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Revisado por pares
Characterization of a bacteriocin produced by a newly isolated Bacillus sp. Strain 8 A
2002; Oxford University Press; Volume: 93; Issue: 3 Linguagem: Inglês
10.1046/j.1365-2672.2002.01720.x
ISSN1365-2672
AutoresDelmar Bizani, Adriano Brandelli,
Tópico(s)Microbial Metabolites in Food Biotechnology
ResumoJournal of Applied MicrobiologyVolume 93, Issue 3 p. 512-519 Free Access Characterization of a bacteriocin produced by a newly isolated Bacillus sp. Strain 8 A D. Bizani, D. Bizani Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, 91501–970 Porto Alegre, BrazilSearch for more papers by this authorA. Brandelli, A. Brandelli Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, 91501–970 Porto Alegre, BrazilSearch for more papers by this author D. Bizani, D. Bizani Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, 91501–970 Porto Alegre, BrazilSearch for more papers by this authorA. Brandelli, A. Brandelli Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, 91501–970 Porto Alegre, BrazilSearch for more papers by this author First published: 12 August 2002 https://doi.org/10.1046/j.1365-2672.2002.01720.xCitations: 117 * Correspondence to: A. Brandelli, ICTA – UFRGS, Avenue. Bento Gonçalves 9500, 91501–970 Porto Alegre, Brazil (e-mail: abrand@vortex.ufrgs.br abrand@vortex.ufrgs.br) AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Aims: The aim of this research was to investigate the production of bacteriocins by Bacillus spp. isolated from native soils of south of Brazil. Methods and Results: A bacteriocin produced by the bacterium Bacillus cereus 8 A was identified. The antimicrobial activity was produced starting at the exponential growth phase, although maximum activity was at stationary growth phase. A crude bacteriocin obtained from culture supernatant fluid was inhibitory to a broad range of indicator strains, including Listeria monocytogenes, Clostridium perfringens, and several species of Bacillus. Clinically relevant bacteria such as Streptococcus bovis and Micrococcus luteus were also inhibited. Bacteriocin was stable at 80°C, but the activity was lost when the temperature reached 87°C. It was resistant to the proteolytic action of trypsin and papain, but sensitive to proteinase K and pronase E.Bacteriocin activity was observed in the pH range of 6·0–9·0. Conclusions: A bacteriocin produced by Bacillus cereus 8 A was characterized, presenting a broad spectrum of activity and potential for use as biopreservative in food. Significance and impact of study: The identification of a bacteriocin with large activity spectrum, including pathogens and spoilage microorganisms, addresses an important aspect of food safety. Introduction Bacteriocins are bacterial peptides that inhibit or kill microorganisms that are usually, but not always, closely related to the producer strain (Klaenhammer 1988). Bacteriocins are classified into different groups (Klaenhammer 1993). Class I bacteriocins (lantibiotics) are small peptides that undergo extensive post-translational modification to produce the active peptide. Nisin, the most studied bacteriocin, belongs to class I bacteriocins, which are active against a broad spectrum of food spoilage and pathogenic bacteria, including Listeria monocytogenes (Maisnier-Patin et al. 1992). Class II bacteriocins are heat-stable, low molecular weight, membrane-active peptides. Members of class III are large heat-labile proteins, and a fourth class (complex bacteriocins) has also been suggested, requiring nonprotein moieties for activity (Klaenhammer 1993). Bacteriocins from a variety of Gram-positive species have been biochemically and genetically characterized, including staphylococci (Navaratna et al. 1998; Oliveira et al. 1998) and coryneform bacteria (Valdés-Stauber et al. 1991; Motta and Brandelli 2002). Because of their potential use as natural preservatives, bacteriocins produced by lactic acid bacteria have been subject of intensive investigation in recent years (Nettles and Barefoot 1993; Eijsink et al. 1998), and many attempts are being made to incorporate bacteriocins into process and products. However, only nisin A has been granted Generally Recognized as Safe (GRAS) status by the US Food and Drug Administration. Bacillus is an interesting genus to investigate for antimicrobial activity since Bacillus species produce a large number of peptide antibiotics representing several different basic chemical structures (von Döhren 1995). The production of bacteriocins or bacteriocin-like substances has been already described for B. subtilis, B. cereus, B. stearothermophilus, B. megaterium and other Bacillus species (Tagg et al. 1976). Although several bacteriocin producing strains are active against a narrow spectrum of bacteria (Naclerio et al. 1993; Lee et al. 2001), some strains produce bacteriocins with a broad spectrum of activity, including important pathogens such as L. monocytogenes (Oscariz and Pisabarro 2000) and Streptococcus pyogenes (Cherif et al. 2001). The objective of this study was to evaluate the potential antimicrobial activity of a bacteriocin produced by a Bacillus sp. strain 8 A isolated from native soils of south of Brazil. The antimicrobial spectrum and some properties of the bacteriocin are described. Materials and methods Reagents and media Nutrient broth was from Difco (Detroit, USA), BHI and MRS were from Oxoid (Basingstone, UK). Trypsin, Proteinase K, Pronase E, β-N-acetylglucosaminidase and β-glucuronidase were from Sigma (St. Louis, USA). α-Amylase and β-galactosidase were from Novo Nordisk (Bagsvaerd, Denmark). All other media and reagents were from Merck (Darmstadt, Germany). Bacterial cultures Indicator strains listed in Table 1 are laboratory stocks obtained from different sources and were kept frozen in 20% (v/v) glycerol at −20°C. The organisms were propagated in appropriate media and temperature, as indicated in Table 1. Table 1. Antimicrobial activity spectrum of bacteriocin * Indicator organism Medium Temperature (°C) Inhibition zone (mm)† Bacillus subtilis ATCC 9372 BHI 37 18 Bacillus subtilis var niger (food isolate) BHI 37 13 Bacillus cereus ATCC 9634 BHI 37 14 Bacillus stearothermophilus ATCC 31195 BHI 37 15 Bacillus coagulans (clinical isolate) BHI 37 15 Bacillus macerans (clinical isolate) BHI 37 15 Lactobacillus acidophilus ATCC 4356 MRS 30 8 Lactobacillus plantarum ATCC 8014 MRS 30 – Lactobacillus casei (food isolate) MRS 30 – Lactobacillus rhamnosus (food isolate) MRS 30 – Lactococcus lactis R704 MRS 30 – Listeria monocytogenes ATCC 7644 BHI 37 16 Listeria innocua (food isolate) BHI 37 12 Staphylococcus aureus ATCC 25923 BHI 37 – Streptococcus sp. (α-haemolytic) BA 37 – Streptococcus pyogenes (clinical isolate) BA 37 – Streptococcus bovis (clinical isolate) BA 37 12 Streptococcus uberis (clinical isolate) BA 37 12 Enterococcus faecalis (clinical isolate) BA 37 11 Micrococcus luteus (clinical isolate) BA 37 13 Corynebacterium pyogenes (clinical isolate) BHI 37 – Corynebacterium fimi NCTC 7547 BHI 37 11 Corynebacterium glutamicum ATCC 14752 BHI 37 – Brevibacterium linens ATCC 19391 BHI 37 12 Clostridium perfringens ATCC 3624 RCM 37 12 Clostridium septicum (clinical isolate) RCM 37 10 Enterobacter aerogenes (clinical isolate) BHI 37 – Escherichia coli ATCC 25922 BHI 37 – Escherichia coli (ETEC) BHI 37 – Salmonella Enteritidis ATCC 13076 BHI 37 – Pseudomonas aeruginosa (clinical isolate) BHI 37 – Pseudomonas fluorescens (clinical isolate) BHI 37 – Pasteurella haemolytica (clinical isolate) BHI 37 11 Aeromonas hydrophila (clinical isolate) BHI 30 – Aeromonas salmonicida (clinical isolate) BHI 30 – Klebsiella oxytoca (clinical isolate) BHI 37 – Edwardsiella tarda (clinical isolate) BHI 30 – Proteus mirabilis (clinical isolate) BHI 37 – Alcaligenes faecalis (clinical isolate) BHI 30 – Erwinia carotovora (food isolate) BHI 25 – Kluyveromyces marxianus CBS 6556 SAB 37 – Candida albicans (clinical isolate) SAB 37 – Candida kefir (food isolate) SAB 37 – Aspergillus sp. (food isolate) SAB 37 – Penicillium sp. (food isolate) SAB 37 8 Fusarium sp. (food isolate) SAB 37 – Pyrenophora sp. (food isolate) SAB 37 – * Aliquots of 20 μl were applied to discs, corresponding to 32 AU per disc. † Diameter of the inhibition zone in mm around the disc. BA, sheep blood agar; BHI, brain hearth infusion; MRS, de Man-Rogosa-Sharpe agar, RCM, reiforced clostridial medium; SAB, Sabouraud's agar. Corynebacterium fimi NCTC 7547 was used as a positive control since it is described as susceptible to all bacteriocins tested (Oliveira et al. 1998). Isolation of microorganisms Soil samples were collected at native woodlands of south of Brazil (28–29°S, 51°W). Samples were obtained by removing the leaf litter and collecting the top 10 cm of soil. Soil samples (100 g moist weight) were mixed with sterile water (1 : 1 w/v), homogenized for 15 min at 60 cycles in a laboratory blender (Seward, London, UK), and allowed to stand for 1 h at room temperature. One ml of this suspension was inoculated into 100 ml of nutrient broth, after microbial growth was observed by turbidity, aliquots were inoculated onto nutrient agar plates, incubated at 30°C, and single colonies were isolated and screened for antimicrobial activity. Bacterial identification Bacterial identification was based on morphological and biochemical tests, conducted at Department of Bacteriology, Fundação Oswaldo Cruz (FIOCRUZ, Rio de Janeiro, Brazil). Preparation of crude bacteriocin To produce bacteriocin, bacteria were grown in 200 ml of brain heart infusion (BHI) medium at 30°C in a rotary shaker at 125 cycles per min for desired times. The cells were harvested by centrifugation at 10 000 × g for 15 min and culture supernatants were filtered through 0·22 μm membranes and stored in sterile flasks at 4°C until used for antimicrobial assay. Bacteriocin activity assay The antimicrobial activity was detected by agar disk diffusion assay (Kimura et al. 1998) and was tested against all indicator strains. An aliquot of 20 µl cell-free culture supernatant was applied on disks (6 mm) on agar plates previously inoculated with 0·3 ml of each individual indicator strain suspension, which corresponded to a 0·5 McFarland turbidity standard solution. Plates were incubated at optimal temperature of the test organism. The bacteriocin titre was determined by the serial two-fold dilution method previously described by Mayr-Harting et al. (1972). Activity was defined as the reciprocal of the dilution after the last serial dilution giving a zone of inhibition and expressed as activity units (AU) per millilitre. Growth determination The determination of the number of viable cells (colony forming units, CFU ml−1) was carried out as described elsewhere (Motta and Brandelli 2002). Bacterial growth was developed at 25°C on a rotary shaker. At 8 h intervals, the bacterial suspension was diluted to 10−8 in 8·75 g l-1 NaCl, samples were homogenized and then loaded (20 μl) in triplicate onto nutrient agar plates. Plates were incubated for 24 h at 30°C and counts performed on plates having between 30 and 300 colonies. In parallel, optical density (OD) of the cultures was measured at 600 nm with a Hitachi U-1100 spectro- photometer (Hitachi, Tokyo, Japan). Effects of proteolytic enzymes, heat and pH on antimicrobial activity Proteolytic enzymes were tested on cell-free supernatant. Samples of 1 ml were treated at 37°C for 1 h with either 1 mg ml-1 or 2 mg ml-1 final concentration of the following enzymes: papain, trypsin, proteinase K, pronase E, α-amylase, β-glucuronidase, β-galactosidase and β-N-acetylglucosaminidase. Samples were then boiled for 2 min to inactivate the enzyme. To analyse thermal stability, samples of bacteriocin were exposed to temperatures ranging from 25 to 90°C for 30 min, 100°C for 1–15 min, 121°C (103.5 kPa) for 15 min and frozen for up to 30 days. The activity of bacteriocin at different pH values was estimated by adjusting the pH of supernatant samples to pH 3–11. Chemicals (working concentrations in Table 4) were added to the bacteriocin and the samples were incubated for 1 h at 25°C before being tested for antimicrobial activity. After the treatments, the samples were tested for antimicrobial activity against B. cereus ATCC 14579. Figure 4Open in figure viewerPowerPoint Effect of pH on the bacteriocin activity. Bacteriocin (3200 AUml−1) was subjected to assays of antibacterial activity at various pHvalues. Activity is expressed as the percentage of maximum activitydetermined against B. cereus ATCC 14579 Results Isolation and identification of bacteriocin-producing strain The isolates were screened for antibacterial activity against C. fimi NCTC 7547 and B. cereus ATCC 14579 as indicator strains. The isolate 8 A was selected by producing higher inhibition zones. This microorganism is a Gram-positive spore-forming bacterium, presenting catalase- and lecitinase-positive reactions. Except for the presence of a subterminal spore, all physiological and morphological characteristics were identical to Bacillus cereus ATCC 2599 (Claus and Berkeley 1986). The preliminary identification of this strain was based on phenotypical characteristics, indicating Bacillus cereus. Bacteriocin production Strain 8 A was aerobically incubated in BHI broth at different temperatures in a rotary shaker. Cell growth reached the stationary phase at 8 h of cultivation, and similar growth curves were observed at 25 and 30°C (Fig. 1a). Kinetics of bacteriocin production studied in BHI broth shown that synthesis and/or secretion started at the exponential growth phase at 25 and 30°C, with maximum activity observed at the late stationary growth phase (Fig. 1b). Maximum values of antibacterial activity were observed at 30°C, corresponding to 3200 AU ml−1. When the temperature was increased to 37°C, the bacteriocin activity decreased to 600 AU ml−1. Figure 1Open in figure viewerPowerPoint Production of antimicrobial activity during growth of Bacillus cereus A8 in TSB-modified medium. (a) Bacterial growth and (b) antibacterial activity was monitored at 25°C (•), 30°C (▮), and 37°C (▴) at the indicated times. Each point represents the mean of three independent experiments The number of viable cells (CFU ml−1) and pH was also determined during growth of the strain 8 A (Fig. 2). The values of CFU ml−1 correlate well with OD (r2 value of 0·98). It was observed that pH values increased from 7·5 to 8·5 at the end of incubation. Figure 2Open in figure viewerPowerPoint Viable cell counts (•) and pH values (▮) during growth of Bacillus cereus A8 in BHI broth. Each point represents the mean of three independent experiments Inhibitory spectrum of bacteriocin Cell-free supernatant of a culture of Bacillus cereus 8 A was tested for the presence of antimicrobial activity against several strains, including Gram-positive and Gram-negative bacteria, yeast and moulds. The results are shown in Table 1. Inhibitory activity was observed on several Gram-positive bacteria, including important pathogenic and spoilage microorganisms such as Clostridium perfringens, B. cereus and L. monocytogenes. Clinically relevant bacteria such as Streptococcus bovis, Strep. uberis and Micrococcus luteus were also inhibited. Among the Gram-negative bacteria tested, only Pasteurella haemolytica was inhibited. The yeasts tested were not inhibited, but a Penicillium sp. strain was inhibited. Larger inhibitory zones were observed against species of Bacillus. The producer strain was not inhibited by its bacteriocin. B. cereus ATCC 14579 was used as indicator strain in subsequent experiments. Effect of enzymes, heat and pH on antimicrobial activity To test the effect of proteolytic enzymes, 3200 AU ml−1 of bacteriocin were tested for sensibility to papain, trypsin, proteinase K and pronase E, and residual activity was measured by agar disk diffusion assay against B. cereus ATCC 14579. The bacteriocin was sensitive to proteinase K and pronase E at the concentration of 2 mg ml-1 (Table 2), but was not sensible to these enzymes at 1 mg ml-1. Table 2. Effect of enzymes on bacteriocin activity * Treatment Residual Activity (%) Untreated bacteriocin 100 Trypsin 100 Papain 100 Proteinase K 0 Pronase E 0 α-amylase 100 β-glucuronidase 100 β-galactosidase 100 β-N-acetylglucosaminidase 100 * Bacteriocin was treated with 2 mg/ml of each enzyme and then boiled for 2 min at 100°C for enzyme inactivation. Controls with each enzyme were performed. The effect of glycosidases on bacteriocin activity was also tested. None of the glycosidases tested reduced the antimicrobial activity (Table 2). The bacteriocin was incubated for 30 min at different temperatures and residual activity was measured. It was stable at 80°C, but the activity gradually decreased with the increase in temperature. The residual activity was 90% after incubation at 82°C, and total loss of activity was observed after incubation at 87°C or more (Fig. 3a and Table 3). When the bacteriocin was incubated at 100°C, the residual activity was 80% after 2·5 min, but it was completely absent after 3 min incubation (Fig. 3b). Bacteriocin activity was not lost by cooling or freezing storage (Table 3). Figure 3Open in figure viewerPowerPoint Thermal stability of the bacteriocin. Bacteriocin (3200 AU ml−1) was incubated at various temperatures for 30 min (A) or at 100°C for different times (B) and residual activity was measured. Activity is expressed as the percentage of residual activity determined against B. cereus ATCC 14579 Table 3. Thermal stability of bacteriocin on different conditions Treatment Residual activity (%) 100°C/15 min 0 121°C/103·5 kPa/15 min 0 4°C/30 d 100 −20°C/30 d 100 Freeze-dried 100 The bacteriocin was active over a pH range of 5·0–8·0, but it was inactivated when incubated outside of these limits (Fig. 4). The effect of several chemicals on the antimicrobial activity was evaluated. The bacteriocin lost its activity after treatment with trichloroacetic acid (Table 4). Antimicrobial activity was not affected by treatment with organic solvents, detergents or EDTA (Table 4). Table 4. Effect of chemicals on bacteriocin activity * Treatment Concentration Residual activity (%) Acetone 10% (v/v) 100 Chloroform 10% (v/v) 92 Dimethyl sulfoxide 10% (v/v) 100 Ethanol 10% (v/v) 92 Methanol 10% (v/v) 100 Ethyl ether 10% (v/v) 100 Xylol 10% (v/v) 100 EDTA 10 mmol l-1 83 Trichloroacetic acid† 100 mg ml-1 0 Sodium deoxycholate 1 mg ml-1 100 Sulphobetaine 14 1 mg ml-1 92 Triton X-100 1% (v/v) 100 Tween 20 10% (v/v) 100 Tween 80 10% (v/v) 92 * Bacteriocin was previously incubated for 1 h at 25°C with chemicals and then assayed for antimicrobial activity. Controls with each chemical were adequately done. † After treatment with TCA samples were centrifuged at 10 000 × g for 5 min and the supernatant was neutralized to pH 7·0 before testing for antimicrobial activity. Considering the properties of the inhibitory substance produced by Bacillus cereus 8 A, it was characterized as a bacteriocin-like compound. We propose cerein 8 A as a designation for this bacteriocin. Discussion A bacteriocin-producing bacterium was isolated from soil samples of native woodlands of south of Brazil. Strain 8 A was preliminarily identified as Bacillus cereus by biochemical profiling, and its antimicrobial activity was released into culture broth during cultivation. B. cereus ATCC 14579, C. perfringens ATCC 3624 and L. monocytogenes ATCC 7644, among other bacteria were inhibited by this antimicrobial activity. Among Gram-negative bacteria tested only P. haemolytica was sensitive. C. fimi NCTC 7547, which is described as susceptible to all bacteriocins tested (Oliveira et al. 1998), was sensitive for bacteriocin of strain 8 A as well. The bacteriocin was able to inhibit the growth of L. monocytogenes and C. perfringens, a very important property to food safety. Bacillus spp. has been also considered as a potential agent to biological control against phytopathogenic fungi (Podile and Prakash 1996; Yoshida et al. 2001). In this regard, inhibitory effect against Penicillium sp. was also observed, although all other fungi tested were insensitive. Since the tests were performed with a crude bacteriocin preparation, the possibility that there is a different molecule showing antifungal activity can not be ruled out. The inhibition of bacterial strains involved in bovine mastitis by cerein 8 A would be very beneficial to the cattle industry. Because bacteriocin treatment is inexpensive, effective and nontoxic to animals and humans, it has been already proposed as an alternative strategy for disease control (Milles et al. 1992; Oliveira et al. 1998). The bacteriocin produced by the strain 8 A may represent an antimicrobial substance with potential application in the prevention and treatment of mastitis. Although some bacteriocins from Bacillus present a narrow antimicrobial spectrum, the antibacterial activity of cerein 8 A was comparable to broad-range bacteriocins associated with Bacillus spp. Oscariz and Pisabarro (2000), isolated and identified cerein 7, a bacteriocin produced by B.cereus Bc7, that was inhibitory for growth of Listeria spp. and other gram-positive bacteria. Coagulin, a bacteriocin-like substance produced by B. coagulans I4 has been reported (Hyronimus et al. 1998). It presents a large antibacterial spectrum, inhibiting strains of the same species as the producer strain. In addition, a B. brevis strain isolated from kimchi produce a bacteriocin active on a broad spectrum of bacteria, including some pathogens food-spoilage microorganisms, and some yeast strains (Mah et al. 2001). Bacteria can produce a variety of inhibitory substances. In this case, it is unlikely that organic acid causes the inhibition observed. Although B. cereus can produce acids from carbohydrates, the pH in the growth medium of Bacillus sp. strain 8 A was in the range of 7·5–8·5. An increase in pH during cultivation is often associated with proteolytic microorganisms. Indeed, the production of extracellular proteases by B. cereus has been described (Makinen and Makinen 1987) and proteolytic activity could be harmful to antimicrobial peptides. Bacteriocin activity was not lost during cultivation, indicating that the bacteriocin is resistant to extracellular proteases of B. cereus. Bacillus spp. produce antimicrobials which are cyclic peptides containing unusual amino acids, therefore more resistant to proteases (von Döhren 1995). In agreement with this fact, cerein 8 A was resistant to papain and trypsin hydrolysis. In the evaluation of bacteriocin properties, its inhibitory activity was sensitive to microbial proteases and was lost with trichloroacetic acid (TCA) treatment, which indicates its proteinaceous nature. Other bacteriocins produced by Bacillus, such as cerein and coagulin I4, are often less resistant to proteolytic treatments (Naclerio et al. 1993; Hyronimus et al. 1998). None of the glycosidases tested affect the activity, contrary to observed for carnocin LA54A (Keppler et al. 1994), suggesting that cerein 8 A is not a complex bacteriocin. Total loss of activity was observed after incubation at 87°C or higher, but activity was maintained at 80°C, indicating the inhibitory compound was relatively heat stable. Some studies have addressed the use of bacteriocins for food protection. Bacillus strains cause the inhibition of Clostridium butolinum in challenge studies on surimi nuggets (Lyver et al. 1998). Inhibition of L. monocytogenes has been already described for some foods such as meats (Ming et al. 1997) and cheese (Ennahar et al. 1998). However, increased tolerance of L. monocytogenes to conventional bacteriocins, such as nisin and pediocin, have been reported (Rasch and Knochel 1998; van Schaik et al. 1999). Therefore, research for new products presenting antimicrobial activity is a very important field. In addition, current starters were not inhibited by cerein 8 A, which is an attractive property of this bacteriocin for food industry use. Bacteriocins have gained importance as natural biopreservatives for control of spoilage and pathogenic organisms in foods. This study indicates the importance of the bacteriocin produced by Bacillus cereus 8 A against pathogenic microorganisms such as L. monocytogenes and C. perfringens. The identification and characterization of bacteriocins, and exploring their potential use in the biological control of pathogenic and spoilage microorganisms, addresses a very important aspect of food protection. Acknowledgements D.B. has received a Ph.D. fellowship from CNPq, Brazil. A.B. is Research Fellow of CNPq. References Cherif, A., Ouzari, H., Daffonchio, D., Cherif, H., Bem Slama, K., Hassen, A., Jaoua, S. and Boudabous, A. (2001) Thuricin 7: a novel bacteriocin produced by Bacillus thuringiensis BMG1.7, a new strain isolated from soil. Letters in Applied Microbiology 32, 2434– 2247. Wiley Online LibraryWeb of Science®Google Scholar Clauss, D. and Berkeley, R.C.W. (1986) Genus Bacillus Cohn 1872. In: Bergey's Manual of Determinative Bacteriology, Vol. 2 ed. P.H.A. Sneath, pp. 1105– 1141. Baltimore: Williams & Wilkins. Google Scholar Von Döhren, H. (1995) Peptides. In: Genetics and Biochemistry of Antibiotic Production ed. L.C. Vining and C Stuttard, pp. 129– 171. Newton, MA: Butterworth-Heinemann. Google Scholar Eijsink, V.G.H., Skeeie, M., Middelhoven, P.H., Brurberg, M.B. and Nes, I.F. (1998) Comparative studies of class IIa bacteriocins of lactic acid bacteria. Applied and Environmental Microbiology 64, 3275– 3281.CASPubMedWeb of Science®Google Scholar Ennahar, S., Assobhei, O. and Hasselmann, C. (1998) Inhibition of Listeria monocytogenes in a smear-surface soft cheese by Lactobacillus plantarum WHE 92, a pediocin AcH producer. Journal of Food Protection 61, 186– 191.CrossrefCASPubMedWeb of Science®Google Scholar Hyronimus, B., Le Marrec, C. and Urdaci, M.C. (1998) Coagulin, a bacteriocin-like inhibitory substance produced by Bacillus coagulans I4. Journal of Applied Microbiology 85, 42– 50.DOI: 10.1046/j.1365-2672.1998.00466.xWiley Online LibraryCASPubMedWeb of Science®Google Scholar Keppler, K., Geisen, R. and Holzapfel, W.H. (1994) An α-amylase sensitive bacteriocin of Leuconostoc carnosum. Food Microbiology 11, 39– 45.DOI: 10.1006/fmic.1994.1006CrossrefCASWeb of Science®Google Scholar Kimura, H., Sashihara, T., Matsusaki, H., Sonomoto, K. and Ishizaki, A. (1998) Novel bacteriocin of Pediococcus sp. ISK-1 isolated from well-aged bed of fermented rice bran. Annals of New York Academy of Sciences 864, 345– 348. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Klaenhammer, T.R. (1988) Bacteriocins of lactic acid bacteria. Biochimie 70, 337– 349.CrossrefCASPubMedWeb of Science®Google Scholar Klaenhammer, T.R. (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiology Reviews 12, 39– 86.Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Lee, K.H., Jun, K.D., Kim, W.S. and Paik, H.D. (2001) Partial characterization of polyfermenticin SCD, a newly identified bacteriocin of Bacillus polyfermenticus. Letters in Applied Microbiology 32, 146– 151.Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Lyver, A., Smith, J.P., Austin, J. and Blanchfield, B. (1998) Competitive inhibition of Clostridium butulinum type E by Bacillus species in a value-added seafood product packaged under a modified atmosphere. Food Research International 31, 311– 319.DOI: 10.1016/S0963-9969(98)00097-0CrossrefWeb of Science®Google Scholar Mah, J.H., Kim, K.S., Park, J.H., Byun, M.W., Kim, Y.B. and Hwang, H.J. (2001) Bacteriocin with a broad antimicrobial spectrum, produced by Bacillus sp. isolated from kimchi. Journal of Microbiology and Biotechnology 11, 577– 584. CASWeb of Science®Google Scholar Maisnier-Patin, S., Deschamps, N., Tatini, S.R. and Richard, J. (1992) Inhibition of Listeria monocytogenes in Camembert cheese made with a nisin-producing starter. Lait 72, 249– 263. CrossrefCASGoogle Scholar Makinen, K.K. and Makinen, P.L. (1987) Purification and properties of an extracellular collagenolytic protease produced by the human oral bacterium Bacillus cereus (strain SOC-67). Journal of Biological Chemistry 262, 12488– 12495.CASPubMedWeb of Science®Google Scholar Mayr-Harting, A., Hedges, A.J. and Berkeley, C.W. (1972) Methods for studying bacteriocins. In: Methods in Microbiology, Vol. 7 ed. J.R. Norris and D. Ribbons, pp. 315– 412. New York: Academic Press. Google Scholar Milles, H., Lesser, W. and Sears, P. (1992) The economic implication of bioengineered mastitis control. Journal of Dairy Science 75, 596– 605.CrossrefPubMedWeb of Science®Google Scholar Ming, X., Weber, G.H., Ayres, J.W. and Sandine, W.E. (1997) Bacteriocins applied to food packaging materials to inhibit Listeria monocytogenes on meats. Journal of Food Science 62, 413– 415. Wiley Online LibraryCASWeb of Science®Google Scholar Motta, A.S. and Brandelli, A. (2002) Characterisation of an antimicrobial peptide produced by Brevibacterium linens. Journal of Applied Microbiology 92, 63– 70.Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Naclerio, G., Ricca, E., Sacco, M. and Defelice, M. (1993) Antimicrobial activity of a newly identified bacteriocin of Bacillus cereus. Applied and Environmental Microbiology 59, 4313– 4316.CASPubMedWeb of Science®Google Scholar Navaratna, M.A.D.B., Sahl, H.G. and Tagg, J.R. (1998) Two-component anti-Staphylococcus aureus lantibiotic activity produced by Staphylococcus aureus C55. Applied and Environmental Microbiology 64, 4803– 4808.CrossrefCASPubMedWeb of Science®Google Scholar Nettles, C.G. and Barefoot, S.F. (1993) Biochemical and genetic characteristics of bacteriocins of food associated lactic acid bacteria. Journal of Food Protection 56, 338– 356. CrossrefCASPubMedWeb of Science®Google Scholar Oliveira, S.S., Abrantes, J., Cardoso, M., Sordelli, D. and Bastos, M.C.F. (1998) Staphylococcal strains involved in bovine mastitis are inhibited by Staphylococcus aureus antimicrobial peptides. Letters in Applied Microbiology 27, 287– 291.Wiley Online LibraryPubMedWeb of Science®Google Scholar Oscariz, J.C. and Pisabarro, A.G. (2000) Characterization and mechanism of action of cerein 7, a bacteriocin produced by Bacillus cereus Bc7. Journal of Applied Microbiology 89, 361– 369.DOI: 10.1046/j.1365-2672.2000.01123.xWiley Online LibraryCASPubMedWeb of Science®Google Scholar Podile, A.R. and Prakash, A.P. (1996) Lysis and biological control of Aspergillus niger by Bacillus subtilis AF1. Canadian Journal of Microbiology 42, 533– 538.CrossrefCASPubMedWeb of Science®Google Scholar Rasch, M. and Knochel, S. (1998) Variations in tolerance of Listeria monocytogenes to nisin, pediocin PA-1 and bavaricin A. Letters in Applied Microbiology 27, 275– 278.Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Van Schaik, W., Gahan, C.G.M. and Hill, C. (1999) Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. Journal of Food Protection 62, 536– 539.CrossrefCASPubMedWeb of Science®Google Scholar Tagg, J.R., Dajani, A.S. and Wannamaker (1976) Bacteriocins of gram-positive bacteria. Bacteriology Reviews 40, 722– 756. CASPubMedWeb of Science®Google Scholar Valdés-Stauber, N., Götz, H. and Busse, M. (1991) Antagonistic effect of coryneform bacteria from red smear cheese against Listeria species. International Journal of Food Microbiology 13, 119– 130.CrossrefPubMedWeb of Science®Google Scholar Yoshida, S., Hiradate, S., Tsukamoto, T., Hatakeda, K. and Shirata, A. (2001) Antimicrobial activity of culture filtrate of Bacillus amyloliquefaciens RC-2 isolated from mulberry leaves. Phytopathology 91, 181– 187. CrossrefCASPubMedWeb of Science®Google Scholar Citing Literature Volume93, Issue3September 2002Pages 512-519 FiguresReferencesRelatedInformation
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