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Carnobacterium: positive and negative effects in the environment and in foods

Jørgen J. Leisner, Birgit Groth Laursen, Hervé Prévost and 2 more

FEMS Microbiology Reviews · 2007 · Review

doi:10.1111/j.1574-6976.2007.00080.x

Abstract

The genus Carnobacterium contains nine species, but only C. divergens and C. maltaromaticum are frequently isolated from natural environments and foods. They are tolerant to freezing/thawing and high pressure and able to grow at low temperatures, anaerobically and with increased CO(2) concentrations. They metabolize arginine and various carbohydrates, including chitin, and this may improve their survival in the environment. Carnobacterium divergens and C. maltaromaticum have been extensively studied as protective cultures in order to inhibit growth of Listeria monocytogenes in fish and meat products. Several carnobacterial bacteriocins are known, and parameters that affect their production have been described. Currently, however, no isolates are commercially applied as protective cultures. Carnobacteria can spoil chilled foods, but spoilage activity shows intraspecies and interspecies variation. The responsible spoilage metabolites are not well characterized, but branched alcohols and aldehydes play a partial role. Their production of tyramine in foods is critical for susceptible individuals, but carnobacteria are not otherwise human pathogens. Carnobacterium maltaromaticum can be a fish pathogen, although carnobacteria are also suggested as probiotic cultures for use in aquaculture. Representative genome sequences are not yet available, but would be valuable to answer questions associated with fundamental and applied aspects of this important genus.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 18, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Carnobacteria are ubiquitous lactic acid bacteria (LAB) isolated from cold and temperate environments. More importantly from a practical viewpoint, they also frequently predominate in a range of foods, including fish, meat, and some dairy products. In this regard, they have been extensively studied in the last two decades as protective cultures, to inhibit pathogenic and spoilage microorganisms, and as potential spoilage bacteria in chilled seafood and meat products. In addition, owing to their presence in the aqueous environment, their importance as fish pathogens or probiotic cultures in the aquaculture industry has been examined.

The genus Carnobacterium currently consists of nine species, but only two of these, Carnobacterium divergens and C. maltaromaticum (formerly C. piscicola) are frequently encountered in the environment and in foods (Table 1). This review concerns the importance of these two species in dairy, meat and fish products and in the aquatic environment. The taxonomy and methods for isolation and identification of carnobacteria are not described. It is, however, important to note that older studies frequently used carbohydrate fermentation patterns to distinguish between C. divergens and C. maltaromaticum. These methods are now considered less reliable than molecular methods, and results relying on phenotypic criteria must be interpreted with caution.

Natural environment

Among the nine reported species of Carnobacterium, only two species, C. divergens and C. maltaromaticum, are frequently isolated from various sources (Table 1). Four species, C. alterfunditum, C. funditum, C. gallinarum and C. mobile, have been isolated a few times from at most three sources (Table 1). Three species, C. inhibens, C. pleistocenium and C. viridans, have only been isolated from one source, but it should be noted that Carnobacterium spp. related to, for example, C. inhibens have been described. Carnobacterium spp. appear to have both the temperate and polar aquatic environments as habitats including live fish (see also ‘Carnobacteria as pathogenic organisms and/or probiotic cultures’), marine sponges, Antarctic lakes, Arctic and Antarctic sea water as well as the deep sea, aquous alkaline tufa columns from Greenland, and freshwater habitats from the temperate clima zone, including a Sphagnum pond (Leisner et al., unpublished results) and rivers in the northwest region of Spain (Table 1). Although C. maltaromaticum and/or C. divergens have been isolated from tropical fish products, including smoked surubim, a Brazilian tropical freshwater fish, and from vacuum-packed tuna caught in the Indian Ocean and processed in Sri Lanka, it cannot, at least in the latter case, be excluded that this is due to contamination associated with repackaging in Denmark.

The presence of carnobacteria has also been demonstrated in the terrestrial environment, including a field treated with whey, Canadian winter soil, permafrost ice, a compost pile, a collapsed horse manure pile, the larval midgut of a moth species, and other sources (Table 1). It appears that the temperate/polar aquatic and terrestrial environments are both natural habitats.

Carnobacterium divergens and C. maltaromaticum possess traits that may play a role in their survival in these surroundings. One study has reported that a Carnobacterium sp. soil isolate related to C. maltaromaticum survived 48 serial freeze–thaw cycles better than Escherichia coli and an Enterococcus sp. soil isolate, but worse than a few other soil isolates, including an Acinetobacter sp.. Indeed, these organisms may survive freezing for considerable periods of time, as witnessed by the isolation of a Carnobacterium sp. preserved in a permafrost ice wedge for 25 000 years. Additional data on the abilities of carnobacteria to grow at low temperatures and to survive frozen storage is available for food products. Also, a cold-active β-galactosidase from C. maltaromaticum and a cold-adapted alanine dehydrogenase from a Carnobacterium sp. related to C. alterfunditum have been reported. Some carnobacterial isolates originate from natural high-pressure habitats, and additional data on resistance to pressure have been reported for high-pressure-processed foods. It has not been described how other physical/chemical parameters such as salt content, atmosphere and pH affect survival and growth of these organisms in the natural environment.

With respect to energy-yielding substrates, one species, C. maltaromaticum, expresses chitinase activity (Leisner & Ingmer, unpublished data). This may facilitate adherence to and survival on zooplankton as suggested for enterococci, and also explain the isolation of this species from the midgut of the larval stage of a species of moth. Interestingly, the arginine deiminase pathway is expressed by the most frequently encountered species, C. divergens, C. gallinarum, C. maltaromaticum and C. mobile (e.g.,;; ) but not by C. inhibens or C. viridans. Arginine is not a substrate that results in growth of C. alterfunditum and C. funditum, and information is not available for C. pleistocenium. This amino acid may represent an additional energy source for growth and survival when carbohydrates are scarce, and it may offer protection against acid stress, as described for Enterococcus faecalis and related species. Finally, carnobacteria are able to catabolize a range of carbohydrates, although there are considerable interspecies and intraspecies heterogeneities. Examples of sources of such carbohydrates include animals (e.g. chitin and, to some extent, lactose, although the targets of the lactose hydrolytic activity shown by carnobacteria may instead be byproducts of plant sugar polymers and saccharides adsorbed to humic acid substances in the soil), plants (e.g. salicin and sucrose), fungi (e.g. chitin and trehalose), prokaryotes (N-acetylglucosamine), and living organisms in general (ribose). The importance of these abilities for growth and survival in the environment deserves further study. The genome sizes of C. alterfunditum, C. divergens and C. pleistocenium strains and a Carnobacterium sp. AT7 deep sea isolate have been estimated to be 2.9, 3.2, 3.2 and 2.4 Mb, respectively, and for the AT7 isolate, the data are reported in a database described by. These sizes are relatively large in comparison to many other LAB, suggesting that carnobacterial genomes may encode a range of genes that makes them well adapted to deal with environmental challenges.

Even if carnobacteria are well adapted to temperate or polar aqueous environments, this does not always provide improved ability to survive as compared to other bacteria. Thus, the actual abilities of strains of C. divergens and C. maltaromaticum isolated from a Sphagnum pond to survive in water from this source were not improved as compared to related gram-positive bacteria originating from other sources (Leisner et al., unpublished data). At present, therefore, the precise mechanisms by which Carnobacterium spp. persist in the natural environment and their underlying genetics are not known. Finally, it should be noted that the environments from which carnobacteria can be isolated are not always as extreme as they appear at first sight. Thus, Carnobacterium spp. isolated from Lake Vanda, Antarctica were found at a depth of 61 m, where the temperature was c. 15–20°C.

Dairy, fish and meat products

High concentrations of bacteria (>106–107 CFU g−1) in food are typically required before their activity is sufficient to influence the sensory properties of a product. For this to happen, occurrence and growth kinetics are the key parameters, and databases, including ComBase, are available to determine the effect of food storage conditions and product characteristics on growth of specific bacteria. However, information on carnobacteria has not yet been included in such databases.

Carnobacterium maltaromaticum and another Carnobacterium sp. have been isolated from milk (; EF204312), and they, in addition to C. divergens, have been detected in soft cheeses, including mold-ripened brie, mozzarella, Camembert and other types. The high concentration of C. divergens in the curd of mozzarella, exposed to 10–37°C during processing, is in agreement with the maximum growth temperature (40°C) of this species.

The occurrence of Carnobacterium in dairy products (and other foods) is most likely underreported. This is due to the common use of acetate containing media, particularly MRS agar (Oxoid CM361) or Rogosa agar (Oxoid CM0627), for enumeration of LAB. Growth of Carnobacterium is inhibited by acetate, and both MRS and Rogosa agar media significantly underestimate concentrations in food.

Carnobacterium divergens and C. maltaromaticum are present in seafood and are able to grow to high concentrations in different fresh and lightly preserved products. Studies of naturally contaminated products suggest which storage conditions and product characteristics select for carnobacteria as compared to the other bacteria present in seafood. For chilled fresh seafood, we have found no reports where C. divergens and C. maltaromaticum dominated the microbial communities in aerobically stored products, but this has been reported for modified atmosphere-packed (MAP) coalfish, cod, pollack, rainbow trout, salmon, shrimp, swordfish and tuna. After frozen storage (−20 to −30°C for 5–8 weeks), C. divergens and C. maltaromaticum seem to be particularly prominent in chilled MAP fish, as has been reported for cod, garfish, salmon, and tuna. In addition to freezing, these carnobacteria are relatively resistant to high-pressure processing and are found in high concentrations in vacuum-packed and chilled squid mantle and cold-smoked salmon previously treated with 200–400 MPa for 15–20 min. In vacuum-packed cold-smoked or sugar-salted (‘gravad’) seafood with 3–7% NaCl in the water phase and a pH of 5.8–6.5, high concentrations of C. divergens and C. maltaromaticum are particularly common, as reported for halibut, rainbow trout, salmon, surubim, and tuna. High concentrations of C. maltaromaticum are also reported in salted lumpfish roe, and it has been isolated from frozen, smoked mussels. Finally, for cooked seafood, high concentrations of C. maltaromaticum have been detected in MAP shrimp after storage at 2–8°C. Both C. divergens and C. mobile were isolated from cooked and brined MAP shrimps (with NaCl, benzoic acid, citric acid and sorbic acid) after storage at 2–8°C. Clearly, carnobacteria are common in chilled fresh and lightly preserved seafood, but at higher storage temperatures (15–25°C), other species, including Enterococcus spp., more frequently dominate the spoilage microbial community of seafood.

Carnobacterium divergens and C. maltaromaticum are able to grow in meat products at temperatures as low as 2 to −1.5°C, and they are frequently predominant members (up to 50%C. divergens and up to 26%C. maltaromaticum of the gram-positive or LAB isolates obtained) of the microbial community of raw meat (beef, pork, lamb, and poultry). The two species are found irrespective of whether products have been stored aerobically, vacuum packaged, or subjected to modified atmospheres, including gas compositions of CO2/N2 (%) ranging from 10: 90 to 80: 20. One study demonstrated the presence of C. divergens in beef stored in air but not in MAP beef with increased concentrations of O2 (20–40%) in addition to CO2 (40%). The growth of C. funditum is impaired by oxygen, and it will be of interest to study further whether addition of O2 to the gas composition of modified atmospheres consistently inhibits growth of carnobacteria, as has been observed for some other bacteria.

Further studies are needed in order to determine whether differences in the presence of carnobacteria in meat are due to variations in storage conditions or variations in contamination levels at the processing plants. The source of carnobacteria in meat products is most probably the processing plant, as these organisms have not been isolated from the gastrointestinal system or skin of chicken, cattle, pigs or sheep, except for one unpublished study (cow rumen, AY244979). Thus, the source of contamination of broiler carcasses by C. divergens and C. maltaromaticum was shown to be the air in the processing plant and not incoming broiler chickens. In fact, two studies confirmed that C. divergens and C. maltaromaticum present in the raw material were eliminated or reduced in number by cooking of a processed meat product, ham.

Carnobacterium divergens and C. maltaromaticum have, however, been detected in a variety of processed meat products, including the cured pork product bacon, ham, a Danish processed pork product (‘rullepølse’) ( and unpublished results), various Spanish processed meat products, cooked poultry meat, pressure-treated (408–888 MPa) chicken, and irradiated pork and chicken. On a few occasions, C. maltaromaticum has even been isolated from fermented sausages; as noted by, this contrasts with the usual nonaciduric habitats of carnobacteria. Other Carnobacterium spp. isolated from processed meat products include C. gallinarium (irradiated chicken), C. mobile (cooked turkey) and C. viridans (vacuum-packed Bologna sausage). Although these organisms are frequently isolated from processed meat products, it has been suggested that they are rarely present in high numbers, and that terminal spoilage of cooked, cured meats is primarily caused by aciduric LAB.

Finally, a Carnobacterium sp. has also been isolated from egg contents, and it was shown that this isolate had a similar ability to penetrate the eggshell and contaminate the whole egg as various other gram-positive and gram-negative bacteria.

Transmission routes for carnobacteria from the natural environment into food-manufacturing plants and further on to dairy, fish and meat products are not known to any extent. Knowledge on this topic is essential to evaluate if species and intraspecific clusters that differ in spoilage ability (as discussed later) also have different colonization abilities. Such knowledge would also illuminate the feasibility of using the production of metabolites, especially tyramine, by C. divergens and C. maltaromaticum as an index of microbial spoilage of specific fish and meat products.

Bacteriocins and antimicrobial properties

Carnobacteria with the ability to produce antimicrobial peptides, bacteriocins, are commonly encountered in foods (e.g.; ). The characterized carnobacterial bacteriocins belong to class I and class II [e.g. for bacteriocin nomenclature]. So far, only one class I bacteriocin (lantibiotic), UI149, has been reported to be produced by Carnobacterium. In contrast, ten amino acid-sequenced bacteriocins belong to class II, and most of these more specifically to class IIa, which comprises small pediocin-like peptides (Table 2). The inhibition spectrum of carnobacterial class IIa bacteriocins includes Listeria, and antimicrobial activity is exerted by pore formation, dissipation of membrane potential, and leakage of internal low molecular weight substances.

Class IIa bacteriocins are ribosomally synthesized as inactive prepeptides that are modified by posttranslational cleavage of the N-terminal peptide leader at a double-glycine site in order to release mature and active cationic peptides. Carnobacterial class IIa bacteriocins (Table 2) have similar amino acid sequences, with a YGNGV(X)C(X)4C motif (X denotes any amino acid) near the N-terminus of the mature peptide. Two cysteine residues form a disulfide bond in the N-terminal region, and there is an amphipathic α-helix near the C-terminus. The N-terminal region is relatively hydrophilic and conserved, whereas the C-terminus is hydrophobic and diverse. To establish the structure–activity relationships of carnobacterial bacteriocins, the structures of carnobacteriocin B2 and divercin V41 were modified. Thus, amino acid substitutions closer to the N-terminus in carnobacteriocin B2 drastically reduced or eliminated antimicrobial activity, whereas this was not so for substitutions close to the C-terminal part. Divercin V41 contains a second disulfide bond located in the C-terminal region. When the C-terminal region of divercin V41 was separated from the N-terminus by endoproteinase Asp-N, only the C-terminal fragment was active. After trypsin cleavage next to lysine at position 42 or disulfide reduction, the C-terminus lost its inhibitory activity. These results suggested that both hydrophobicity and folding imposed by this second disulfide bond were essential for antilisterial activity of the C-terminal hydrophobic peptide. Chemical oxidation of tryptophan residues by N-bromosuccinimide showed that these residues were crucial for inhibitory activity, as modification of any one of them rendered divercin V41 inactive. The three-dimensional structure of carnobacteriocin B2, its precursor and the corresponding immunity protein have been solved by nuclear magnetic resonance. These are, at present, the only reported carnobacterial protein structures.

Carnobacterial class II bacteriocins that contain a double-glycine-type leader peptide are transported by a dedicated ATP-binding cassette (ABC) transport system. In contrast, divergicin A does not require a secretion protein, as the transport depend on the general cellular secretion (sec) pathway.

The genes involved in carnobacterial bacteriocin production are generally clustered in operons. In the simplest case, corresponding to the sec-dependent divergicin A, the bacteriocin operon is composed of only the structural gene followed downstream by the gene encoding an immunity protein that protects the cell from is own bacteriocin. Production of class IIa bacteriocins requires four genes as a minimum, including genes encoding bacteriocin, immunity protein, ABC of transport protein and its membrane-bound accessory protein. Genes for bacteriocin production may be encoded on the chromosome or on plasmids (Table 2). Carnobacterium maltaromaticum LV17 produces at least three class II bacteriocins. Carnobacteriocins A and B2 are encoded on different but compatible plasmids, pCP49 (72 kb) and pCP40 (61 kb), respectively. The carnobacteriocin BM1 structural gene and its immunity gene are localized on the chromosome. Activation and export of carnobacteriocin BM1 depend on genes located on plasmid pCP40 encoding carnobacteriocin B2. For carnobacteriocins BM1 and B2, a peptide-pheromone dependent quorum-sensing mode caused by the bacteriocin itself or an autoinducer peptide is involved in the regulation of bacteriocin production by two- and three-component signal transduction systems. The components of this regulatory system consist of an induction factor, a histidine protein kinase, and a response regulator. Four carnobacterial bacteriocin operons including genes for immunity proteins and regulatory proteins involved in bacteriocin expression and secretion have been sequenced (Fig. 1).

External parameters also affect bacteriocin production. Thus, increasing concentrations of NaCl (2–7%) reduced production of A9b/B2 bacteriocin, increasing the temperature from below 19 to 25°C inhibited production of piscicolin 126, and reducing the pH from 6.5 to 5.5 inhibited production of carnobacteriocins BM1 and B2. Acetate (A9b bacteriocin) or the presence of a bacteriocin-sensitive strain belonging to the same genus induced bacteriocin production. It is clear that, in order to apply carnobacterial bacteriocins for the biopreservation of foods, detailed knowledge of the factors that influence production of the bacteriocin is necessary. Finally, it should be noted that the bacteriocinogenic activity may be lost, as shown for a C. divergens divercin V41-producing strain that retained only partial activity after being subjected to spray-drying.

Interest in applying carnobacterial bacteriocins in foods and feeds has been directed towards inhibiting Listeria monocytogenes (Table 3) and spoilage microorganisms, to extend the shelf-life of lightly preserved seafood. These attempts have generally, but not always [e.g. regarding prevention of spoilage, and ], met with success, although diversity in sensitivity of the target organism has been observed. However, the occurrence of resistant L. monocytogenes target organisms has led to the suggestion that bacteriocin-negative LAB may be more suitable for practical use as bioprotective agents against L. monocytogenes in ready-to-eat foods. Indeed, L. monocytogenes is inhibited by carnobacterial cultures that do not produce bacteriocins, and this is partly due to glucose depletion. One study also reported a successful application of cultures with no demonstrated bacteriocinogenic activity for extension of the shelf-life of vacuum-packed cold-smoked salmon. This effect was not, however, observed for a C. divergens strain that was unable to produce the class IIa divercin V41.

Resistance of L. monocytogenes to the class IIa divergicin M35 was probably due to modification of the cell wall fatty acid composition. Listeria monocytogenes strains resistant to the class IIa divercin V41 also showed substantial differences in protein expressions as compared with the wild type strain. A σ54-dependent PTS permease of the mannose family (EIItMan), which belongs to the phosphotransferase system (PTS), is responsible for sensitivity of L. monocytogenes to class IIa bacteriocins. These results suggested that EIItMan encoded by the mptACD operon might be a target molecule for class IIa bacteriocins. Recently, two genes coding for a glycerophosphoryl diester phosphodiesterase (GlpQ) and a protein with a putative phosphoesterase function (Pde) were identified as also being involved in the class IIa sensitivity of En. faecalis. Finally, it is important to note that the susceptibility of the target strain is affected by various environmental conditions such as NaCl and pH.

Another cause of concern when using carnobacteria for biopreservation is that C. divergens and C. maltaromaticum both produce tyramine, as discussed further below. Therefore, it has been suggested that a C. divergens strain in which the tyrosine decarboxylase gene is inactivated by mutagenesis could be used as a protective culture to prevent growth of L. monocytogenes in cold-smoked salmon. Currently, no carnobacterial culture, bacteriocin producing or not, is commercially applied for protection against the growth of L. monocytogenes or other bacterial pathogens or spoilage organisms in food.

Effect of catabolic activities on sensory characteristics and safety of foods

As shown in Table 4, the catabolic activities of carnobacteria may result in sensory spoilage of inoculated fish and meat products. Whether this is so for cheese products is not clear. In naturally contaminated products, it seems other members of the bacterial community are typically more important with regard to sensory effects, including spoilage. It is of interest that spoilage was enhanced if moderate-spoilage strains of C. maltaromaticum were inoculated with nonspoilage Vibrio sp. strains or the moderate-spoilage organism Brochothrix thermosphacta into cold-smoked salmon that was subsequently vacuum-packaged. However, this was not so for combinations of C. maltaromaticum and Photobacterium phosphoreum in this product. In addition, a spoilage synergy effect was observed for combinations of B. thermosphacta and C. divergens, C. maltaromaticum or C. mobile in MAP shrimp.

We will first focus on catabolic reactions with carbohydrates and/or organic acids as substrates and with pyruvic acid as an intermediate metabolite. Respiration might occur in the presence of hematin, as shown for C. maltaromaticum, and, indeed, this species consumes substantial proportions of oxygen during exponential growth under aerobic conditions. Carnobacterium spp. are, however, considered to be homofermentative organisms that produce lactic acid from glucose. The presence of the glycolytic pathway in C. divergens has been demonstrated. It can be debated whether carnobacteria should instead be considered facultative or atypical heterofermentative organisms, as C. divergens and C. maltaromaticum are able to utilize ribose and gluconic acid as substrates for growth, and may produce acetic acid, formic acid, and CO2 (e.g.;;; ) as end-products of some secondary decarboxylation/dissimilation reactions of pyruvic acid. Indeed, carnobacteria were initially described as heterofermenters. Acetic acid production by C. divergens and C. maltaromaticum can be substantial during growth in laboratory media under aerobic conditions or in MAP shrimp, and quantitatively it can exceed lactic acid production. Production of acetic acid by C. maltaromaticum is also increased relative to lactic acid if glucose is substituted by ribose. Furthermore, C. maltaromaticum can produce large amounts of ethanol from glucose and ribose during growth in a shrimp extract under anaerobic conditions.

Acetoin can be generated by C. maltaromaticum from pyruvic acid, and this reaction is also found for C. divergens and C. gallinarum but not for C. alterfunditum, C. funditum, C. inhibens and C. viridance, according to reactions in the Voges–Proskauer test. Carnobacterium mobile gives variable reactions, and information is not available for C. pleistocenium. The factors affecting acetoin production are not well known, but production is increased by resting cells of C. maltaromaticum in the presence of hematin. In addition, two out of four strains of C. divergens and C. maltaromaticum isolated from mozzarella cheese were reported to be able to metabolize citric acid, but the potential sensory role of this reaction, e.g. by production of acetoin and diacetyl, was not examined. Production of diacetyl and 2,3-pentanedione by C. maltaromaticum during growth in cold-smoked salmon resulted in a butter-like odor but not in spoilage (Table 4). In conclusion, even, if carbohydrate catabolism by carnobacteria appears to result in a diverse number of metabolites, these have generally a limited effect on the sensory attributes of foods. H2O2 may be produced by C. divergens, and formation of this compound by C. viridans has been associated with spoilage in the form of green discoloration of cured Bologna ham (Table 4).

Whether carnobacteria possess proteolytic activities of potential importance for taste in products such as cheese is not known, and this deserves further investigation. In contrast, metabolites resulting from the degradation of amino acids certainly cause sensory effects in foods (Table 4). Generation of branched alcohols and aldehydes (2-methyl-1-butanal, 2-methyl-1-butanol, 3-methyl-1-butanal, 3-methyl-1-butanol, 2-methylpropanal, and 2-methylpropanol) by transamination, decarboxylation and reduction of the amino acids valine, leucine and isoleucine appears to be particularly important. Production of some of these compounds, such as 3-methyl-1-butanal, is strain or species dependent. Production by a C. maltaromaticum strain of 3-methylbutanal, 3-methylbutanol and 3-methylbutanoic acid from leucine was, in general, increased at pH values of 6.5 or higher and in the presence of increased concentrations of α-ketoisocaproic acid and glucose. This strain affected the odor and reduced the leucine content of a sausage mince, but a clear causal relationship was not demonstrated. Production by C. maltaromaticum of alcohols and aldehydes from valine, leucine and/or isoleucine resulted in a malty, green aroma in skimmed milk and shrimp, and has also caused spoilage of cured ham (Table 4). The association between the presence of these compounds and spoilage is, however, not always straightforward, as production of 3-methyl-1-butanal and/or 3-methyl-1-butanol in shrimp by certain C. maltaromaticum strains did not result in malty off-flavors.

Production of NH4+ from arginine as a result of its catabolism catalyzed by the arginine deaminase pathway may, in theory, cause spoilage of shrimp or squid that contain high levels of free arginine. Carnobacterium maltaromaticum and C. divergens but not C. mobile were able to produce NH4+ in MAP shrimp, but this was not the cause of spoilage of this product.

Production of indole from the amino acid tryptophan is also a potential cause of spoilage, although C. divergens, C. maltaromaticum and C. mobile are all unable to carry out this reaction in standard laboratory media. It has, however, been observed that C. divergens and strains belonging to a major phenotypic cluster of C. maltaromaticum were able to use tryptophan as a substrate during growth in MAP shrimp. Whether this resulted in generation of indole was not examined.

Production of tyramine from tyrosine is the only known metabolic reaction by Carnobacterium spp. that constitutes a cause of concern regarding food safety. Not all carnobacterial species possess this ability, as C. mobile does not produce tyramine during growth in shrimp, and variation exists among different strains and phenotypic clusters of C. divergens and C. maltaromaticum for amounts of tyramine produced. Tyramine production by one C. divergens strain was at its maximum during the stationary growth phase and at a low initial pH in the presence of 0.6% glucose, whereas NaCl (10%) was inhibitory. Regardless of strain variation and the effects of environmental parameters, tyramine production by C. divergens and/or C. maltaromaticum has been reported in a range of foods, including meat (up to 28 mg kg−1), a meat–fat mixture (up to 121 mg kg−1), cold-smoked salmon (up to c. 370 mg kg−1), frozen and thawed salmon (up to 40–60 mg kg−1), and shrimp (up to 20–60 mg kg−1). These levels have no adverse effects on most consumers, but for sensitive individuals, e.g. with reduced monoamine oxidase activity due to medication or hereditary deficiency, very little tyramine can cause migraine headaches, and an intake of no more than 5 mg of tyramine per meal has been recommended. Typical consumption of fish and meat products is 50–150 g per meal. As described above, C. divergens and/or C. maltaromaticum are able to form c. 20–370 mg tyramine kg−1 in these products, corresponding to c. 1–55 mg of tyramine per meal. Consequently, tyramine formation by carnobacteria in specific foods can represent a hazard for sensitive individuals who might suffer migraine headaches. This risk for sensitive individuals can be minimized by restricting their consumption of fish and meat to products that are newly processed, i.e. that are not close to the declared shelf-life expiry day.

Growth of Carnobacterium spp. in food products may result in accumulation of a range of volatile alcohols, ketones, hydrocarbons, and other compounds. The metabolic reactions leading to these products have not been studied in detail for Carnobacterium, in contrast to the situation for other LAB, but may be a result of NAD+-generating reactions or nonenzymatic reactions. Several ketones have characteristic odors, but whether they contribute to spoilage off-flavors as a result of carnobacterial metabolic activity is not well understood. With regard to lipids, C. maltaromaticum has been reported to hydrolyze tributyrin, a triglyceride with butyrate as fatty acid, but it is not known whether this lipase activity contributes to flavor changes of dairy, fish and meat products. Carnobacterium divergens and C. maltaromaticum were not able to limit oxidation of linoleic acid during growth. This indicates that these species may not prevent quality deterioration of meat products by lipid oxidation. Finally, C. maltaromaticum has been shown to cause a softer texture of salmon fillets when inoculated in high numbers.

It is worth noting that interspecies and intraspecies differences exist regarding carnobacterial spoilage capacity. showed that C. mobile and a minor phenotypic cluster of C. maltaromaticum did not spoil MAP shrimp, in contrast to what was seen with C. divergens and the major phenotypic cluster of C. maltaromaticum. It would be of interest to examine whether similar heterogeneities exist for Carnobacterium spp. growing in other dairy, fish and meat products. As environmental parameters readily affect the metabolism of carbohydrates and amino acids, it is not surprising that product-specific and storage-specific conditions also play important roles. The ability of two C. maltaromaticum strains to relatively rapidly spoil meat during growth under aerobic conditions at 7°C but not or only after a long storage period in vacuum packs at 2°C serves as an example (Table 4).

Carnobacteria as pathogenic organisms and/or probiotic cultures

Two human clinical cases caused by opportunistic infection with C. maltaromaticum and a Carnobacterium sp. have been described. Two clinical isolates of C. divergens have also been obtained (accession number AY650920). Carnobacteria are not known members of the human gastrointestinal microbial community, unlike several other LAB. The exceptions are an unpublished study reporting an uncultured Carnobacterium sp. clone from cow rumen (AY244976) and two studies demonstrating the presence of carnobacteria in pig and horse effluent-impacted environments (DQ337521; DQ337531). Nevertheless, it is safe to conclude that the presence of Carnobacterium spp. in food does not present a risk factor for human illness, except for the production of the biogenic amine, tyramine, as discussed previously. Neither do Carnobacterium spp. appear to present a risk for nocosomial infections in hospitals and similar institutions, although they have, in one instance, been isolated from contaminated blood plasma.

The presence of virulence factors in carnobacteria is not well documented. Thus C. maltaromaticum strains isolated from diseased fish lacked hemolytic and phospholipolytic activities. Carnobacterium viridans shows, however, β-hemolytic activity on sheep blood agar. Although several isolates of carnobacteria produce bacteriocins, none of these compounds has been reported to exert a cytolytic activity as shown for the En. faecalis class I-related bacteriocin cytolysin. Regarding chemotherapeutic agents, fish pathogenic strains of C. maltaromaticum were resistant to several of the agents widely used in aquaculture, such as oxytetracycline, quinolones, nitrofurans and potentiated sulfonamides, but sensitive to erythromycin. This species is not resistant to lysozyme from salmonid eggs, which supports the idea that it is not vertically transmitted, at least in this fish species. Finally, it should be noted that two clinical isolates of C. divergens have been reported to possess a gene encoding a new class of penicillinase (AY650920). It will be of interest to further explore the distribution of this enzyme among carnobacterial species as well as its functionality.

It has been documented that some strains of C. maltaromaticum are pathogenic for several fish species, including Australian salmonids, carp, rainbow trout, striped bass and channel catfish, and salmon. Pathologic effects vary, and include, for example, septicemia, peritonitis, exophthalmia, accumulation of ascitic fluid, and hemorrhages. In most (but not all) instances, the virulence appears, however, to be low and only causes problems in fish undergoing severe stress, e.g. due to spawning. It is, therefore, not surprising that C. maltaromaticum and C. maltaromaticum-like strains are also found in the intestine or gills of healthy fish, including Arctic charr, Atlantic cod, Atlantic salmon, brown bullhead, trout, and various freshwater fish. also summarize some of these findings.

The presence of other carnobacterial species in healthy fish has also been reported, including C. divergens [Arctic charr, Atlantic salmon, Atlantic cod and wolffish, trout, and freshwater fish], C. alterfunditum-like [rainbow trout], C. funditum-like [Arctic charr and Atlantic cod], C. gallinarum [Atlantic cod], C. inhibens [Atlantic salmon], C. mobile-like [Arctic charr and Atlantic cod], and Carnobacterium spp. [Arctic charr and carp]. Clearly, further research is necessary to clarify under what circumstances Carnobacterium spp. may be pathogenic for fish and whether the infective capability is species and clone specific.

The reported pathogenicity of C. maltaromaticum has not hindered research into the possibility of using other carnobacteria as probiotic cultures in aquaculture, including Carnobacterium sp., C. alterfunditum, C. divergens, and C. inhibens. Isolates of these species, in addition to C. maltaromaticum, exhibit inhibitory activity towards bacterial fish pathogens. Carnobacterium divergens and C. maltaromaticum enhance the cellular and humoral immune responses and cytokine expression ratios of rainbow trout. Use of carnobacteria as probiotics leads to increased survival of the fish in some instances [larvae of cod fry and Atlantic salmon fry, rainbow trout, and salmon], but not in others [larvae of cod fry, and rainbow trout]. One study showed that in vitro exposure to C. divergens did not reverse the effects of bacterial pathogens, although these were alleviated. Additional research is necessary to validate the usefulness of carnobacteria as probiotic cultures.

Carnobacterium maltaromaticum has also been reported to be pathogenic for the fruit fly, Drosophila melanogaster, upon injection into the thorax. This specific case of pathogenesis is probably best understood as a result of opportunistic infection, although C. maltaromaticum (but not C. divergens, C. gallinarum, C. inhibens, C. mobile or C. viridans) exerts chitinolytic acitivity (Leisner & Ingmer, unpublished data), a feature that can be perceived as targeting the chitin-containing exoskeleton of insects. Indeed, insects may serve as a host for this species.

Genomics

The complete chromosomes of many LAB species have now been sequenced. Currently, 19 complete genome sequences of streptococci and 18 complete genome sequences of the nonpathogenic LAB representing 14 species from the order Lactobacillales are available. However, no genome sequence or physical genetic map is available for Carnobacterium. The LAB have relatively small genomes for nonobligatory bacterial parasites or symbionts, ranging from c. 1.6 to c. 3 Mb. For C. divergens and C. pleistocenium, the genome size was estimated to 3.2 Mb, and for C. alterfunditum pf4T, it was estimated to be 2.9 Mb. At the time of writing (March 2007), there is only one Carnobacterium genome sequencing project. Carnobacterium sp. AT7, a piezophilic strain isolated from the Aleutian trench at a depth of 2500 m, is being sequenced for the Moore Foundation Marine Microbial Genome Sequencing Project with a grant to the J. Craig Venter Institute. The data already available indicate that the Carnobacterium sp. AT7 genome contains 2.4 Mb and encodes 2388 proteins (http://www.genomesonline.org). Carnobacterium sp. AT7 is closely related to C. alterfunditum and C. pleistocenium.

To date, knowledge on the genes and DNA sequences of Carnobacterium is comparatively sparse, concerning mostly bacteriocin-related genes in the species C. divergens and C. maltaromaticum (Table 2) and 16S rRNA and 16S–23S rRNA gene intergenic spacer sequences. Genes involved in some important carnobacterial metabolic traits have been sequenced (Table 5). The genetic information obtained is, for most sequences, derived from just one strain, and may therefore be strain specific, as shown for a number of L. monocytogenes genes.

Clearly, our knowledge of important phenotypes of strains and species of Carnobacterium would benefit from the availability of a complete genome sequence for a strain representative of C. maltaromaticum, which is the species with most importance for the food and aquaculture industries. The most extensive study on phenotypic variation of C. maltaromaticum revealed that the majority of strains studied belonged to one phenotypic cluster (cluster H). Thus, in our opinion, a suitable candidate for a whole genomic sequence could be either C. maltaromaticum LMG 22901 (isolated from pork meat), LMG 22899 (isolated from cod) or LMG 22898 (isolated from salmon), which all belong to this phenotypic cluster. LMG 22901 does not harbor plasmids (Laursen, unpublished), and therefore appears to be a prime candidate for such an endeavor.

Concluding remarks

We have come some way towards understanding important aspects of the presence of carnobacteria in foods and the environment, particularly concerning the genetics of carnobacterial bacteriocins and their application. However, there are important areas where knowledge on these bacteria is limited. These include the following:

Distribution and quantitative microbial ecology: Carnobacterium spp. have not been reported from a number of habitats, such as plants, fermented vegetable foods and the gastrointestinal system of birds and mammals, including humans, that have otherwise been associated with several genera and species of LAB. This may, in some instances, be due to faulty methodology for detecting carnobacteria. Generally, however, our quantitative understanding is limited regarding factors that influence inactivation, survival or growth of carnobacteria in various natural environments. In foods, more detailed information is available, but mathematical models for quantitative prediction of processing, product and storage effects on growth and metabolic activity, including bacteriocin and tyramine formation, awaits further development together with recording of responses in databases. In addition, further studies are needed to elucidate mechanisms underlying the relationship between environmental parameters and kinetic responses of carnobacteria.

Routes of food contamination: To reduce the negative effects of carnobacteria in foods (spoilage metabolites and tyramine), further information on routes of contamination is desirable. In fact, very little research has been performed so far concerning this aspect of carnobacteria in food.

Metabolic activity: It is known that carnobacteria, or at least C. maltaromaticum and C. divergens, have the capacity to produce a wide range of metabolites in chilled food. Further studies on the importance of these metabolites with respect to positive and negative sensory attributes of various foods are, however, needed.

Diversity: We are beginning to appreciate how interspecies and intraspecies variation determine the positive and negative effects of the presence of carnobacteria in food and the environment, but we still do not understand how such variation affects, for instance, their survival in food-processing plants and contamination of foods. The significance of such variation for their potential as fish pathogens also needs to be substantiated. This is also the case for their role as spoilage organisms in meat and fish products, with the exception of a few products such as vacuum-packed smoked salmon and cooked MAP shrimps.

Genomics: Representative genome sequences would offer a very valuable road map in order to answer many of the outstanding questions associated with this important genus.

Statement

Reuse of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

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    González-Rodríguez M-N, Sanz J-J, Santos J-Á, Otero A, García-López M-L. Numbers and types of microorganisms in vacuum-packed cold-smoked freshwater fish at the retail level. Int J Food Microbiol. 2002;77:161-168.

    Not in our library10.1016/s0168-1605(02)00048-x

  67. 67.

    Gram L, Ringø E, Holzapfel WH, Naughton PJ. Prospects of fish probiotics. Microbial Ecology in Growing Animals. 2005;379-417.

    Not in our library

  68. 68.

    Grant IR, Patterson MF. A numerical taxonomic study of lactic acid bacteria isolated from irradiated pork and chicken packaged under various gas atmospheres. J Appl Bacteriol. 1991;70:302-307.

    Not in our library10.1111/j.1365-2672.1991.tb02940.x

  69. 69.

    Gravesen A, Ramnath M, Rechinger KB, Andersen N, Jänsch L, Héchard Y, Hastings JW, Knøchel S. High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiol. 2002;148:2361-2369.

    Not in our library10.1099/00221287-148-8-2361

  70. 70.

    Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H, Antranikian G. Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic sea ice, Spitzbergen. Extremophiles. 2004;8:475-488.

    Not in our library10.1007/s00792-004-0409-0

  71. 71.

    Guldager HS, Bøknæs N, Østerberg C, Nielsen J, Dalgaard P. Thawed cod fillets spoil less rapidly than unfrozen fillets when stored under modified atmosphere at 2°C. J Food Prot. 1998;61:1129-1136.

    Not in our library10.4315/0362-028x-61.9.1129

  72. 72.

    Gursky LJ, Martin NI, Derksen DJ, van Belkum MJ, Kaur K, Vederas JC, Stiles ME, McMullen LM. Production of piscicolin 126 by Carnobacterium maltaromaticum UAL26 is controlled by temperature and induction peptide concentration. Arch Microbiol. 2006;186:317-325.

    Not in our library10.1007/s00203-006-0147-z

  73. 73.

    Hagi T, Tanaka D, Iwamura Y, Hoshino T. Diversity and seasonal changes in lactic acid bacteria in the intestinal tract of cultured freshwater fish. Aquaculture. 2004;234:335-346.

    Not in our library

  74. 74.

    Hammes WP, Hertel C, Dworkin M. The genera Lactobacillus and Carnobacterium. The Procaryotes: An Evolving Electronic Resource for the Microbiological Community. 2003;320-403.

    Not in our library

  75. 75.

    Herbin S, Mathieu F, Brulé F, Branlant C, Lefebvre G, Lebrihi A. Characteristics and genetic determinants of bacteriocin activities produced by Carnobacterium piscicola CP5 isolated from cheese. Curr Microbiol. 1997;35:319-326.

    Not in our library10.1007/s002849900262

  76. 76.

    Himelbloom B, Nilsson L, Gram L. Factors affecting production of an antilisterial bacteriocin by Carnobacterium piscicola strain A9b in laboratory media and model fish systems. J Appl Microbiol. 2001;91:506-513.

    Not in our library10.1046/j.1365-2672.2001.01401.x

  77. 77.

    Hirano T, Yamaguchi M, Shirai T, Suzuki T, Suyama M. Free amino acids, trimethylamine oxide, and betaines of the raw and boiled meats of mantis shrimp Oratosquilla oratolia. Nippon Suisan Gakkaishi. 1992;58:973.

    Not in our library

  78. 78.

    Hiu SF, Holt RA, Sriranganathan N, Seidler RJ, Fryer JL. Lactobacillus piscicola, a new species from salmonid fish. Int J System Bacteriol. 1984;34:393-400.

    Not in our library

  79. 79.

    Holck AL, Axelsson L, Schillinger U. Purification and cloning of piscicolin-61, a bacteriocin from Carnobacterium piscicola LV61. Curr Microbiol. 1994;29:63-68.

    Not in our library10.1007/bf01575750

  80. 80.

    Holck A, Axelsson L, Schillinger U. Divergicin 750, a novel bacteriocin produced by Carnobacterium divergens 750. FEMS Microbiol Lett. 1996;136:163-168.

    Not in our library10.1111/j.1574-6968.1996.tb08043.x

  81. 81.

    Holley RA, Guan TY, Peirson M, Yost CK. Carnobacterium viridans sp. nov., an alkaliphilic, facultative anaerobe isolated from refrigerated, vacuum-packed bologna sausage. Int J System Evol Microbiol. 2002;52:1881-1885.

    Not in our library10.1099/00207713-52-5-1881

  82. 82.

    Humphrey JD, Lancaster CE, Gudkovs N, Copland JW. The disease status of Australian salmonids: bacteria and bacterial diseases. J Fish Dis. 1987;10:403-410.

    Not in our library

  83. 83.

    Irianto A, Austin B. Probiotics in aquaculture. J Fish Dis. 2002;25:633-642.

    Not in our library

  84. 84.

    Jack RW, Wan J, Gordon J, Harmark K, Davidson BE, Hillier AJ, Wettenhall REH, Hickey MW, Coventry MJ. Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl Environ Microbiol. 1996;62:2897-2903.

    Not in our library10.1128/aem.62.8.2897-2903.1996

  85. 85.

    Jensen RL, Pedersen KS, Loeschcke V, Ingmer H, Leisner JJ. Limitations in the use of Drosophila melanogaster as a model host for Gram positive bacterial infection. Lett Appl Microbiol. 2007;44:218-223.

    Not in our library10.1111/j.1472-765x.2006.02040.x

  86. 86.

    Jeppesen VF, Huss HH. Characteristics and antagonistic activity of lactic acid bacteri isolated from chilled fish products. Int J Food Microbiol. 1993;18:305-320.

    Not in our library10.1016/0168-1605(93)90153-8

  87. 87.

    Jöborn A, Olsson JC, Westerdahl A, Conway PL, Kjelleberg S. Colonization in the fish intestinal tract and production of inhibitory substances in intestinal mucus and faecal extracts by Carnobacterium sp. strain K1. J Fish Dis. 1997;20:383-392.

    Not in our library

  88. 88.

    Jöborn A, Dorsch M, Olsson JC, Westerdahl A, Kjelleberg S. Carnobacterium inhibens sp. nov., isolated from the intestine of Atlantic salmon (Salmo salar). Int J System Bacteriol. 1999;49:1891-1898.

    Not in our library10.1099/00207713-49-4-1891

  89. 89.

    Joffraud JJ, Leroi F, Roy C, Berdagué JL. Characterisation of volatile compounds produced by bacteria isolated from the spoilage flora of cold-smoked salmon. Int J Food Microbiol. 2001;66:175-184.

    Not in our library10.1016/s0168-1605(00)00532-8

  90. 90.

    Joffraud J-J, Cardinal M, Cornet J, Chasles J-S, Léon S, Gigout F, Leroi F. Effect of bacterial interactions on the spoilage of cold-smoked salmon. Int J Food Microbiol. 2006;112:51-61.

    Not in our library10.1016/j.ijfoodmicro.2006.05.014

  91. 91.

    Jones RJ. Observations on the succession dynamics of lactic acid bacteria populations in chill-stored vacuum-packaged beef. Int J Food Microbiol. 2004;90:273-282.

    Not in our library10.1016/s0168-1605(03)00310-6

  92. 92.

    Jørgensen LV, Huss HH, Dalgaard P. The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol. 2000;89:920-934.

    Not in our library10.1046/j.1365-2672.2000.01196.x

  93. 93.

    Kabadjova P, Dousset X, Le Cam V, Prevost H. Differentiation of closely related Carnobacterium food isolates based on 16S–23S ribosomal DNA intergenic spacer region polymorphism. Appl Environ Microbiol. 2002;68:5358-5366.

    Not in our library10.1128/aem.68.11.5358-5366.2002

  94. 94.

    Katayama T, Tanaka M, Moriizumi J, Nakamura T, Brouchkov A, Douglas TA, Fukuda M, Tomita F, Asano K. Phylogenetic analysis of bacteria preserved in a permafrost ice wedge for 25 000 years. Appl Environ Microbiol. 2007;73:2360-2363.

    Not in our library10.1128/aem.01715-06

  95. 95.

    Kim D-H, Austin B. Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics. Vet Immun Immunopath. 2006a;114:297-304.

    Not in our library10.1016/j.vetimm.2006.08.015

  96. 96.

    Kim D-H, Austin B. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol. 2006b;21:513-524.

    Not in our library10.1016/j.fsi.2006.02.007

  97. 97.

    Kleerebezem M, Kuipers OP, de Vos WM, Stiles ME, Quadri LEN. A two-component signal-transduction cascade in Carnobacterium piscicola LV17B: two signaling peptides and one sensor-transmitter. Peptides. 2001;22:1597-1601.

    Not in our library10.1016/s0196-9781(01)00494-6

  98. 98.

    Lai S, Manchester LN. Numerical phenetic study of the genus Carnobacterium. Anton Leeuw. 2000;78:73-85.

    Not in our library10.1023/a:1002723609675

  99. 99.

    Lakshmanan R, Dalgaard P. Effects of high-pressure processing on Listeria monocytogenes, spoilage microflora and multiple compound quality indices in chilled cold-smoked salmon. J Appl Microbiol. 2004;96:398-408.

    Not in our library10.1046/j.1365-2672.2004.02164.x

  100. 100.

    Larrouture C, Ardaillon V, Pépin M, Montel MC. Ability of meat starter cultures to catabolize leucine and evaluation of the degradation products by using an HPLC method. Food Microbiol. 2000;17:563-570.

    Not in our library

  101. 101.

    Larrouture-Thiveyrat C, Montel M-C. Effects of environmental factors on leucine catabolism by Carnobacterium piscicola. Int J Food Microbiol. 2003;81:177-184.

    Not in our library10.1016/s0168-1605(02)00227-1

  102. 102.

    Larrouture-Thiveyrat C, Pepin M, Leroy-Sétrin S, Montel M-C. Effect of Carnobacterium piscicola on aroma formation in sausage mince. Meat Sci. 2003;63:423-426.

    Not in our library10.1016/s0309-1740(02)00083-9

  103. 103.

    Lauro FM, Chastain RA, Blankenship LE, Yayanos AA, Bartlett DH. The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl Environ Microbiol. 2007;73:838-845.

    Not in our library10.1128/aem.01726-06

  104. 104.

    Laursen BG, Bay L, Cleenwerck I, Vancanneyt M, Swings J, Dalgaard P, Leisner JJ. Carnobacterium divergens and Carnobacterium maltaromaticum as spoilers or protective cultures in meat and seafood: phenotypic and genotypic characterization. Syst Appl Microbiol. 2005;28:151-164.

    Not in our library10.1016/j.syapm.2004.12.001

  105. 105.

    Laursen BG, Leisner JJ, Dalgaard P. Carnobacterium species: effect of metabolic activity and interaction with Brochothrixthermosphacta on sensory characteristics of modified atmosphere packed shrimp. J Agric Food Chem. 2006;54:3604-3611.

    Not in our library10.1021/jf053017f

  106. 106.

    Leblanc EL, Stiles ME, McMullen LM, Leisner JJ, Luten JB, Børresen T, Oehlenschläger J. Characterization of the prevailing flora of Carnobacterium ssp. growing on CO2 modified atmosphere packaged rainbow trout (Oncorhynchus mykiss) fillets. Seafood from Producer to Consumer. Integrated Approach to Quality. 1997;445-454.

    Not in our library

  107. 107.

    Lebois M, Connil N, Onno B, Prévost H, Dousset X. Effects of divercin V41 combined to NaCl content, phenol (liquid smoke) concentration and pH on Listeria monocytogenes Scott A growth in BHI broth by an experimental design approach. J Appl Microbiol. 2004;96:931-937.

    Not in our library10.1111/j.1365-2672.2004.02221.x

  108. 108.

    Leisner J. Characterisation of lactic acid bacteria isolated from lightly preserved fish products and their ability to metabolise various carbohydrates and amino acids. 1992.

    Not in our library

  109. 109.

    Leisner JJ, Millan JC, Huss HH, Larsen LM. Production of histamine and tyramine by lactic acid bacteria isolated from vacuum-packed sugar-salted fish. J Appl Bacteriol. 1994a;76:417-423.

    Not in our library10.1111/j.1365-2672.1994.tb01097.x

  110. 110.

    Leisner JJ, Tidemand J, Larsen LM. Catabolism of arginine by Carnobacterium spp. isolated from vacuum-packed sugar-salted fish. Curr Microbiol. 1994b;29:95-99.

    Not in our library

  111. 111.

    Leisner JJ, Greer GG, Dilts BD, Stiles ME. Effect of growth of selected lactic acid bacteria on storage life of beef stored under vacuum and in air. Int J Food Microbiol. 1995;26:231-243.

    Not in our library10.1016/0168-1605(94)00133-q

  112. 112.

    Leroi F, Arbey N, Joffraud J-J, Chevalier F. Effect of inoculation with lactic acid bacteria on extending the shelf-life of vacuum-packed cold smoked salmon. Int J Food Sci Technol. 1996;31:497-504.

    Not in our library

  113. 113.

    Leroi F, Joffraud J-J, Chevalier F, Cardinal M. Study of the microbial ecology of cold-smoked salmon during storage at 8°C. Int J Food Microbiol. 1998;39:111-121.

    Not in our library10.1016/s0168-1605(97)00126-8

  114. 114.

    Lewus CB, Kaiser A, Montville TJ. Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl Environ Microbiol. 1991;57:1683-1688.

    Not in our library10.1128/aem.57.6.1683-1688.1991

  115. 115.

    Li Z-Y, Liu Y. Marine sponge Craniella austrialiensis-associated bacterial diversity revelation based on 16S rDNA library and biologically active Actinomycetes screening, phylogenetic analysis. Lett Appl Microbiol. 2006;43:410-416.

    Not in our library10.1111/j.1472-765x.2006.01976.x

  116. 116.

    Liolios K, Tavernarakis N, Hugenholtz P, Kyrpides N. The genomes on line database (GOLD) v.2: a monitor of genome projects worldwide. Nucl Acids Res. 2006;34:D332-D334.

    Not in our library10.1093/nar/gkj145

  117. 117.

    Lyhs U, Björkroth J, Hyytiä E, Korkeala H. The spoilage flora of vacuum-packaged, sodium nitrite or potassium nitrate treated, cold-smoked rainbow trout stored at 4°C or 8°C. Int J Food Microbiol. 1998;45:135-142.

    Not in our library10.1016/s0168-1605(98)00160-3

  118. 118.

    Lyhs U, Korkeala H, Björkroth J. Identification of lactic acid bacteria from spoiled, vacuum-packaged ‘gravad’ rainbow trout using ribotyping. Int J Food Microbiol. 2002;72:147-153.

    Not in our library10.1016/s0168-1605(01)00634-1

  119. 119.

    Makarova KS, Koonin EV. Evolutionary genomics of lactic acid bacteria. J Bacteriol. 2007;189:1199-1208.

    Not in our library10.1128/jb.01351-06

  120. 120.

    Marquis RE, Bender GR, Murray DR, Wong A. Arginine deiminase system and bacterial adaptation to acid environments. Appl Environ Microbiol. 1987;53:198-200.

    Not in our library10.1128/aem.53.1.198-200.1987

  121. 121.

    Masson F, Talon R, Montel MC. Histamine and tyramine production by bacteria from meat products. Int J Food Microbiol. 1996;32:199-207.

    Not in our library10.1016/0168-1605(96)01104-x

  122. 122.

    Masson F, Lebert A, Talon R, Montel MC. Effects of physico-chemical factors influencing tyramine production by Carnobacterium divergens. J Appl Microbiol. 1997;83:36-42.

    Not in our library10.1046/j.1365-2672.1997.00163.x

  123. 123.

    Masson F, Johansson G, Montel MC. Tyramine production by a strain of Carnobacterium divergens inoculated in meat – fat mixture. Meat Sci. 1999;52:65-69.

    Not in our library10.1016/s0309-1740(98)00149-1

  124. 124.

    Mauguin S, Novel G. Characterization of lactic acid bacteria isolated from seafood. J Appl Bacteriol. 1994;76:616-625.

    Not in our library

  125. 125.

    McCabe BJ. Dietary tyramine and other pressor amines in MAOI regimes: a review. J Am Diet Assoc. 1986;86:1059-1064.

    Not in our library

  126. 126.

    McMeekin TA, Baranyi J, Bowman J, Dalgaard P, Kirk M, Ross T, Schmid S, Zwietering MH. Information systems in food safety management. Int J Food Microbiol. 2006;112:181-194.

    Not in our library10.1016/j.ijfoodmicro.2006.04.048

  127. 127.

    McMullen LM, Stiles ME. Microbial ecology of fresh pork stored under modified atmosphere at −1°C, 4.4°C and 10°C. Int J Food Microbiol. 1993;18:1-14.

    Not in our library10.1016/0168-1605(93)90002-x

  128. 128.

    Meisel J, Wolf G, Hammes WP. Heme-dependent cytochrome formation in Lactobacillus maltaromicus. Syst Appl Microbiol. 1994;17:20-23.

    Not in our library

  129. 129.

    Mejlholm O, Bøknæs N, Dalgaard P. Shelf life and safety aspects of chilled cooked and peeled shrimps (Pandalus borealis) in modified atmosphere packaging. J Appl Microbiol. 2005;99:66-76.

    Not in our library10.1111/j.1365-2672.2005.02582.x

  130. 130.

    Métivier A, Pilet M-F, Dousset X, Sorokine O, Anglade P, Zagorec M, Piard J-C, Marion D, Cenatiempo Y, Fremaux C. Divercin V41, a new bacteriocin with two disulphide bonds produced by Carnobacterium divergens V41: primary structure and genomic organization. Microbiology. 1998;144:2837-2844.

    Not in our library10.1099/00221287-144-10-2837

  131. 131.

    Michel C, Faivre B, Kerouault B. Biochemical identification of Lactobacillus piscicola strains from France and Belgium. Dis Aquat Org. 1986;2:27-30.

    Not in our library

  132. 132.

    Michel C, Pelletier C, Boussaha M, Douet D-G, Lautraite A, Tailliez P. Diversity of lactic acid bacteria associated with fish and the fish farm environment, established by amplified rDNA gene restriction analysis. Appl Environ Microbiol. 2007;73:2947-2955.

    Not in our library10.1128/aem.01852-06

  133. 133.

    Miller A, Morgan ME, Libbey LM. Lactobacillus maltaromicus, a new species producing a malty aroma. Int J System Bacteriol. 1974;24:346-354.

    Not in our library

  134. 134.

    Millière JB, Lefebvre G. Carnobacterium piscicola, a common species of French soft cheeses from cow's raw milk. Neth Milk Dairy J. 1994;48:19-30.

    Not in our library

  135. 135.

    Millière JB, Michel M, Mathieu F, Lefebvre G. Presence of Carnobacterium spp. in French surface mould-ripened soft-cheese. J Appl Bacteriol. 1994;76:264-269.

    Not in our library

  136. 136.

    Mora D, Scarpellini M, Franzetti L, Colombo S, Galli A. Reclassification of Lactobacillus maltaromicus (Miller et al., 1974) DSM 20342T and DSM 20344 and Carnobacterium piscicola (Collins et al., 1987) DSM 20730T and DSM 20722 as Carnobacterium maltaromaticum comb. nov. Int J System Evol Microbiol. 2003;53:675-678.

    Not in our library10.1099/ijs.0.02405-0

  137. 137.

    Morea M, Baruzzi F, Cocconcelli PS. Molecular and physiological characterization of dominant bacterial populations in traditional Mozzarella cheese processing. J Appl Microbiol. 1999;87:574-582.

    Not in our library10.1046/j.1365-2672.1999.00855.x

  138. 138.

    Morzel M, Fitzgerald GF, Arendt EK. Fermentation of salmon fillets with a variety of lactic acid bacteria. Food Res Int. 1997;30:777-785.

    Not in our library

  139. 139.

    Naghmouchi K, Drider D, Kheadr E, Lacroix C, Prévost H, Fliss I. Multiple characterizations of Listeria monocytogenes sensitive and insensitive variants to divergicin M35, a new pediocin-like bacteriocin. J Appl Microbiol. 2006;100:29-39.

    Not in our library10.1111/j.1365-2672.2005.02771.x

  140. 140.

    Naser S, Thompson FL, Hoste B, Gevers D, Vandemeulebroecke K, Cleenwerck I, Thompson CC, Vancanneyt M, Swings J. Phylogeny and identification of enterococci by atpA gene sequence analysis. J Clin Microbiol. 2005;43:2224-2230.

    Not in our library10.1128/jcm.43.5.2224-2230.2005

  141. 141.

    Naser SM, Vancanneyt M, Hoste B, Snauwaert C, Swings J. Lactobacillus cypricasei Lawson et al. 2001 is a later heterotypic synonym of Lactobacillus acidipiscis Tanasupawat et al. 2000. Int J System Evol Microbiol. 2006;56:1681-1683.

    Not in our library10.1099/ijs.0.64229-0

  142. 142.

    Nelson KE, Fouts DE, Mongodin EF, et al. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 2004;32:2386-2395.

    Not in our library10.1093/nar/gkh562

  143. 143.

    Newberry CJ, Webster G, Cragg BA, Parkes RJ, Weightman AJ, Fry JC. Diversity of prokaryotes and methanogenesis in deep subsurface sediments from the Nankai Trough, Ocean Drilling Program Leg 190. Environ Microbiol. 2004;6:274-287.

    Not in our library10.1111/j.1462-2920.2004.00568.x

  144. 144.

    Nilsson L, Gram L, Huss HH. Growth control of Listeria monocytogenes on cold-smoked salmon using a competitive lactic acid bacteria flora. J Food Prot. 1999;62:336-342.

    Not in our library10.4315/0362-028x-62.4.336

  145. 145.

    Nilsson L, Nielsen MK, Ng Y, Gram L. Role of acetate in production of an autoinducible class IIa bacteriocin in Carnobacterium piscicola A9b. Appl Environ Microbiol. 2002;68:2251-2260.

    Not in our library10.1128/aem.68.5.2251-2260.2002

  146. 146.

    Nilsson L, Ng YY, Christiansen JN, Jørgensen BL, Grótinum D, Gram L. The contribution of bacteriocin to inhibition of Listeria monocytogenes by Carnobacterium piscicola strains in cold-smoked salmon systems. J Appl Microbiol. 2004;96:133-143.

    Not in our library10.1046/j.1365-2672.2003.02129.x

  147. 147.

    Nilsson L, Hansen TB, Garrido P, Buchrieser C, Glaser P, Knøchel S, Gram L, Gravesen A. Growth inhibition of Listeria monocytogenes by a nonbacteriocinogenic Carnobacterium piscicola. J Appl Microbiol. 2005;98:172-183.

    Not in our library10.1111/j.1365-2672.2004.02438.x

  148. 148.

    Ntougias S, Zervakis GI, Kavroulakis N, Ehaliotis C, Kapadopoulou KK. Bacterial diversity in spent mushroom compost assessed by amplified rDNA restriction analysis and sequencing of cultivated isolates. Syst Appl Microbiol. 2004;27:746-754.

    Not in our library10.1078/0723202042369857

  149. 149.

    O'Brien JK, Marshall RT. Microbiological quality of raw ground chicken processed at high isostatic pressure. J Food Prot. 1996;59:146-150.

    Not in our library10.4315/0362-028x-59.2.146

  150. 150.

    Paarup T, Sanchez JA, Peláez C, Moral A. Sensory, chemical and bacteriological changes in vacuum-packed pressurised squid mantle (Todaropsis eblanae) stored at 4°C. Int J Food Microbiol. 2002;74:1-12.

    Not in our library10.1016/s0168-1605(01)00701-2

  151. 151.

    Paludan-Müller C, Dalgaard P, Huss HH, Gram L. Evaluation of the role of Carnobacterium piscicola in spoilage of vacuum- and modified-atmosphere-packed cold-smoked salmon stored at 5°C. Int J Food Microbiol. 1998;39:155-166.

    Not in our library10.1016/s0168-1605(97)00133-5

  152. 152.

    Papon M, Talon R. Factors affecting growth and lipase production by meat lactobacilli strains and Brochothrix thermosphacta. J Appl Bacteriol. 1988;64:107-115.

    Not in our library10.1111/j.1365-2672.1988.tb02729.x

  153. 153.

    Peirson MD, Guan TY, Holley RA. Aerococci and carnobacteria cause discoloration in cooked cured bologna. Food Microbiol. 2003;20:149-158.

    Not in our library

  154. 154.

    Pikuta EV, Marsic D, Bej A, Tang J, Krader P, Hoover RB. Carnobacterium pleistocenium sp. nov., a novel psychrotolerant, facultative anerobe isolated from permafrost of the Fox tunnel in Alaska. Int J System Evol Microbiol. 2005;55:473-478.

    Not in our library10.1099/ijs.0.63384-0

  155. 155.

    Pilet M-F, Dousset X, Barré R, Novel G, Desmazeaud M, Piard J-C. Evidence for two bacteriocins produced by Carnobacterium piscicola and Carnobacterium divergens isolated from fish and active against Listeria monocytogenes. J Food Prot. 1995;58:256-262.

    Not in our library10.4315/0362-028x-58.3.256

  156. 156.

    Pond MJ, Stone DM, Alderman DJ. Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Aquaculture. 2006;261:194-203.

    Not in our library

  157. 157.

    Quadri LEN, Sailer M, Roy KL, Vederas JC, Stiles ME. Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J Biol Chem. 1994;269:12204-12211.

    Not in our library

  158. 158.

    Quadri LEN, Sailer M, Terebiznik MR, Roy KL, Vederas JC, Stiles ME. Characterization of the protein conferring immunity to the antimicrobial peptide carnobacteriocin B2 and expression of carnobacteriocins B2 and BM1. J Bacteriol. 1995;177:1144-1151.

    Not in our library10.1128/jb.177.5.1144-1151.1995

  159. 159.

    Quadri LEN, Yan LZ, Stiles ME, Vederas JC. Effect of amino acid substitutions on the activity of carnobacteriocin B2. J Biol Chem. 1997a;272:3384-3388.

    Not in our library10.1074/jbc.272.6.3384

  160. 160.

    Quadri LEN, Kleerebezem M, Kuipers OP, de Vos WM, Roy KL, Vederas JC, Stiles ME. Characterization of a locus from Carnobacterium piscicola LV17B involved in bacteriocin production and immunity: evidence for global inducer-mediated transcriptional regulation. J Bacteriol. 1997b;179:6163-6171.

    Not in our library10.1128/jb.179.19.6163-6171.1997

  161. 161.

    Rachman C, Kabadjova P, Valcheva R, Prévost H, Dousset X. Identification of Carnobacterium species by restriction fragment length polymorphism of the 16S–23S rRNA gene intergenic spacer region and species-specific PCR. Appl Environ Microbiol. 2004;70:4468-4477.

    Not in our library10.1128/aem.70.8.4468-4477.2004

  162. 162.

    Richard C, Brillet A, Pilet MF, Prévost H, Drider D. Evidence on inhibition of Listeria monocytogenes by divercin V41 action. Lett Appl Microbiol. 2003;36:288-292.

    Not in our library10.1046/j.1472-765x.2003.01310.x

  163. 163.

    Ringø E, Olsen RE. The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). J Appl Microbiol. 1999;86:22-28.

    Not in our library10.1046/j.1365-2672.1999.00631.x

  164. 164.

    Ringø E, Holzapfel W. Identification and characterization of carnobacteria associated with the gills of Atlantic salmon (Salmo salar L.). Syst Appl Microbiol. 2000;23:523-527.

    Not in our library10.1016/s0723-2020(00)80026-0

  165. 165.

    Ringø E, Bendiksen HR, Grausen SJ, Sundsfjord A, Olsen RE. The effect of dietary fatty acids on lactic acid bacteria associated with the epithelial mucosa and from faecalia of Arctic charr, Salvelinus alpinus (L.). J Appl Microbiol. 1998;85:855-864.

    Not in our library10.1046/j.1365-2672.1998.00595.x

  166. 166.

    Ringø E, Bendiksen HR, Wesmajervi MS, Olsen RE, Jansen PA, Mikkelsen H. Lactic acid bacteria associated with the digestive tract of Atlantic salmon (Salmo salar L.). J Appl Microbiol. 2000;89:317-322.

    Not in our library10.1046/j.1365-2672.2000.01116.x

  167. 167.

    Ringø E, Wesmajervi MS, Bendiksen HR, Berg A, Olsen RE, Johnsen T, Mikkelsen H, Seppola M, Strøm E, Holzapfel W. Identification and characterization of carnobacteria isolated from fish intestine. Syst Appl Microbiol. 2001;24:183-191.

    Not in our library10.1078/0723-2020-00020

  168. 168.

    Ringø E, Seppola M, Berg A, Olsen RE, Schillinger U, Holzapfel W. Characterization of Carnobacterium divergens strain 6251 isolated from intestine of Arctic charr (Salvelinus alpinus L.). Syst Appl Microbiol. 2002a;25:120-129.

    Not in our library10.1078/0723-2020-00080

  169. 169.

    Ringø E, Lødemel JB, Mykleburst R, Jensen L, Lund V, Mayhew TM, Olsen RE. The effect of soybean, linseed and marine oils on aerobic gut microflora of Arctic charr (Salvelinus alpinus L.) before and after challenge with Aeromonas salmonicida spp. salmonicida. Aquaculture Res. 2002b;33:591-606.

    Not in our library

  170. 170.

    Ringø E, Schillinger U, Holzapfel WH, Holzapfel WH, Naughton PJ. Antimicrobial activity of lactic acid bacteria isolated from aquatic animals and the use of lactic acid bacteria in aquaculture. Microbial Ecology in Growing Animals. 2005;418-453.

    Not in our library

  171. 171.

    Ringø E, Sperstad S, Mykleburst R, Refstie S, Krogdahl Å. Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.). The effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture. 2006;261:829-841.

    Not in our library

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    Ringø E, Salinas I, Olsen RE, Nyhaug A, Mykleburst R, Mayhew TM. Histological changes in intestine of Atlantic salmon (Salmo salar L.) following in vitro exposure to pathogenic and probiotic bacterial strains. Cell Tissue Res. 2007;328:109-116.

    Not in our library10.1007/s00441-006-0323-0

  173. 173.

    Robertson PAW, O'Dowd C, Burrels C, Williams P, Austin B. Use of Carnobacterium sp. as a probiotic for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture. 2000;185:235-243.

    Not in our library

  174. 174.

    Rohde BH, Quadri LEN. Functional characterization of a three-component regulatory system involved in quorum sensing-based regulation of peptide antibiotic production in Carnobacterium maltaromaticum. BMC Microbiol. 2006;6:93.

    Not in our library10.1186/1471-2180-6-93

  175. 175.

    Roller S, Sagoo S, Board R, O'Mahony T, Caplice E, Fitzgerald G, Fogden M, Owen M, Fletcher H. Novel combinations of chitosan, carnocin and sulphite for the preservation of chilled pork sausages. Meat Sci. 2002;62:165-177.

    Not in our library10.1016/s0309-1740(01)00243-1

  176. 176.

    Rudi K, Maugesten T, Hannevik SE, Nissen H. Explorative multivariate analyses of 16S rDNA gene data from microbial communities in modified-atmosphere-packed salmon and coalfish. Appl Environ Microbiol. 2004;70:5010-5018.

    Not in our library10.1128/aem.70.8.5010-5018.2004

  177. 177.

    Sakala RM, Hayashidani H, Kato Y, Hirata T, Makino Y, Fukushima A, Yamada T, Kaneuchi C, Ogawa M. Change in the composition of the microflora on vacuum-packaged beef during chiller storage. Int J Food Microbiol. 2002;74:87-99.

    Not in our library10.1016/s0168-1605(01)00732-2

  178. 178.

    Samelis J, Blackburn C de W. Managing microbial spoilage in the meat industry. Food Spoilage Microorganisms. 2006;213-286.

    Not in our library

  179. 179.

    Samelis J, Kakouri A, Georgiadou KG, Metaxopoulos J. Evaluation of the extent and type of bacterial contamination at different stages of processing of cooked ham. J Appl Microbiol. 1998;84:649-660.

    Not in our library10.1046/j.1365-2672.1998.00392.x

  180. 180.

    Samelis J, Kakouri A, Rementzis J. The spoilage microflora of cured, cooked turkey breasts prepared commercially with or without smoking. Int J Food Microbiol. 2000;56:133-143.

    Not in our library10.1016/s0168-1605(99)00190-7

  181. 181.

    Saucier L, Poon A, Stiles ME. Induction of bacteriocin in Carnobacterium piscicola LV17. J Appl Bacteriol. 1995;78:684-690.

    Not in our library

  182. 182.

    Schillinger U, Lücke F-K. Identification of lactobacilli from meat and meat products. Food Microbiol. 1987;4:199-208.

    Not in our library

  183. 183.

    Schillinger U, Holzapfel WH, Wood BJB, Holzapfel WH. The genus Carnobacterium. The Genera of Lactic Acid Bacteria. 1995;307-326.

    Not in our library

  184. 184.

    Schmidt M, Priemé A, Stougaard P. Bacterial diversity in permanently cold and alkaline ikaite columns from Greenland. Extremophiles. 2006;10:551-562.

    Not in our library10.1007/s00792-006-0529-9

  185. 185.

    Schöbitz R, Zaror T, León O, Costa M. A bacteriocin from Carnobacterium piscicola for the control of Listeria monocytogenes in vacuum-packaged meat. Food Microbiol. 1999;16:249-255.

    Not in our library

  186. 186.

    Seppola M, Olsen RE, Sandaker E, Kanapathippillai P, Holzapfel W, Ringø E. Random amplification of polymorphic DNA (RAPD) typing of carnobacteria isolated from hindgut chamber and large intestine of Atlantic cod (Gadus morhua l). Syst Appl Microbiol. 2005;29:131-137.

    Not in our library10.1016/j.syapm.2005.07.006

  187. 187.

    Shannon AL, Attwood G, Hopcroft DH, Christeller JT. Characterization of lactic acid bacteria in the larval midgut of the keratinophagous lepidopteran Hofmannophila pseudospretella. Lett Appl Microbiol. 2001;32:36-41.

    Not in our library10.1046/j.1472-765x.2001.00854.x

  188. 188.

    Shaw BG, Harding CD. A numerical taxonomic study of lactic acid bacteria from vacuum-packed beef, pork, lamb and bacon. J Appl Bacteriol. 1984;56:25-40.

    Not in our library10.1111/j.1365-2672.1984.tb04693.x

  189. 189.

    Signoretto C, Burlacchini G, Pruzzo C, Canepari P. Persistence of Enterococcus faecalis in aquatic environments via surface interactions with copepods. Appl Environ Microbiol. 2005;71:2756-2761.

    Not in our library10.1128/aem.71.5.2756-2761.2005

  190. 190.

    Silva J, Carvalho AS, Teixeira P, Gibbs PA. Bacteriocin production by spray-dried lactic acid bacteria. Lett Appl Microbiol. 2002;34:77-81.

    Not in our library10.1046/j.1472-765x.2002.01055.x

  191. 191.

    Simpson JM, Domingo JWS, Reasoner DJ. Assessment of equine fecal contamination: the search for alternative bacterial source-tracking targets. FEMS Microbiol Ecol. 2004;47:65-75.

    Not in our library10.1016/s0168-6496(03)00250-2

  192. 192.

    Sip A, Grajek W, Boyaval P. Enhancement of bacteriocin production by Carnobacterium divergens AS7 in the presence of a bacteriocin-sensitive strain Carnobacterium piscicola. Int J Food Microbiol. 1998;42:63-69.

    Not in our library10.1016/s0168-1605(98)00062-2

  193. 193.

    Smit G, Smit BA, Engels WJM. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev. 2005;29:591-610.

    Not in our library10.1016/j.femsre.2005.04.002

  194. 194.

    Spanggaard B, Huber I, Nielsen J, Sick EB, Pipper CB, Martinussen T, Slierendrecht J, Gram L. The probiotic potential against vibriosis of the indigenous microflora of rainbow trout. Environ Microbiol. 2001;3:755-765.

    Not in our library10.1046/j.1462-2920.2001.00240.x

  195. 195.

    Sprules T, Kawulka KE, Gibbs AC, Wishart DS, Vederas JC. NMR solution structure of the precursor for carnobacteriocin B2, an antimicrobial peptide from Carnobacterium piscicola. Implications of the α-helical leader section for export and inhibition of type IIa bacteriocin activity. Eur J Biochem. 2004a;271:1748-1756.

    Not in our library10.1111/j.1432-1033.2004.04085.x

  196. 196.

    Sprules T, Kawulka KE, Vederas JC. NMR solution structure of imB2, a protein conferring immunity to antimicrobial activity of the type IIa bacteriocin, carnobacteriocin B2. Biochemistry. 2004b;43:11740-11749.

    Not in our library10.1021/bi048854+

  197. 197.

    Starliper CE, Shotts EB, Brown J. Isolation of Carnobacterium piscicola and an unidentified Gram-positive bacillus from sexually mature and post-spawning rainbow trout Oncorhynchus mykiss. Dis Aquat Org. 1992;13:181-187.

    Not in our library

  198. 198.

    Stoffels G, Nes IF, Gudmundsdottir A. Isolation and properties of a bacteriocin-producing Carnobacterium piscicola isolated from fish. J Appl Bacteriol. 1992a;73:309-316.

    Not in our library10.1111/j.1365-2672.1992.tb04982.x

  199. 199.

    Stoffels G, Nissen-Meyer J, Gudmundsdottir A, Sletten K, Holo H, Nes IF. Purification and characterization of a new bacteriocin isolated from a Carnobacterium sp. Appl Environ Microbiol. 1992b;58:1417-1422.

    Not in our library10.1128/aem.58.5.1417-1422.1992

  200. 200.

    Stohr V, Joffraud JJ, Cardinal M, Leroi F. Spoilage potential and sensory profile associated with bacteria isolated from cold-smoked salmon. Food Res Int. 2001;34:797-806.

    Not in our library

  201. 201.

    Susiluoto T, Korkeala H, Björkroth KJ. Leuconostoc gasicomitatum is the dominating lactic acid bacterium in retail modified-atmosphere-packaged marinated broiler meat strips on sell-by-day. Int J Food Microbiol. 2003;80:89-97.

    Not in our library10.1016/s0168-1605(02)00123-x

  202. 202.

    Suzuki M, Yamamoto T, Kawai Y, Inoue N, Yamazaki K. Mode of action of piscicocin CS526 produced by Carnobacterium piscicola CS526. J Appl Microbiol. 2005;98:1146-1151.

    Not in our library10.1111/j.1365-2672.2005.02546.x

  203. 203.

    Tahiri I, Desbiens M, Benech R, Kheadr E, Lacroix C, Thibault S, Oullet D, Fliss I. Purification, characterization and amino acid sequencing of divergicin M35: a novel class IIa bacteriocin produced by Carnobacterium divergens M35. Int J Food Microbiol. 2004;97:123-136.

    Not in our library10.1016/j.ijfoodmicro.2004.04.013

  204. 204.

    Talon R, Walter D, Montel MC. Growth and effect of staphylococci and lactic acid bacteria on unsaturated free fatty acids. Meat Sci. 2000;54:41-47.

    Not in our library10.1016/s0309-1740(99)00068-6

  205. 205.

    Thornley MJ. Observations on the microflora of minced chicken meat irradiated with 4 MeV cathode rays. J Appl Bacteriol. 1957;20:286-298.

    Not in our library

  206. 206.

    Thornley MJ, Sharpe ME. Micro-organisms from chicken meat related to both lactobacilli and aerobic sporeformers. J Appl Bacteriol. 1959;22:368-376.

    Not in our library

  207. 207.

    Toffin L, Webster G, Weightman AJ, Fry JC, Prieur D. Molecular monitoring of culturable bacteria from deep-sea sediment of the Nankai Trough, Leg 190 Ocean Drilling Program. FEMS Microbiol Ecol. 2004;48:357-367.

    Not in our library10.1016/j.femsec.2004.02.009

  208. 208.

    Toranzo AE, Romalde JL, Nuñez S, Figueras A, Barja JL. An epizootic in farmed, market-size rainbow trout in Spain caused by a strain of Carnobacterium piscicola of unusual virulence. Dis Aquat Org. 1993a;17:87-99.

    Not in our library

  209. 209.

    Toranzo AE, Novoa B, Baya AM, Hetrick FM, Barja JL, Figueras A. Histopathology of rainbow trout, Oncorhynchus mykiss (Walbaum), and striped bass, Morone saxatilis (Walbaum), experimentally infected with Carnobacterium piscicola. J Fish Dis. 1993b;16:261-267.

    Not in our library

  210. 210.

    Truelstrup Hansen L, Huss HH. Comparison of the microflora isolated from spoiled cold-smoked salmon from three smokehouses. Food Res Int. 1998;31:703-711.

    Not in our library

  211. 211.

    van Belkum MJ, Stiles ME. Characterization of the theta-type plasmid pCD3.4 from Carnobacterium divergens, and modulation of its host range by repA mutation. Microbiology. 2006;152:171-178.

    Not in our library10.1099/mic.0.28294-0

  212. 212.

    Vermeiren L, Devlieghere F, Vandekinderen I, Debevere J. The interaction of the non-bacteriocinogenic Lactobacillus sakei 10A and lactocin S producing Lactobacillus sakei 148 towards Listeia monocytogenes on a model cooked ham. Food Microbiol. 2006;23:511-518.

    Not in our library10.1016/j.fm.2005.10.005

  213. 213.

    Vihavainen E, Lundström H-S, Susiluoto T, Koort J, Paulin L, Auvinen P, Björkroth KJ. Role of broiler carcasses and processing plant air in contamination of modified-atmosphere-packaged broiler products with psychrotrophic lactic acid bacteria. Appl Environ Microbiol. 2007;73:1136-1145.

    Not in our library10.1128/aem.01644-06

  214. 214.

    Walker VK, Palmer GR, Voordouw G. Freeze – thaw tolerance and clues to the winter survival of a soil community. Appl Environ Microbiol. 2006;72:1784-1792.

    Not in our library10.1128/aem.72.3.1784-1792.2006

  215. 215.

    Wan J, Harmark K, Davidson BE, Hillier AJ, Gordon JB, Wilcock A, Hickey MW, Coventry MJ. Inhibition of Listeria monocytogenes by piscicolin 126 in milk and Camembert cheese manufactured with a thermophilic starter. J Appl Microbiol. 1997;82:273-280.

    Not in our library10.1046/j.1365-2672.1997.00349.x

  216. 216.

    Wang Y, Henz ME, Gallagher NLF, Chai S, Gibbs AC, Yan LZ, Stiles ME, Wishart DS, Vederas JC. Solution structure of carnobacteriocin B2 and implications for structure–activity relationships among type IIa bacteriocins from lactic acid bacteria. Biochemistry. 1999;38:15438-15447.

    Not in our library10.1021/bi991351x

  217. 217.

    Worobo RW, Henkel T, Sailer M, Roy KL, Vederas JC, Stiles ME. Characteristics and genetic determinant of a hydrophobic peptide bacteriocin, carnobacteriocin A, produced by Carnobacterium piscicola LV17A. Microbiology. 1994;140:517-526.

    Not in our library10.1099/00221287-140-3-517

  218. 218.

    Worobo RW, van Belkum MJ, Sailer M, Roy KL, Vederas JC, Stiles ME. A signal peptide secretion-dependent bacteriocin from Carnobacterium divergens. J Bacteriol. 1995;177:3143-3149.

    Not in our library10.1128/jb.177.11.3143-3149.1995

  219. 219.

    Xu J, Yang H, Lai X, Fu X, Wu J, Huang L, Yu X, Wu Y, Wu Y, Liu B. Etiological study for a case of multi-bacterial synergistic gangrene. Chinese Sci Bull. 1997;42:511-517.

    Not in our library

  220. 220.

    Yamazaki K, Suzuki M, Kawai Y, Inoue N, Montville TJ. Inhibition of Listeria monocytogenes in cold-smoked salmon by Carnobacterium piscicola CS526 isolated from frozen surimi. J Food Prot. 2003;66:1420-1425.

    Not in our library10.4315/0362-028x-66.8.1420

  221. 221.

    Yamazaki K, Suzuki M, Kawai Y, Inoue N, Montville TJ. Purification and characterization of a novel class IIa bacteriocin, piscicocin CS526, from surimi-associated Carnobacterium piscicola CS526. Appl Environ Microbiol. 2005;71:554-557.

    Not in our library10.1128/aem.71.1.554-557.2005

  222. 222.

    Yousif AN, Albright LJ, Evelyn TPT. In vitro evidence for the antibacterial role of lysozyme in salmonid eggs. Dis Aquat Org. 1994;19:15-19.

    Not in our library

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