the Eco RI restriction map of the pcbAB gene of the other species (Fig. The 12.5-kb signal could be explained either by the presence of the pcbAB gene with a different Eco RI restriction map (where only the two Eco RI sites at the 3? end of the gene had been conserved) or by a phenomenon of heterologous hybridization with another gene having a high degree of similarity with the pcbAB gene. To further investigate these possibilities, different DNA fragments from P. verrucosum genomic DNA were PCR amplified and sequenced. First, we studied whether the 2.5-kb Eco RI fragment located at the 3? end of the pcbAB gene was present in P. verrucosum , as suggested by the result of the hybridization with probe C (Fig. For this purpose the primers NALAB1 and NALAB2, designed according to the sequence of the P. chrysogenum pcbAB gene (situated at bp 9410 and 10430, respectively, from the ATG) (6), were used to amplify by PCR a DNA fragment of approximately 1 kb from P. verrucosum , included within the 2.5-kb Eco RI fragment. Partial sequence analysis of the amplified fragment showed 95% identity with the P. chrysogenum gene at the DNA level, thus confirming the presence of the 3? end of the pcbAB gene in P. Another pair of primers, PCAB1 and PCAB2, designed also from the P. chrysogenum pcbAB sequence and belonging to the central part of the gene (located at bp 4497 and 5291, respectively, from the ATG) between probes D and E was used to test the presence of that portion of the pcbAB gene in P. griseofulvum NRRL 2300 and NRRL 991 were used as control templates in the PCR. A fragment of the expected size, about 0.8 kb, was amplified with different intensities in all the strains, though in P. verrucosum additional fragments were also amplified (not shown). verrucosum 0.8-kb fragment was subcloned and partially sequenced, showing also a very high percentage of identity (96%) at the DNA level to the corresponding fragment of the P. This result confirmed the presence of the central part of the pcbAB gene (corresponding to the second activating domain of the enzyme) in P. The pcbAB gene encodes ACV synthetase, an enzyme belonging to the family of the nonribosomal peptide synthetases. These enzymes are organized in domains, each activating one amino acid. In each domain there are several conserved boxes that have different functions in the enzyme (21, 35). To test whether the hybridization signal of 12.5 kb observed in P. verrucosum with probes D and E was due to a gene with a high degree of identity with the pcbAB , the following approach was developed. Two degenerated oligonucleotides, PVCB and PVCG, were designed according to the amino acid sequence of boxes B and G, following the codon usage of P. With these primers, a temperature gradient PCR was performed. Several bands amplified; among these, one of the expected size for the pcbAB gene domains (1.0 kb) became predominant at higher temperatures. This band when subcloned was shown to be composed of two different DNA fragments, which corresponded, respectively, to positions 1190 to 2197 and 4472 to 5467, numbered from the P. The sequence of these fragments revealed that they corresponded, respectively, to the first and second activating domains of the ACV synthetase, and showed a high degree (92 to 96%) of identity at the DNA level with the pcbAB gene of P. Eleven other amplified fragments of different sizes were subcloned and sequenced. Their sequences did not show significant identity with peptide synthetases. Therefore, we concluded that the 12.5-kb hybridization signal in P. verrucosum corresponds to the pcbAB gene and that this gene is present apparently in all its length in this fungus; no evidence for the possible presence of additional peptide synthetase genes in P. Among different fungal species belonging to the genus Penicillium that are currently used as starter cultures in the food industry or that are frequently isolated from cured meat products, only P. griseofulvum (in addition to the previously reported P. nalgiovense ) was found to produce penicillin and possess the three penicillin biosynthetic genes ( pcbAB , pcbC , and penDE ). It is important that the commonly used cheese starters P. roqueforti neither are penicillin producers nor possess the penicillin biosynthetic genes, which implies that they do not represent a risk regarding the problem of the presence of penicillin in food. griseofulvum is frequently isolated from corn, wheat, barley, flour, and walnuts (40) and from meat products (27), thus being a potential source for the presence of penicillin in food. griseofulvum strains used in the present study was sensitive to ?-lactamase, indicating that P. griseofulvum is a penicillin producer, which was confirmed by HPLC (Fig. griseofulvum strains—NRRL 991, NRRL 992, and NRRL 989—an antibacterial activity could still be detected in the presence of excess ?-lactamase, suggesting that another compound with antibacterial activity must be produced and secreted to the medium in these strains.
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