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Applied and Environmental Microbiology, September 1998, p. 3313-3319, Vol. 64, No. 9
Department of Food and Environmental Hygiene,
University of Helsinki, Helsinki, Finland,1
and
Department of Microbiology, University of Ghent, Ghent,
Belgium2
Received 26 February 1998/Accepted 15 June 1998
Leuconostoc carnosum was shown to be the specific
spoilage organism in vacuum-packaged, sliced, cooked ham showing
spoilage during 3 weeks of shelf life. Identification of the specific
spoilage organism was done by use of phenotypic data and
ClaI, EcoRI, and HindIII reference
strain ribopatterns. One hundred L. carnosum isolates
associated with the production and spoilage of the ham were further
characterized by pulsed-field gel electrophoresis (PFGE), together with
some meat-associated Leuconostoc species: L. citreum, L. gelidum, L. mesenteroides subsp. dextranicum, and L. mesenteroides subsp. mesenteroides. ApaI and
SmaI digests divided the industrial L. carnosum
strains into 25 different PFGE types, ApaI and
SmaI types being consistent. Only one specific PFGE type was associated with the spoiled packages. This type also was detected in air and raw-meat mass samples. The spoilage strain did not produce
bacteriocins. Only seven isolates belonging to three different PFGE
types produced bacteriocins. Similarity analysis of the industrial L. carnosum strains revealed a homogeneous cluster which
could be divided into eight subclusters consisting of strains having at
most three-fragment differences. The L. carnosum cluster
was clearly distinguished from the other meat-associated leuconostoc clusters, with the exception of the L. carnosum type
strain. Ribotyping can be very helpful in the identification of
L. carnosum, but its discriminatory power is too weak for
strain characterization. PFGE provides good discrimination for studies
dealing with the properties of homogeneous L. carnosum
strains.
Lactic acid bacteria (LAB) are the
major spoilage bacteria in vacuum-packaged, cooked meat products
(1, 2, 10, 13, 25, 27, 31, 38, 44, 47, 56).
Lactobacillus and Leuconostoc have been the main
genera associated with the spoilage of these products,
Lactobacillus sake and Lactobacillus curvatus
being isolated commonly (12, 16, 18, 19, 24, 27, 30, 35, 39,
43-46). Compared to aerobic spoilage bacteria, spoilage LAB produce their typical sensory changes, such as souring, gas formation, and/or slime formation, later, at the stationary phase (29, 44), and a vacuum-packaged product is usually expected to
maintain good sensory quality for at least 3 to 4 weeks. However,
due to an increased level of LAB contamination or particularly active spoilage strains, spoilage may occur during the shelf-life period, subjecting the producer to recalls (30, 31, 33, 46).
In an LAB contamination study of vacuum-packaged, sliced, cooked ham,
982 LAB isolates from the spoiled product and production line were
characterized in order to determine the underlying reasons for
fluctuations in product quality (4, 6). Many lots had been
showing spoilage changes, i.e., sour odor and taste, before the sell-by
date. In that study, ribotyping (21) was used as a tool for
contamination analysis. Based on EcoRI and
HindIII ribopatterns, two major spoilage LAB types,
types G and A, were detected. Contamination with these spoilage LAB was
shown to have occurred postcooking, and a probable site of air-mediated
contamination from the macerated raw-meat mass to the cooked product
was revealed. Because type G showed the typical EcoRI and
HindIII ribopatterns of L. sake
(5), no further identification or characterization studies
were warranted. However, the most important specific spoilage organism,
type A, was not identified to the species level. Type A had been
detected as the dominant type in the macerated raw-meat mass and in the
spoiled packages with the strongest changes in sensory characteristics
(6). It had also persisted in the plant during the 1-year
study period, consisting of two separate large-scale contamination
experiments (4, 6).
In this study, we set out to identify type A LAB to the species level
and characterize in more detail the 100 isolates possessing the type A
EcoRI and HindIII ribopatterns. Since
phenotypic characteristics alone are seldom sufficient for
species identification of LAB (15), a reference strain
library was created by ribotyping and was used with phenotypic
data. Pulsed-field gel electrophoresis (PFGE) was applied in
order to provide further strain-level characterization. Production of
bacteriocins was determined for evaluation of the impact of this
characteristic in a population associated with process contamination
and product spoilage.
Bacterial strains.
One hundred type A LAB possessing the
same EcoRI and HindIII ribopatterns had been
isolated during a contamination study of a meat plant (6).
All isolates were gram-positive, oval cocci isolated from a macerated
raw-meat mass, air in the macerating room, surfaces and air in the
cooking room, worker's gloves, surfaces of the ham prior to slicing,
and vacuum-packaged, sliced, cooked ham cultured on the sell-by date.
Isolates originating from different sources are listed in Table
1.
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Identification and Characterization of
Leuconostoc carnosum, Associated with Production and
Spoilage of Vacuum-Packaged, Sliced, Cooked Ham
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
TABLE 1.
Division of the isolates into different types and certain
phenotypic properties
70°C and cultured with MRS broth or MRS agar (Oxoid, Basingstoke,
United Kingdom) as previously described (28).
Phenotypic characterization. The anaerobic growth of all industrial isolates on Rogosa selective Lactobacillus agar (Orion Diagnostica, Espoo, Finland) was determined, and the scheme of Villiani et al. (55) was used for the presumptive identification of Leuconostoc spp. Gas production from glucose was tested with modified MRS broth in Durham tubes (51). Production of ammonia from arginine was observed by the method of Briggs (14), and dextran formation was studied with 5% sucrose-containing agar (22). Fermentation of carbohydrates was determined by use of the API 50 CH Lactobacillus identification system (Biomerieux, Marcy l'Etoile, France) for five randomly selected isolates (I27a, M1f, V8a, M6f, and P31a), which were also tested for the ability to produce different lactic acid isomers by an enzymatic method (57) with D- and L-lactate dehydrogenases (Boehringer GmbH, Mannheim, Federal Republic of Germany). The five randomly selected isolates were also tested for growth in MRS broth at 8, 10, 15, and 37°C.
Bacteriocin determination. The agar spot test method modified by Schillinger and Lücke (48) was used for screening bacteriocin activity. Based on existing literature, L. mesenteroides subsp. mesenteroides DSM 20343T was selected as the indicator bacterium (3, 26, 40, 54, 58).
In vitro isolation of DNA and ribotyping for species identification. Reference strains and the five randomly selected industrial isolates, already known to possess similar EcoRI and HindIII ribotypes, were characterized with ClaI, EcoRI, and HindIII (New England BioLabs, Beverly, Mass.). These enzymes were selected because they characterize LAB well (4-6). DNA was isolated by the guanidium thiocyanate method of Pitcher et al. (42) as modified by Björkroth and Korkeala (4) by combined lysozyme and mutanolysin treatments. Restriction endonuclease treatment of 3 µg of DNA was done as specified by the manufacturer (New England BioLabs). Genomic blotting was done by vacuum blotting (Vacugene; Pharmacia, Uppsala, Sweden), and the ribosomal DNA probe for ribotyping was labeled by reverse transcription (avian myeloblastosis virus reverse transcriptase [Promega, Madison, Wis.]; Dig DNA labeling kit [Boehringer]) as previously described by Blumberg et al. (11). Membranes were hybridized at 68°C as described by Björkroth and Korkeala (5). Similarity between all ribopatterns was determined visually.
In situ DNA isolation and PFGE. Cells were harvested from 2 ml of MRS broth cultures grown overnight at 30°C. DNA isolation in situ from agarose blocks was performed as described by Maslow et al. (37) with the modifications described by Björkroth et al. (9). Initially, 11 rare-cutting restriction enzymes, ApaI, AscI, EagI, MluI, NotI, NruI, RsrII, SacII, SmaI, XbaI, and XhoI, were tested for the cleavage of DNA of three strains (NCFB 2776T, M6f, and I27a). ApaI and SmaI, which produced convenient numbers of fragments with discriminatory patterns, were chosen for the cleavage of all strains. The samples were electrophoresed through a 1.2% (wt/vol) agarose gel (SeaKem Gold; FMC BioProducts, Rockland, Maine) in 0.5× TBE (45 mM Tris, 4.5 mM boric acid [pH 8.3], 1 mM sodium EDTA) at 14°C by use of a Gene Navigator system with the hexagonal electrode (Pharmacia). Interpolation ramping from 0.5 to 15 s for 20 h at 200 V was used for both enzyme digests.
PFGE data management. Photographs of the PFGE banding patterns were scanned with a ScanJet 4c/T scanner (Hewlett-Packard Co., Boise, Idaho). Numerical analysis of macrorestriction patterns was performed with a GelCompar system (version 4.0; Applied Maths, Kortijk, Belgium). The similarity between all pairs was expressed by Dice coefficient correlation, and clustering by the unweighted pair-group method with arithmetic averages was used for the construction of the dendrogram. Types were considered closely related (53) in the presence of at most a three-band difference (one genetic event). This relationship was indicated in the type nomination by a shared roman numeral.
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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The 100 isolates did not grow on Rogosa selective
Lactobacillus agar; all produced gas from glucose but did
not produce ammonia from arginine. Fifteen isolates (11 different PFGE
types) produced slime from sucrose, and bacteriocins were produced
by 7 isolates (Table 1). The five isolates tested produced only
D-lactic acid and had similar fermentation patterns for the
utilization of ribose, D-glucose,
D-fructose, 
-methyl-D-glucoside,
N-acetylglucosamine, cellobiose, saccharose, trehalose,
-gentiobiose, D-turanose, and gluconate. Growth occurred
at 8, 10, and 15°C but not at 37°C.
Previously determined oval cell morphology and the phenotypic characteristics typical of leuconostocs led to the comparison with the Leuconostoc and Weissella type strains. Figures 1, 2, and 3 show that the ClaI, EcoRI, and HindIII ribotypes, respectively, of the reference strains differed clearly from the Lactobacillus ribotypes obtained previously (5, 7). The ClaI, EcoRI, and HindIII ribopatterns of the industrial isolates were found to be identical to those of L. carnosum NCFB 2776T (Fig. 1, 2, and 3, lanes 10). All of the other type strains were distinct from L. carnosum NCFB 2776T. Based on the phenotypic data and the identical ribopatterns, the industrial isolates were classified as L. carnosum. HindIII and EcoRI generated the least distinguishing ribotypes for the Leuconostoc and Weissella species. ClaI was the only enzyme distinguishing L. mesenteroides subsp. mesenteroides from L. mesenteroides subsp. dextranicum (Fig. 1, lanes 5 and 7).
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Both ApaI and SmaI generated 25 different patterns for the meat plant isolates when one-band differences are noted. The ApaI types were consistent with the SmaI types (Table 1). All meat-associated reference strains, with the exception of L. carnosum NCFB 2776T, were clearly distinguished from the industrial isolates (Fig. 4 and 5). Both ApaI and SmaI resulted in convenient numbers of fragments for macrorestriction analysis (Fig. 4). However, SmaI cleaved the DNA efficiently, whereas some partial digestion was occasionally noted with ApaI. Because of the better reproducibility, SmaI patterns were chosen for the numerical analysis.
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Figure 5 shows the dendrogram of the industrial isolates and the reference strains. L. carnosum formed a homogeneous cluster, within which eight subclusters consisted of strains having at most three-band differences. Reference strains, with the exception of the L. carnosum type strain, clustered separately from the industrial isolates. Isolates associated with the sensorially spoiled products all showed the type A I-h pattern (Fig. 4, lanes 8 and 17) and belonged to the largest cluster, consisting of A I types (Fig. 5 and Table 1). Type A I-h was also detected in two raw-meat mass samples and two air samples, one from the macerating room and one from the postcooking form removal area.
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DISCUSSION |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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L. carnosum was identified as the specific spoilage organism in the vacuum-packaged, cooked ham studied here. This species was described along with L. gelidum by Shaw and Harding in 1989 (50). It belongs to the main Leuconostoc cluster designated Leuconostoc sensu stricto and shares 97 to 99% rRNA homology with the other sensu stricto species: L. citreum, L. gelidum, L. lactis, L. mesenteroides, and L. pseudomesenteroides (15). Characterization studies of L. carnosum have been sparse and have been done with a limited number of strains (50, 58). Studies associated with L. carnosum have mainly focused on the production and purification of bacteriocins produced by this species (3, 20, 23, 26, 40, 41, 49, 52, 54).
L. carnosum seems to be strongly associated with ham products. In an earlier meat production plant contamination study (6), type A was found to dominate in the microflora of the raw-pork mass macerated overnight. In this plant, we noted that L. carnosum contamination occurred mainly in ham, whereas L. sake and L. curvatus have been detected in a variety of products (4, 6). Approximately 36% of the spoilage flora in Vienna sausages has been reported to consist of leuconostocs (17). When these Leuconostoc species were identified (18), the absence of L. carnosum was emphasized. In another characterization study of the LAB causing spoilage in vacuum-packaged, processed meats, a high prevalence of bacteriocin-producing psychrotropic leuconostocs was revealed (58). In that study, nine isolates were identified as L. carnosum; eight of these nine originated from different types of ham and one originated from sliced turkey. The strains forming the L. carnosum cluster (III) in the work describing this species (50) were from cold-stored, vacuum-packaged beef, pork, bacon, cooked ham, and luncheon meat. Compared with ham and other whole-meat products, emulsion sausages have more variable raw materials, such as different meat mixtures, pork skin emulsion, and spices, and undergo a different type of processing. The process and ingredients used for ham manufacturing may favor the survival and/or growth of L. carnosum. However, an adequate cooking process, considered to be the most important factor destroying LAB on products prior to packaging (1, 33, 34, 36), and the use of nitrite are similar in the production of emulsion sausages and whole-meat products.
PFGE characterization of L. carnosum confirmed the assumption that the raw-meat mass was the major source of contamination. The type of LAB contamination in a product has been considered to reflect the type of contamination in the processing facility (25, 38). Various LAB types were shown to contaminate the environment associated with the ham processing line studied here (4, 6). The greatest diversity in the different types of LAB was found in the environmental surface samples (4, 6). However, the majority of these LAB types have never been isolated from packaged products (4, 6). Only type A I-h isolates associated with the spoiled packages (V isolates), raw material (M5o and M6a isolates), and air of the macerating room (isolate I2b) and postcooking form removal area (isolate I27a) contaminated the products before they were transferred to the slicing-packaging department. The products were contaminated with a spoilage organism from the raw-meat mass before they entered the slicing line. In this case, the slicing line and the slicing room were not the main site and source of contamination, as is so often thought (25, 38). This route of contamination may be more common than is generally considered, also explaining the link between raw-meat mass and cooked ham.
Identification of species of the genus Leuconostoc is difficult (15, 55), which apparently is the main reason for the sparse population characterizations published. Leuconostoc spp. are phenotypically related to Weissella spp., heterofermentative lactobacilli, and pediococci and form a natural phylogenetic group with Weissella confusa, W. halotolerans, Weissella kandleri, Weissella minor, and W. viridescens (15). Due to the variable results obtained, sugar fermentation patterns are of little value in the species identification and could lead to misclassification (15). For presumptive identification, the scheme proposed by Villiani et al. (55) was found practical. However, in this scheme L. carnosum is supposed to form dextran. Only 15 of the 100 isolates tested here (11 of the established 25 PFGE types) formed slime from sucrose, lessening the value of this characteristic in L. carnosum identification.
It has been stated that reliable differentiation between L. carnosum and L. gelidum is impossible without DNA-DNA hybridization (15). Our results indicate that ribotyping can be used to distinguish L. carnosum from the other phenotypically related leuconostocs. However, care must be taken when enzymes are selected for species identification by ribotyping. Using HindIII-based ribopatterns, Villiani et al. (55) could not distinguish L. mesenteroides subsp. mesenteroides from L. mesenteroides subsp. dextranicum and L. lactis. We found HindIII and EcoRI to be the least distinguishing enzymes and ClaI to be the only enzyme generating a clear one-band shift in the patterns of these two subspecies (Fig. 1, lanes 5 and 7). ClaI may thus provide better results for the discrimination of L. mesenteroides subspecies. However, the HindIII pattern of the L. lactis type strain was clearly distinguished from the patterns of the L. mesenteroides subspecies (Fig. 3, lanes 5, 7, and 12). Despite its value in species identification and LAB contamination studies dealing with a diversity of species, ribotyping cannot be used for strain characterization when such a homogeneous population, such as the population of L. carnosum isolated from the meat production plant studied here, is assessed.
Only one type, A I-h (Fig. 4, lanes 8 and 17), from the largest lineage, was associated with the sensorially spoiled packages; however, even the production environment was not overwhelmingly contaminated by this specific organism. Strains of this type may possess characteristics that aid in growth niche occupation. Specific spoilage organisms have been considered to have better competitive ability, enabling them to prevail in the microflora present (8, 13, 32). Differences in the generation time, production of bacteriocins, strong ability to produce slime or volatile compounds causing sensorial spoilage, and better resistance to different stress factors, such as cold, heat, and disinfectants, are factors considered to be associated with specific spoilage organisms. For the L. carnosum population studied here, the production of bacteriocins was not found to be a common characteristic, as reported by Yang and Ray (58). The nine L. carnosum isolates studied by Yang and Ray (58) all inhibited L. mesenteroides. The true general impact of bacteriocin production in the development of spoilage flora is still not clear. Studies of bacteriocin production have mainly focused on the use of bacteriocins or cultures producing bacteriocins as biopreservatives. Biopreservatives are inoculated at a high initial concentration or a dense population in a freshly prepared product. This situation differs clearly from the situation in which some or one species in a contaminating flora gradually occupies a niche in a package and, finally, when reaching the stationary phase, spoils the product.
Molecular typing methods also provide valuable information for applied microbiology. They can contribute to knowledge of different bacterial populations associated with food processing and enable future research to be focused accurately on specific spoilage organisms and their specific characteristics. Such work will rely mainly on the reliable species identification and good strain characterization of specific spoilage organisms.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Food and Environmental Hygiene, Faculty of Veterinary Medicine, University of Helsinki, P.O. Box 57, FIN-00014 Helsinki, Finland. Phone: 358-50-5976555. Fax: 358-9-70849718. E-mail: johanna.björkroth{at}helsinki.fi.
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REFERENCES |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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