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Review

The Application of Protective Cultures in Cheese: A Review

by
Thomas Bintsis
1,* and
Photis Papademas
2
1
Laboratory of Safety and Quality of Milk and Dairy Products, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
2
Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology, Limassol 50329, Cyprus
*
Author to whom correspondence should be addressed.
Fermentation 2024, 10(3), 117; https://doi.org/10.3390/fermentation10030117
Submission received: 25 January 2024 / Revised: 15 February 2024 / Accepted: 18 February 2024 / Published: 20 February 2024
(This article belongs to the Special Issue Dairy Fermentation 2.0)
Versions Notes

Abstract

:
A number of non-thermal preservation strategies have been adopted from the dairy industry to improve cheese quality and safety. The application of lactic acid bacteria cultures that produce bacteriocins has been extensively studied as a means of bio-preservation. However, the application of purified bacteriocins as a bio-protective agent is limited in cheese. The application of protective cultures is another strategy, and the aim of the current review is to provide an overview of the application of commercial and autochthonous adjunct cultures on the bio-protection of cheese; both public health and spoilage aspects are considered.

1. Introduction

Cheese is a fermented dairy product which has been produced and consumed since the 7th millennium BC [1]. Cheesemaking practices have evolved throughout the years in different ways in different countries and more than 1400 traditional cheese varieties are produced worldwide, displaying a great diversity of organoleptic characteristics [2]. Since the first introduction of starter cultures at the end of the 19th century, a number of changes have been adoptedin the cheesemaking process and nowadays cheeses are produced in large quantities by fully controlled automated processes, and the use of commercial starter cultures is a prerequisite for a successful cheesemaking process [3]. Starter cultures are divided into defined- and mixed-strain cultures; defined-strain cultures are pure cultures with known physiological characteristics and technological properties [4]. Mixed-strain cultures contain different species or genera of lactic acid bacteria (LAB). The use of commercial starter cultures has been proved to be the best way to standardize cheese manufacture with small variations in the organoleptic characteristics. However, their extended use may reduce the microbiota diversity and its associated benefits [5].
LAB, including the genera Lactobacillus, Lactococcus, Leuconostoc, Enterococcus, Streptococcus and Pediococcus, are the dominant population in raw milk [6,7]. As raw milk is the main source of the cheese microbiota, LAB from the starter and those not deliberately added as part of the starter or adjunct culture (that is, cultures that are added to cheese for purposes other than acidification [8,9,10]) constitute the main part of this microbiota [11,12]. This group of bacteria, either natural or selected, produce compounds that are essential for the acidification of the curd and the cheese flavour development during ripening; additionally, they produce antimicrobial peptides, like bacteriocins, which naturally inhibit undesirable microorganisms [11]. Other strains of non-LAB, yeasts and moulds are also present in the complex milk microflora [6].
The microbiota in cheese is formed from raw milk, the starter culture, the equipment used for the cheesemaking process and the environment; the microbiota ensures the diversity between cheeses throughout cheesemaking and maturation processes [5]. This microbiota is transformed according to the specific conditions of the ripening and maturation and includes LAB from the starter, and the autochthonous microbiota composed mainly of non-starter lactic acid bacteria (NSLAB) [12]. In parallel with the development of defined cultures, autochthonous or natural starter cultures have been developed for a number of cheeses [13,14,15,16,17,18,19]. The use of the latest DNA and RNA next generation sequencing technologies during recent years have greatly contributed to the understanding of the interactions between the autochthonous cheese microbial communities. These complex microbial communities with their enzymic system contribute to the complex biochemical activities occurring throughout cheese ripening and producing flavour compounds, which characterize the organoleptic properties of the final cheese and are much appreciated by consumers of all the world [5,20].
Bio-preservation is a natural way to protect food from spoilage and harmful contamination with either pathogenic or spoilage microorganisms [21]. Bio-preservation is an effective strategy to reduce food waste without using chemical preservatives. In addition, enhanced safety and extended shelf-life using indigenous or added adjunct cultures to control the growth of pathogenic and spoilage microbes can be achieved [22,23]. Chen et al. [22] reviewed the application of antifungal compounds and provided an overview of the mechanisms involved. Moreover, the preservation strategies of non-thermal and packaging technologies and the addition of natural antimicrobial agents and plant extracts and essential oils in cheese have been reviewed by Moula Ali et al. [23].
Protective cultures have been suggested as microorganisms which can reduce the risk of the growth and survival of both pathogenic and spoilage-causing microbes [21,24]. These are added in different cheeses to improve the safety and extend the shelf-life of the cheese.
LAB have been suggested to be used as protective cultures, as they have a long history in safe cheese production and their antagonistic interactions against pathogens and spoilage microbes are well known [25,26]. However, to finally apply LAB protective cultures in cheesemaking, a screening procedure is required and the selected strains should be phenotypically and genotypically characterized, to ensure their safety, and validated for their bio-protecting activities. In this context, Souza et al. reviewed the main strategies for the identification and characterization of the properties of bioprotective LAB [25].
The success of any bio-preservation strategy, applied in cheese, depends on the in situ antimicrobial efficacy of the LAB metabolites [21]. Several reviews have studied the application of bacteriocin-producing LAB in cheese, mainly focusing on nisin and/or other lactococcal bacteriocins [20,27,28,29,30,31,32,33,34,35,36,37,38]. Gonzalez-Gonzalez et al. [31] reviewed the functional properties of bacterial cultures used for different dairy applications and Rangel-Ortega et al. reviewed the food safety issues related to the artisanal cheeses and two strategies for the control of the main pathogenic bacteria, that is, applying LAB and natural compounds [32]. In addition, Ahansaz et al. recently reviewed antimicrobial agents, that is, bacteriocins, organic acids and other metabolites produced by LAB in dairy products; the authors highlighted the limitations in applying bacteriocins in cheese due to the degradation caused by certain peptidases [33].
The aim of the current review is to provide an overview of the application of commercial and autochthonous adjunct cultures on the bio-protection of cheese, both as a control measure for pathogenic bacteria and for spoilage microorganisms. Cheeses were categorized into thirteen groups according to their moisture content and the special cheesemaking practices [2].

2. Antimicrobial Mechanisms

Protective cultures in cheese will exert their antimicrobial activity depending on several factors, i.e., the initial level of contamination, the type of microbial contaminant and technological parameters (i.e., maturation time, storage temperature). It should be mentioned that protective cultures primarily have the potential to stop or delay the onset of further contamination, rather than act on initial high concentrations of microbial contaminants [37]. The three main antimicrobial mechanisms of protective cultures in cheese are briefly described below.

2.1. Metabolites

The protective cultures usually exhibit an amensalism relationship, i.e., interactions in which one type of microbe negatively affects another type, without being affected itself. In dairy fermentations, strains of LAB produce metabolites such as acetic, lactic, propionic, phenyllactic and hydroxyphenyl lactic acids, which have been shown to inhibit the growth of certain bacteria and fungi. The inhibitory effect is either attributed to the reduction in the pH, or to their undissociated forms by diffusing through the cell membranes and releasing H+ ions that acidify the cell cytoplasm. Moreover, the antimicrobial activity is related to the denaturation of membrane proteins, blocking transmembrane transport, proton gradient interference, enzyme inhibition, and reactive oxygen species production, which disturbs the cell metabolism, resulting in growth inhibition [25]. Other LAB antimicrobials include H2O2, fatty acids (decanoic, coriolic), diacetyl and acetoin and bacteriocins [37]. In the case of acetoin or diacetyl, these compounds can interact with arginine, compromising the structure of some proteins; another possible mechanism is that diacetyl can link to DNA molecules, promoting its unfolding [25]. Finally, reuterin produced by Limosilactobacillus reuteri is reported as a potent compound with broad-range antimicrobial activity that inhibits fungi but also Gram-negative bacteria. Limosilactobacillus reuteri uses a CoA-dependent pathway, in which 3-hydroxypropionaldehyde (3-HPA, the active antimicrobial system) is obtained from glycerol in a reaction catalysed by the coenzyme B12-dependent glycerol/diol dehydratase [19].

2.2. Bacteriocins

Bacteriocins are peptides or proteins produced in the ribosome and secreted, mainly, by Gram-positive bacteria such as LAB. They have distinct mechanisms of action and can be divided according to their promotion of a bactericidal effect or bacteriostatic, inhibiting further cell growth [38]. Bacteriocins are divided into three major classes, i.e., Class I, small post-translationally modified peptides; Class II, unmodified bacteriocins; and Class III, larger peptides (>10 kDa, thermo-labile), with each one subdivided into subclasses. Class I bacteriocins comprise the well-known lantibiotics (nisin, lacticin 3147), Class II examples include cyclized peptides (enterocin AS-48), pediocins produced by Pediococcus spp., while a novel Class III bacteriocin is Helveticin-M, produced by Lactobacillus crispatus [39]. The mode of action of bacteriocins has been extensively studied [25,32,33,34,35,36,37,38,39,40] and they generally exert their antibacterial effect by targeting the cell-envelope-associated mechanisms and by pore formation, resulting in a variation in the cytoplasm membrane potential, disrupting the proton motive forceand ultimately causing cell death. Nisin is capable of both mechanisms, i.e., pore formation and the inhibition of cell wall biosynthesis, which are combined within the same molecule for potent antimicrobial activity. Other bacteriocins can kill their target cells through the inhibition of gene expression and protein production [38,41]. Nisin, lacticin 3147 and 481, pediocin AcH, thermophilin, macedocin, reuterin and enterocin AS-38 and KP are some of the bacteriocins that have been effectively applied in different cheeses [29,35,38].However, the low yields, the complexity and the cost of purification and the inactivation through proteolytic enzymes during ripening are the main limiting factors for the addition of bacteriocins in cheese production [19,26,29,35,38].

2.3. Ecological Competition

Protective cultures engage in competitive exclusion where they outcompete the spoilage agent for nutrients and oxygen. Competitive exclusion as a major bioprotective mechanism of lactobacilli against fungal spoilage in fermented milk products is discussed by Siedler et al., where it was concluded that the mechanism of nutrient depletion constitutes an alternative strategy to chemical preservation [42]. Furthermore, protective cultures can take part in quorum sensing—where the microbial cultures ‘feel’ their environment and adjust their performance to deal with these new challenges [39]. The strong antibacterial (antilisterial) effect of ecological competition as expressed in smear-ripened cheeses by some undefined consortia has been reported by Mayo et al., where the cheese ecosystem, its interactions and their effect on safety and quality are extensively discussed [40].

3. Control of Pathogens

Most studies for the application of protective LAB cultures to control pathogens in cheese have been carried out in model cheeses; however, there are also a number of studies on industrial and artisanal cheeses (Table 1, [43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81]).
Lactococcus lactis and Lactiplantibacillus plantarum strains were studied in model cheeses against Listeria monocytogenes with variable results (Table 1). Nisin producing Lc. lactis strains have been applied in a variety of model cheeses and Cheddar cheese slurries to prevent the growth of L. monocytogenes [43,82]. In some cases, Lc. lactis was applied in combination with other LAB and the combined action was found to be more efficient in reducing the growth of L. monocytogenes [44]. The combination of Lpb. plantarum strain with a strain of Lc. lactis that produced nisin reduced the growth of L. monocytogenes in a model ripened cheese; the combination was more effective than the single action [47]. The application of Staphylococcus equorum was studied by Bockelmann et al. and the authors reported strong anti-listerial activity [45].
The application of autochthonous LAB has been studied in several hard cheeses, such as Cheddar, Graviera and Pecorino Sardo [49,50,51]. Graviera cheese is a hard, ripened cheese and the addition of Enterococcus faecium on L. monocytogenes was studied [50]. Meloni et al. evaluated thermophilic LAB to control L. monocytogenes growth in Pecorino Sardo PDO cheese [51].
A number of research papers have been published on the application of protective cultures in semi-hard cheeses. The application of LAB and Hafnia alvei was successfully studied as bio-protective cultures in raw milk cheese against Salmonella spp. and Shigatoxin producing Escherichia coli (STEC) [52]. Callon et al. reported that a combination of H. alvei, Lpb. plantarum and Lc. lactis was the most inhibitory, reducing STEC O26:H11 and O157:H7 by up to 3 Log CFU/g [52]. LAB consortia, isolated from the cheese rind of Saint-Nectaire and then added to the cheese surface, demonstrated a higher anti-listerial activity as compared to the cheese made with a defined starter culture [58]. Lactobacillus brevis, Lpb. plantarum and E. faecalis, where applied in semi-hard cheese, reduced L. monocytogenes counts by up to 4 Log CFU/g [59].
Coelho et al. isolated eight bacteriocin producer strains, identified as Lc. lactis and Enterococcus faecalis from Pico cheese; the authors reported that the adjunct cultures in situ controlled the growth of L. monocytogenes, anda blend of two bacteriocin producing Enterococcus ssp. optimized the reduction in L. monocytogenes counts in fresh cheese [63]. Autochthonous LAB strains have shown bio-protective activities against pathogens [11]; Carnobacterium maltaromaticum has showed antibacterial activity in different French soft cheeses, inhibiting the growth of Psychrobacter spp. and L. monocytogenes [82]. The inhibition of L. monocytogenes was reported by strains of Lactobacillus sakei and Lpb. plantarum in soft cheese [61]. However, Lawton et al. [65] reported that the bacterial cultures did not significantly inhibit the growth of L. monocytogenes in Queso fresco. Martin et al. evaluated the effect of selected protective cultures of Lactocaseibacillus casei and Lactococcus garvieae on the organoleptic characteristics of Torta del Casar cheese and reported no significant effects [67]. In addition, selected strains of Lc. lactis and Enterococcus durans have also been reported to inhibit the growth of L. monocytogenes in ultrafiltered cheese [69]. The application of protective cultures has been studied in Beyaz and Domiati cheeses; Meral Aktas et al. evaluated a nisin-producing Lc. lactis strain for its efficacy to control the growth of L. monocytogenes in Beyaz cheese [71]. O’Sallivan et al. demonstrated the use of bacteriocin produced by LAB for the bio-preservation of bacterial surface-ripened cheeses [75]. Lb. sakei, Lc. lactis and Carnobacterium strains selected from Gorgonzola cheese have been showed to inhibit L. monocytogenes, up to 2 Log CFU/g, in Gorgonzola [76]. Interestingly, the combination of selected LAB with antimicrobial compounds, that is, acid/sodium lactate and L-sodium lactate, has been suggested [83]. The growth of L. monocytogenes was inhibited by strains of Lb. sakei in synbiotic cheese spread and the expression of the genes sak P and sak Q encoding for bacteriocins production was reported [79]. Gensler et al. studied the impact of ten commercial protective cultures on both the antimicrobial activity against L. monocytogenes, STEC and Salmonella spp. and the growth starter cultures, that is, mesophilic, thermophilic and adjunct cultures (Arthrobacter nicotianae and Brevibacterium linens); the authors discussed the importance of identifying protective cultures with limited impact on the starter and adjunct cultures for specific cheeses [84]. van Gijtenbeek et al. studied the competitive exclusion as a bio-protective mechanism against the growth of Listeria spp. in cottage cheese [78]. The growth of the starter culture, that is, Streptococcus thermophilus and Lactococcus lactis, was not influenced by reduced manganese levels [78]. Finally, the incorporation of bacteriocin in active packaging has been suggested by Contessa et al. [85]; the authors reported the reduction in L. monocytogenes by 3 Log units [85].
An important aspect of cheese safety is the reduction in biogenic amines, as many Gram-negative bacteria have been reported to produce cadaverine, histamine or putrescine [11]. Renes et al. showed that the use of an adjunct culture composed of Lc. lactis, Lc. lactis ssp. cremoris and Lpb. plantarum effectively reduced the amount of biogenic amines in cheese [86].

4. Control of Spoilage Microorganisms

A presentation of the most important applications of protective cultures to control spoilage bacteria in cheese is shown in Table 2 [87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113]. Most studies have been conducted to control fungi and spoilage bacteria such as clostridia, pseudomonads, Enterobacteriaceae and coliforms.
Nisin- and lacticin 481-producing Lc. lactis as a starter was shown to delay late blowing defects in the manufacture of model cheeses; the cheese made with clostridial spores and Lc. lactis INIA 415-2 showed late blowing defect after 120 days of ripening, without altering its sensory characteristics [88]. Souza et al. investigated the antagonist activity of Weissella spp. and Lpb. plantarum isolated from Brazilian artisanal cheese and dairy environments against Aspergillus and Penicillium spp. [91]. Acid-coagulated cheeses such as cottage cheese also benefit from the addition of protective cultures to control the spoilage fungi, as shown by numerous studies [108,109,110,111]. The application of commercial and autochthonous protective cultures to control Pseudomonas spp. and Enterobacteriaceae has been studied for Ricotta fresca [112,113]. Makki et al. demonstrated that commercial LAB cultures vary in their antifungal activities [110].
Shi and Maktabdar reviewed the antifungal activities of LAB against different spoilage moulds [114] and Li et al. reviewed the antifungal activities of Lpb. plantarum and its potential in bio-preservation and the mechanisms for the elimination of mycotoxins [115]. Moreover, Erfani et al. performed a systematic review on probiotic bacteria as bio-preservative cultures and reported that Lpb. plantarum showed significant antifungal activities [116]. Further research is needed to empower the optimal cheesemaking parameters to enable protective culture to produce antifungal metabolites in cheese, and this knowledge could help in the selection of LAB strains for specific cheeses. Additional studies are recommended to characterize the interaction potential with starter and other NSLAB. The selected cultures should be tested in industrial scale cheesemaking process.

5. Conclusions

Nisin and other bacteriocins such as enterocins, lactacins and pediocins have been effectively studied as antimicrobial agents to control L. monocytogenes in a variety of cheeses; however, their commercial application is limited. Protective cultures composed of specific strains of the LAB species such as Lc. lactis, Lpb. plantarum, Lcb. paracasei, Lcb. rhamnosus, Lvb. brevis, Lb. sakei, E. faecium and Carnobacterium spp., Bifidobacterium spp. and Propionibacterium spp. have been used to control the growth of pathogenic and spoilage bacteria in different cheeses. The application of protective cultures has been demonstrated to bean important, clean-label strategy for the control of pathogens, mainly L. monocytogenes and spoilage bacteria in cheese, as an additional measure to the application of good hygiene and manufacture practices throughout the whole cheesemaking process. Single strains or combinations of strains have been suggested, but further research is needed to evaluate the effects on the cheese microbial ecology, physico-chemical, organoleptic and nutritional characteristics of each type, before being applied to manage the microbiological risks. The combined use of protective cultures with other natural bio-preservatives and other treatments has showed promising results.

Author Contributions

Conceptualization, T.B. and P.P.; preparation of the first draft of the manuscript, T.B. and P.P.; review and editing, T.B. and P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Applications of protective cultures to control pathogenic bacteria in different cheeses.
Table 1. Applications of protective cultures to control pathogenic bacteria in different cheeses.
Cheese CategoryCheeseProtective CultureTarget Microorganism(s)Main FindingsReference
ModelFresh cheeseThree nisin producing Lc. lactis strainsL. monocytogenesNumbers of L. monocytogenes were reduced in model cheese by 2 Log units during 7 days of storage[43]
ModelMiniature fresh cheeseLc. lactis 16FS16-9/20234-11FS16 and Lpb. plantarum 1/14537-4A/20045)L. monocytogenesReduction in the growth of L. monocytogenes by 3–4 Log units[44]
ModelModel cheeseStaph. equorum SE3L. monocytogenesStaph. equorum inhibited the growth of L. monocytogenes (<1 Log unit)[45]
ModelModel cheeseCommercial protective cultures and bacterial fermentatesL. monocytogenesThe growth of L. monocytogenes was delayed by the protective cultures[46]
ModelLaboratory-scale cheeseLc. lactis CSK2775 and Lpb. plantarum LMG P-26358L. innocuaCombination of the two cultures was suggested for industrial use[47]
ModelCheddar-likeLcb. paracaseiB. cereus, L. monocytogenesLcb. paracasei inhibited both pathogens[48]
HardCheddarAutochthonous LABL. monocytogenesC. crustorum, Lpb. plantarum and Lmb. fermentum decreased the levels of L. monocytogenes in cheese[49]
HardGravieraEnterocin-producing E. faeciumL. monocytogenesE. faecium KE82 is suggested as a protective culture, but the indigenous bacteriocin-producing LAB might contribute to the inhibition of L. monocytogenes in Graviera[50]
HardPecorino Sardo PDOLpb. plantarum (commercial) and an autochthonous LAB (Lb. delbruekii ssp. sunkii).Protection against L. monocytogenesLb. delbruekii ssp. sunkii was as effective as the commercial culture for the protection against L. monocytogenes[51]
Semi-hardUncooked pressed cheeseSingle or combined cultures of 18 selected bacterial strainsE. coli O26:H11 and O157:H7H. alvei, Lpb. plantarum and Lc. lactis reduced the growth of STEC by 3 Log units[52]
Semi-hardSemi-hard cheeseLc.lactis nisin Z producers (44SGLL3, 29FL1 and 41FL1)L. monocytogenes and Stap. aureusLc. lactis 41FL1 reduced Staph.aureus counts by 1.7–3.5 Log units; no effect on L.monocytogenes was observed[53]
Semi-hardCoalhoLcb. rhamnosus EM1107Staph. aureus, Salmonella enteritidis, L. monocytogenes and E. coliLcb. rhamnosus exhibited different inhibition rates against Staph. aureus, Salmonella enteritidis, L. monocytogenes and E. coli[54]
Semi-hardCoalhoLcb. paracaseiStaph. aureus and L. monocytogenesLcb. paracasei delayed the growth of Staph. aureus and L. monocytogenes in Coalho cheese[55]
Semi-hardPressed uncooked cheeseLb. reuteri INIA P57L. monocytogenes and E. coli O157:H7Reuterin production was enhanced with glycerol and resulted in the control of the pathogenic bacteria[56]
Semi-hardArtisanal cheeseE. faecium CRL1879L. monocytogenesE. faecium CRL1879 ensured an efficient control of L. monocytogenes for up to 30 days without altering the organoleptic properties of the artisanal cheese[57]
Semi-hardSt. NectaireComplex cheese microbial consortiumL. monocytogenesThe species composition of the microbial consortium is the most important factor for the antimicrobial activity[58]
Semi-hardMinas (semi-hard)Lvb. brevis 2-392, Lpb. plantarum 1-399 and E. faecalis (1-37, 2-49, 2-388 and 1-400)L. monocytogenesL. monocytogenes was inactivated (reduction by 4–5.8 Log units) during the ripening of semi-hard cheeses by the mix of LAB added[59]
SoftMinas (soft)Lvb. brevis 2-392, Lpb. plantarum 1-399 and E. faecalis (1-37, 2-49, 2-388 and 1-400)L. monocytogenesSelected LAB strains presented a bacteriostatic anti-listerial effect (reduction by 0.6–1.75 Log units) in Minas soft cheese[59]
SoftMinas FrescalLpb. plantarum 49 and Lcb. paracasei 108L. monocytogenesLpb. plantarum 49 and Lcb. paracasei 108 reduced the counts of L. monocytogenes by 2.8 Log units[60]
SoftSoft cheeseLb. sakei and Lpb. plantarumL. monocytogenesStrains of LAB reduced the growth of L. monocytogenes by 1 Log unit in the soft cheese[61]
SoftFresh cheeseLc. lactis (autochthonous)L. monocytogenesThe application of Lc. lactis reduced the growth of L. monocytogenes by 1 Log unit in fresh cheese[62]
SoftFresh cheeseAutochthonous LABL. monocytogenesAutochthonous LAB inhibited the growth of L. monocytogenes in the soft cheese[63]
SoftKareishLpb. plantarumB. cereusLpb. plantarum decreased the counts of B. cereus in Kareish cheese[64]
SoftQueso frescoLb. curvatus, Lb. sakei, P. acidilactici, and Leuc. carnosum (commercial)L. monocytogenesThe LAB cultures did not show any inhibitory effect on L. monocytogenes[65]
SoftSoft sheep milk cheeseLpb. plantarum (commercial)L. monocytogenesLpb. plantarum can control L. monocytogenes growth without affecting the characteristics of the cheese[66]
SoftTorta del CasarLcpb. casei 116 and Lc. garvieae 151L. monocytogenesLcpb. casei 116 and Lc. garvieae 151 inhibited the growth of L. monocytogenes during the ripening of the cheese[67]
SoftSoft cheeseBif. breve and Bif. animalisL. monocytogenesProbiotic cultures resulted in the decrease in L. monocytogenes counts in soft cheese[68]
SoftUF cheeseLc. lactis ssp. lactis and E. duransL. monocytogenesE. durans and L. lactis were suggested for the control of L. monocytogenes in UF cheese[69]
Dutch-typeGoudaLpb. plantarum LMG P-26358L. innocuaThe addition of Lpb. plantarum LMG P-26358 with a nisin producer was found to eliminate L. innocua in Gouda cheese[70]
White-brinedBeyazLc. lactis L54L. monocytogenesLc. lactis L54 inhibited the growth of L. monocytogenes in Beyaz cheese[71]
White-brinedDomiati-typeAutochthonous LABStaph. aureusLcb. rahmnosus has antimicrobial activity against Staph. aureus and could be used as protective culture in soft cheese[72]
White-brinedDomiati-typeLpb. plantarumStaph. aureusThe mixed culture of Lpb. plantarum strains showed improvement of the safety and quality of Domiati-type cheese[73]
Pasta filataNiteFresco DVS 1010, culture A, Lb. acidophilus LA145, Lcb. rhamnosus VT1 and Lcb. rhamnosus GGCoagulase-positive staphylococci and E. coliThe best inhibitory effect for Nite cheese was observed with Fresco DVS 1010 and Lcb. rhamnosus GG[74]
Bacterial surface-ripenedSmear-ripened cheeseLc. lactis DPC4275L. monocytogenesThe lacticin 3147 producer reduced the counts of L. monocytogenes by 3 Log units; regrowth was observed during the ripening[75]
Blue-veinedGorgonzolaAutochthonous LABL. monocytogenesLc. lactis showed inhibition on the growth of L. monocytogenes at 4 °C[76]
Acid-coagulatedCottageLc. lactis (nisin A, Z and lacticin 481 producers)L. monocytogenesOnly weak abilities to reduce L. monocytogenes were reported from the bacteriocin-producers in Cottage cheese[77]
Acid-coagulatedCottageLcb. rhamnosus (non-bacterio-cinogenic)L. monocytogenesInhibition of L. monocytogenes was found to be caused through competitive exclusion, by depletion of manganese[78]
Acid-coagulatedSymbiotic cheese spreadLb. sakei 2a and inulinL. monocytogenesLb. sakei 2a has been suggested to control L. monocytogenes in the cheese spread[79]
Whey cheesesAnthotyrosCrude enterocin ABP extractL. monocytogenesEnterocin ABP extract showed a decreasein L. monocytogenes counts, probably associated with the acidification of the cheese[80]
Whey cheesesAnariE. faecium DM 224, DM 270 and DM 33L. monocytogenesE. faecium DM 33 was found to decrease L. monocytogenes counts by more than 4 Log units[81]
LAB: Lactic acid bacteria, A.: Aeromonas, B.: Bacillus, Bif.: Bifidobacterium, C.: Companilactobacillus, E.: Enterococcus, H.: Hafnia, L.: Listeria, Lc.: Lactococcus, Lb.: Lactobacillus, Lcb.: Lacticaseibacillus, Lpb.: Lactiplantibacillus, Ltb.: Latilactobacillus, Lvb.: Levilactobacillus, Lmb.: Limosilactobacillus, Leuc.: Leuconostoc, P.: Pediococcus, Staph.: Staphylococcus, Str.: Streptococcus.
Table 2. Applications of protective cultures to control spoilage microorganisms in different cheeses.
Table 2. Applications of protective cultures to control spoilage microorganisms in different cheeses.
Cheese CategoryCheeseProtective CultureTarget Microorganism(s)Main FindingsReference
ModelCheese slurriesLc. lactis ssp.
lactis 32 and encapsulated nisin-A		Cl. tyrobutyricumApplication of Lc. lactis was able to control the growth of Cl. tyrobutyricum[87]
ModelModel cheeseLc. lactis ssp. lactis INIA 415 (nisin- and lacticin 481 producer)Cl. beijerinckii INIA 63Bacteriocin producer Lc. lactis resulted in the prevention of late blowing in model cheese[88]
ModelCheese-mimicking
matrix		LABFungiThe antifungal activity was found to be strain-dependent and the fermentation substrate had a strong effect[89]
ModelMiniature CaciottaLpb. plantarum, Lcb. paracasei, Lvb. brevis and Lb. sakeiPen. chrysogenum ATCC 9179 and Asp. flavus ATCC 46283Single and combined adjunct cultures reduced the mould growth by more than 2 Log units after 15 and 30 days of ripening[90]
ModelCheese matrixW. confusa W5 and W8, W. paramesenteroides W9, W. cibaria W25 and Lpb. plantarum Q4C3Asp. niger IOC 207 and Pen. chrysogenum IOC 132The single LAB strains showed antifungal activities in the model cheese against both fungi targets; however, these activities were reduced when combined with a commercial culture[91]
HardCheddar (shredded)Autochthonous LABFungiAll strains of Lpb. plantarum prolonged the shelf life of Cheddar[92]
HardCheddarLb. amylovorus DSM 19280Pen. expansumThe inoculation of Lb. amylovorus adjunct delayed the growth of the mould on the surface[93]
HardPecorino SicilianoLABPseudomonas spp. and EnterobacteriaceaeThe levels of enterobacteria and pseudomonads were not detectable after five months of ripening[94]
Semi-hardCheddar (semi-hard)Lvb. brevis SJC120 in whey gelatin filmFungiThe active packaging showed antifungal activity in Cheddar[95]
Semi-hardExperimental23 strains of Lactobacillus, Leuconostoc and Propionibacterium spp.Pen. commune, M. racemosus, G. geotrichum, Y. lipolyticaThe combination of different LAB and propionibacteria allowed the development of two antifungal combinations[96]
Semi-hardExperimentalFermentates from Lcb. rhamnosus CIRM-BIA1952, Pr. jensenii CIRM-
BIA1774 and M. lanceolatus UBOCC-A-10919		FungiThe fermentate from Pr. jensenii CIRM-BIA1774 showed the greatest antifungal activity and most selected fermentates delayed the growth of spoilage moulds[97]
SoftFresh cheeseAutochthonous LABGram-negative bacteriaC. maltaromaticum and Lcb. rhamnosus lowered psychotropic bacteria by almost 3 Log CFU/g in the soft cheese[98]
SoftFresh cheeseAutochthonous LABAsp. flavus, Asp. parasiticusLpb. plantarum PIN showed remarkable antifungal activity[99]
SoftQueso fresco (soft cheese)Lcb. rhamnosus species (commercial)FungiCommercial protective cultures vary in performance against yeasts and moulds[100]
SoftSoft cheese (low salt)Lcb. rhamnosusAerobic spore-forming bacteriaCombination with nisin and lysozyme[101]
Dutch-typeDutch-typeLb. paracasei LPC37,
Lb. acidophilus NCFM and Lcb. rhamnosus HN001		Coliform bacteria, Enterococcus ssp., yeasts and mouldsThe application of LAB protective cultures was suggested[102]
Dutch-typeGoudaD. hansenii and/or P. acidilactici combined with cysteine-rich antifungal protein PgAFPAsp. parasiticusThe combination of D. hansenii and the cysteine-rich antifungal protein PgAFP resulted in the inhibition of Asp. parasiticus[103]
White-brinedWhite-brined cheeseLcb. rhamnosus and Lpb. plantarum (commercial)Enterobacteriaceae and coliform bacteriaThe use of Lcb. rhamnosus was recommended for white-brined cheese[104]
Pasta-filataBurrataLcb. rhamnosus and Lpb. plantarum (commercial)Spoilage bacteriaThe combination of MAP and protective culture extended the shelf-life of Burrata cheese[105]
Pasta-filataBurrataLpb. plantarum LPAL
and Lcb. rhamnosus LRB		Staphylococci, coliforms and Pseudomonas spp.The use of Lpb. plantarum LPAL and Lcb. rhamnosus LRB extended the shelf-life of Burrata cheese[106]
Pasta filataGrottoneLcpb. casei LC4P1 (commercial)Cl. sporogenesThe protective culture resulted in an inhibition of the PAB starter development[107]
Pasta-filataKasharLpb. plantarum and Lc. lactis ssp. lactisClostridium spp.The co-inoculum resulted in 1 Log unit reduction in Cl. sporogenes counts[108]
Acid-coagulatedCottageLcb. rhamnosus, Bifid. animalis ssp. lactisFungiLcb. rhamnosus alone or in combination with Bif. animalis ssp. lactis inhibited mould growth[109]
Acid-coagulatedCottageMix of Lacticaseibacillus spp. and Lactiplantibacillus spp., Lcb. rhamnosusFungiThe protective cultures were not very effective against yeast, whereas they delayed the spoilage of at least one mould strain[110]
Acid-coagulatedCottageLpb. plantarumPen. communeAll Lpb. plantarum isolates were found to prevent the visible growth of Pen. commune on Cottage cheese[111]
Whey cheeseRicotta frescaCarnobacterium spp. (commercial)Pseudomonas sppCarnobacterium spp. inhibited the growth of
Pseudomonas spp.		[112]
Whey cheeseRicotta frescaE. faecium,
Lpb. plantarum, Lcb. rhamnosus or Carnobacterium spp. or the fermentate
MicroGARD 430 (commercial)		Pseudomonas spp. and EnterobacteriaceaeDifferent reduction rates were observed in the concentrations of Pseudomonas spp. and Enterobacteriaceae[113]
LAB: Lactic acid bacteria, A.: Aeromonas, Asp.: Aspergillus, B.: Bacillus, Bif.: Bifidobacterium, Cl.: Clostridium, C.: Companilactobacillus, D.: Debaryomyces, E.: Enterococcus, G.: Galactomyces, Lc.: Lactococcus, Lb.: Lactobacillus, Lcb.: Lacticaseibacillus, Lpb.: Lactiplantibacillus, Ltb.: Latilactobacillus, Lvb.: Levilactobacillus, Lmb.: Limosilactobacillus, Leuc.: Leuconostoc, M.: Mucor, P.: Pediococcus, Pen.: Penicillium, Pr.: Propionibacterium, Staph.: Staphylococcus, Str.: Streptococcus, Y.: Yarrowia, W.: Weissella.
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Bintsis, T.; Papademas, P. The Application of Protective Cultures in Cheese: A Review. Fermentation 2024, 10, 117. https://doi.org/10.3390/fermentation10030117

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Bintsis T, Papademas P. The Application of Protective Cultures in Cheese: A Review. Fermentation. 2024; 10(3):117. https://doi.org/10.3390/fermentation10030117

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Bintsis, Thomas, and Photis Papademas. 2024. "The Application of Protective Cultures in Cheese: A Review" Fermentation 10, no. 3: 117. https://doi.org/10.3390/fermentation10030117

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