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Review

The Ambiguous Nature of some Non-Starter Lactic Acid Bacteria Actively Participating in Cheese Ripening

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29 August 2023

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Abstract
This mini-review deals with some non-starter lactic acid bacteria (NSLAB) species with a controversial nature known to be both human and animal pathogens but also health-promoting and probiotic. The focus is put on Lactococcus garvieae, two Streptococcus species (Str. uberis and Str. parauberis), four Weissella species (W. hellenica, W. confusa, W. paramesenteroides and W. cibaria) and Mammalicoccus sciuri which worldwide are often found within the microbiotas of different kinds of cheese, mainly traditional artisanal ones made from raw milk and/or relying on environmental bacteria for their ripening. Based on literature data, their virulence and health-promoting effects are examined, and some of the mechanisms of these actions are investigated. Additionally, their possible roles in cheese ripening are also discussed. The analysis so far showed that, in general, the pathogenic and the beneficial strains, despite belonging to the same species, show pretty different genetic constitutions. Yet, when the safety of a given strain is assessed, genomic analysis on its own is not enough, and a polyphasic approach is needed including additional physiological and functional tests.
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Subject: Biology and Life Sciences  -   Food Science and Technology

1. Introduction

In the last years customers worldwide turned their interest to fermented dairy foods because being considered functional ones. In this regard, special attention was put on traditional artisanally produced kinds of cheese, which are highly priced, and which, in many cases, are prepared from raw milk and/or for their ripening rely on environmental microbiota. In this case, this environmental microbiota comes from the ambient environment (waters, pastures, air, etc.) but also from the human and animal external (skin, furring) and internal environments (gastrointestinal tract (GIT), mammary glands, etc.). For instance, environmental bacteria could be commensal or pathogenic in their nature. Still, when happening in milk, which is a very nutritionally rich environment, they could adapt to this new environment and assimilate the milk sugars, proteins, and fats. These adaptations are in two main directions: loss of some virulence determinants and acquisition of genetic changes allowing better assimilation of the milk’s nutrients. Often, by becoming part of the dominant autochthonous microbiota, these “new dairy bacteria” play an essential role in cheese ripening by contributing to the specific organoleptic and rheological properties.
Typical examples of NSLAB with dualistic nature, which actively participate in cheese ripening, are the members of the genus Enterococcus, which also could be opportunistic human and animal pathogens or probiotics, and which are investigated in both of their aspects from decades [1]. However, in the last decade, with the advent of the next-generation sequencing (NGS) techniques used for metagenomic studies of different kinds of cheese, several ubiquitous newcomers were revealed within the group of the ambivalent NSLAB. Some of the most controversial omnipresent NSLAB belong to the genera Lactococcus, Streptococcus, Weissella and Mammalicoccus (Table 1).

2. Lactococcus Garvieae

Lc. garvieae is a species with a pronounced dualistic nature, participating in the ripening of many cheeses worldwide but also being known as a pathogen. This species is mainly known as the causative agent of fish lactococcosis associated with hyperacute and hemorrhagic septicemia, leading to substantial economic losses [2]. The species is generally considered safe for humans and farm animals; nonetheless, occasionally, it was associated with bovine mastitis [3]. Rare cases of endocarditis in old and immunocompromised persons were also reported [4] (Table 2). On the other hand, Lc. garvieae has been reported to be present in different environmental niches, including plant sprouts [5], as well as in different fermented foods such as fermented sausages [6], but mainly in fermented dairy products, including many types of cheese worldwide.
One of the earliest reports of Lc. garvieae in cheese dates from 2001, when it was found to be part of the microbiotas of some traditionally prepared mozzarellas [7,8]. Later, it was reported worldwide for many kinds of cheese prepared mainly from raw milk and/or without the addition of starter cultures, such as the Italian Toma Piemontese cheese [9], the Spanish Casín cheese [10] and “Torta del Casar” cheese [11], the Slovakian May bryndza cheese [12], the Azorean Pico cheese [13], some traditional Montenegrin brine cheeses [14], some Bulgarian and Turkish “Skin bag” (Tulum) cheeses [15,16] and the Bulgarian “Green” [17] and Krokmach [18] cheeses (Table 1).
It has been reported that when present within the dominant microflora, dairy Lc. garvieae strains positively contribute to cheese ripening and palatability [19], and they are also partially responsible for the typical sensorial characteristics of the final product [20]. It has been proven that dairy-related strains are lactose fermenters [20], despite the relatively slow acidification rate [20] (Table 3). Their presence does not affect the main physicochemical properties such as humidity, water activity, pH, texture, or color while contributing positively to the aroma by the production of methyl-branched acids and reducing the oxidation compounds originating from the β-oxidation of the fatty acids present within the milk [21].
Inhibitory activity against pathogens and spoiling agents has also been reported for some dairy Lc. garvieae strains. Some of the main manifestations of this property are the documented inhibition of Listeria monocytogenes [11] and Staphylococcus aureus [22]. This bacteriostatic effect could be due to nutritional competition or hydrogen peroxide production [23]. However, lactococci are known bacteriocins producers, and dairy-related members of the genus are not an exception. Some examples are the broad-spectrum bacteriocins garvicin KS with inhibitory activity against Bacillus, Listeria, Enterococcus and Staphylococcus [24] and garviecin L1-5 with inhibitory activity against Clostridium, Enterococcus, Lactococcus and Listeria [25] (Table 3). These inhibitory and/or bacteriostatic properties are currently heavily exploited, and to control Listeria growth, some authors propose the addition of selected Lc. garvieae strains as NSLAB within the starter cultures [11] and even their inclusion within the edible cheese coatings [26].
There are many scientific proofs that dairy-derived Lc. garvieae strains show different genetic constitutions from the pathogenic ones. First, they can grow on milk because of their ability to assimilate lactose. Fortina et al. report that dairy isolates possess the genes necessary for lactose catabolism, while these genes are absent in the fish pathogens, and even more, these genes are located on the bacterial chromosome in contrast to the cheese “big classic” Lc. lactis [27]. These observations are further confirmed by the study of Foschino et al., who found that Lc. garvieae from the two ecological niches are genetically divergent [28]. Additionally, dairy-derived strains lack some of the pathogenicity phenotypes: they are non-agglutinating [5], they do not produce hemolysins and gelatinase, as well as many of the dairy strains lack the tetM and tetS genes encoding tetracyclines resistances. [20] All these findings accredit them to low virulence and pathogenicity profiles.
Taking into account these issues, Lc. garvieae should be considered an essential and promising NSLAB that contributes positively to the ripening process and the quality of the product. Nonetheless, to be applied as an additive to the starter cultures, because of the ambiguous nature of the species, to guarantee its safety, a thorough study of each strain should be conducted, for example, by whole-genome sequencing combined with phenotype characteristics.

3. Streptococcus uberis and Streptococcus parauberis

Half a century ago, Str. uberis was reported to be the causative agent of clinical and subclinical cases of bovine mastitis [29]. A decade later, based on some phenotypic characteristics, Str. parauberis, which was also documented as a bovine mastitis causative agent, was separated from Str. uberis as a different species [30]. The new species turned out to be also a fish pathogen [31], while Str. uberis was only detected in water environments and fishes without being associated with some pathogenesis [32]. It has been documented that these species possess good environmental survival capabilities [33], which can explain why they are responsible for a significant proportion of clinical mastitis cases [34]. Str. uberis has been occasionally associated with human infection; however, there is scientific evidence that in these cases, it has probably been misidentified [35]. In the last years in the scientific literature, rare cases of infections in humans caused by Str. parauberis have been reported [36,37] (Table 2). Even though, in both cases, traumatism was involved, and human biological barriers were not passed through in a natural way. Both species have been shown to be present in different ecological niches in dairy farms, such as wastewater disposal sites, raw milk, udder, cow skin, grass, and soil [38].
Since both species are widely spread in the environment, as well as their ability to infect the cattle mammary glands, it is not surprising to find them in milk and fermented dairy products prepared from raw milk (Table 1). Str. uberis has been detected for the first time among the dominant microbiota of a Mozzarella cheese [8], while Str. parauberis was reported as a dominant species for the Spanish blue-veined Cabrales cheese [39]. In combination or separately, both species have been observed in high amounts in many kinds of cheese worldwide. Some examples include the traditional Spanish Casín cheese [10], the Iranian Lighvan and Koozeh cheeses [40], some Slovenian raw milk cheeses [41], the Slovakian May bryndza cheese [12], the Italian Casizolu [42], Giuncata and Caciotta Leccese [43] cheeses, the Turkish Tulum cheese [16] and the Bulgarian Mehovo sirene cheese [15].
The observation of high amounts of Str. uberis and Str. parauberis within the cheese microbiotas means that they play a role in the ripening process (Table 3). It was reported that Str. uberis produces an extracellular protein named streptokinase which activates the plasminogen to active plasmin, which in turn results in plasmin-induced proteolysis of the milk proteins [44]. Initially, this mechanism has evolved for the development of mastitis; still, it also contributes to the ripening of the cheeses. The same mechanism of Str. parauberis was observed and studied during the ripening process of the Azerbaijani Lighvan cheese [45].
Str. thermophilus is known to contribute significantly to flavor development [46], so it is logical to expect that in the ripening process, other members of the genus should play, to some extent, the same role. Indeed, Yang et al. report a positive correlation between some of the organoleptic properties of several cheese samples and the high content of Str. parauberis within their microbiota. These authors explain their observation by the findings that some Str. parauberis strains are capable of producing enzymes needed for the production of linear alkanes and alcohols [47].
In contrast to Lc. garvieae isolates which split into a pathogenic and dairy lineage; not surprisingly, no such observations have been detected for the Str. uberis and Str. parauberis isolates considering the fact that they originate from environmentally infected cattle. Still, in addition to their participation in the cheese ripening process and the development of palatability, because of their ability to inhibit the growth of some other pathogens and spoiling agents, some isolates have additional beneficial effects on the final product (Table 3). Tulini et al. report the isolation of bacteriocins producing Str. uberis strains from Brazilian cheese inhibiting the growth of Carnobacterium maltaromaticum, Latilactobacillus sakei, and Listeria monocytogenes [48]. Antagonistic activity determined by Str. uberis was also reported for several cheese isolates from Serbia, and the authors report that these isolates are also susceptible to antibiotics [49].

4. The genus Weissella

Based on a comparative analysis of the 16S rRNA genes, the Weissella genus was separated from the Leuconostoc genus in 1993, with W. hellenica as a novel species isolated from a type of Greek sausage [50]. Soon after, it became apparent that the genus possesses an ambitious nature comprising species with clear pathogenic potential and species with strong probiotic properties and potential for the food industry. Unfortunately, some species comprise as well as strains with beneficial properties but also proven pathogenic strains [51].
Among Weissella species, mainly W. hellenica, W. confusa, W. cibaria, and W. paramesenteroides were reported to participate in the fermentation of dairy products [43]. Till now, there are no scientific reports on the association of W. hellenica and W. paramesenteroides with clinical cases or infections in humans or animals. In contrast, W. confusa is definitely a species with a dualistic nature—some isolates have been reported as pathogens while others as probiotics (Table 2). W. confusa has been reported to cause bacteremia [52] and endocarditis [53] in humans and even deadly infections in primates [54]. On the other hand, many strains of the same species possess different strong probiotic properties [55,56,57]. W. cibaria was first considered as a human and animal commensal species which can be isolated from feces, saliva, and vaginal mucous; still, the species emerged also as an opportunistic pathogen associated with human blood and lung swab bacteremias, as well as being isolated from human urine [58]. It has also been linked to otitis in dogs [59]. Similarly to W. confusa, for many W. cibaria isolates, probiotic properties have been documented [60,61].
The different Weissella species have been reported to be part of the microbiotas of many kinds of cheese worldwide, mainly artisanal and/or prepared from raw milk (Table 1). W. hellenica was reported for Danish raw milk cheeses [62], Croatian cheese [41], several Brazilian artisanal cheeses [56], and traditional Italian Mozzarella cheese [63]. Some examples of the presence of W. paramesenteroides within the cheeses microbiota are a type of a Mexican ripened cheese [64], some traditional French cheeses [65], the Columbian double cream cheese [66], the Greek hard cheese Manura [67] and the traditional Turkish Sepet cheese [68]. W. confusa was also reported for the latter [68]. Still, it was also found within the microbiotas of Kazak cheese [69] and a quite specific kind of Indonesian cheese [70]. Similarly to the other three species, W. cibaria has been reported to be part of the microbiotas of different cheeses around the globe—within the West African Tchoukou cheese [71] and within a cheese from the Western Himalayas [57]. Moreover, because of their probiotic properties, some W. cibaria have been often added as adjunct cultures [72].
The role of Weissella species in cheese ripening is to a great extent linked to their beneficial and health-promoting effects due to the synthesis of exopolysaccharides (EPS) or the inhibition of pathogens [51,73,74] (Table 3). By synthesizing EPS [57,75], they contribute the rheological properties. On the other hand, by their ability to produce lactic acid and other low molecular weight acids by assimilating lactose and galactose, they not only inhibit the growth of some potential pathogens and soiling agents but also contribute to the coagulation of milk proteins [56,76]. Another significant role that could play dairy Weissella isolates could be related to the lipolytic and proteolytic activities, which in turn contribute to the development of the aroma and the flavor [72]. Many strains are reported to produce the volatile compound diacetyl related to the “buttery” aroma resulting from the conversion of citrate to pyruvate [56].
Many different Weissella spp. isolates have been proven to possess probiotic and health-promoting effects such as the production of EPS; they possess antioxidant activity, can transform prebiotics, and have antimicrobial activities due to the production of hydrogen peroxide, organic acids, and bacteriocins. For W. cibaria, W. confusa, and W. paramesenteroides, which can also be found in cheese and dairy environments, good survival capabilities within the gastrointestinal tract (GIT), alongside the ability to transform prebiotic fibers, have been reported [74].
Different Weissella isolates from different types of samples are among the most potent producers of different types of linear and branched EPS, such as glucans, dextrans, mannose, glucose and galactose homo- and heteropolysaccharides. For many of them, beneficial biological probiotic and prebiotic properties such as antioxidant activity, antimicrobial activities, immunomodulatory activity, prebiotic potential, and stimulation of the growth of probiotic bacteria have been reported [51,77]. Cheese-derived W. cibaria and W. confusa isolates are also reported to be EPS producers [57,78]. Because of both the EPS’s health-beneficial effects and their attribution to the rheological properties of the cheese, EPS-producing strains are often added as an adjunct NSLAB cultures in cheese production [72].
One of the mechanisms of the antibacterial activity against pathogens of Weissella spp. is the production of bacteriocins [74,79,80]. Yet, the antimicrobial action against pathogens can also result from the synthesis of organic acids, EPS, or hydrogen peroxide [61,74]. Hydrogen peroxide production has been proven to have an oral health-promoting effect due to the inhibition of Streptococcus mutans and Fusobacterium nucleatum, which are causative agents of plaque formation and periodontitis [51,60]. A W. confusa isolate was reported to inhibit Helicobacter pylori’s growth and to block its binding to the stomach [55]. The antilisterial and antioxidant activities of a W. cibaria isolate were exploited by its addition as an adjunct NSLAB culture [73]. In addition, antifungal activities of food-isolated Weissella strains were discovered. A W. paramesenteroides strain was shown to inhibit food molds by the production of phenyllactic acid, 2-hydroxy-4-methylpentanoic acid, and other organic acids [81], while a W. cibaria sourdough isolate showed potent inhibitory activity against Aspergillus niger, Penicillium roqueforti and Endomyces fibuliger by an uninvestigated mechanism [82].
Some additional health-promoting and beneficial effects have been identified in some Weissella spp. strains. For example, both antitumor and chemopreventive effects [83] and anti-obesity effects [84] have been reported. Immunomodulating, anti-inflammatory, and antiviral activity have also been observed [51].
Because of the many probiotic and health-promoting effects, Weissella spp. are of great interest to the pharmaceutical and food industries. Yet, because of the controversial dualistic nature of the representatives of the genus, one should take great caution before attributing a “generally recognized as safe” (GRAS) status to a Weissella isolate. Without any doubt, each promising isolate should be investigated separately. It can be done by whole genome sequencing and bioinformatic analysis for the presence of genes encoding probiotic determinants and genes encoding virulence factors. Though, in silico analysis is not enough to assess the virulence potential of a given isolate because some genetic determinants for virulence factors are intrinsic to the genus, and many LAB of other genera with a GRAS status, while at the same time, some others genetic determinants could contribute to the probiotic potential [51]. So, to characterize new Weissella isolates, a polyphasic approach comprising both genomic analyses and physiological and functional tests would give the most accurate results [85].
The presence of genes encoding haemolysins and haemolysin-like proteins appears to be ubiquitous in many LAB [85] and can often be revealed by in silico analyses of Weissella genome sequences [51]. For this reason, it is largely believed that they should not be regarded as an exclusion factor for a probiotic isolate [51,85].
Another potential trait of concern is the presence of antibiotic resistance (AR) genes. Yet, the resistance to some commonly used classes of antibiotics, such as glycopeptides (vancomycin), aminoglycosides (gentamycin, kanamycin), and sulphonamides, is in many cases intrinsic to many LAB, including several Weissella spp. [85]. In general, if the antibiotic-resistance genetic determinants are not located on mobile genetic elements or plasmids, they cannot be assessed as virulence factors because they are considered intrinsic [51]. So, in the case of the AR, only phenotypic characterization is insufficient, and in-depth genomic analysis is needed to assess the virulence potential of a given Weissella strain.
Adhesins are another factor that could raise a concern. In pathogenic bacteria, they play an essential role in the colonization and the interaction with the host [86], yet, the same proteins also contribute to the colonization of the health-beneficial bacteria and block the adhesion of pathogens by concurrence mechanism as is the case of a probiotic W. cibaria isolate [87]. A significant role in the adhesion of the probiotic bacteria within the GIT is played by the mucus-binding proteins, so the presence of genetic determinants is considered a beneficial trait, as it was reported for a W. cibaria cheese isolate [57].

5. Mammalicoccus sciuri (Formerly Known as Staphylococcus sciuri)

Mammalicoccus sciuri is a member of the coagulase-negative staphylococci (CNS) group. The CNS are a group of bacteria found among the predominant species in many fermented foods worldwide [88]. M. sciuri was first identified as Staphylococcus sciuri in 1976 as a new species of the so-called group III staphylococci, which were reported to be human and animal skin commensals [89]. It was reclassified in 2020 as a member of the new genus Mammalicoccus of the Staphylococcaceae family [90]. Within time, some M. sciuri strains were reported to possess strong pathogenic potential for humans and animals. In humans, it has been reported to be a causative agent of wound infections [91], urinary tract infections [92], endocarditis [93], sepsis in adults [94] as well as neonatal sepsis [95], endophtalmitis [96], peritonitis [97], and plevric inflammatory disease [98].
M. sciuri strains have been isolated mainly from warm-blooded animals, comprising farm animals, pets and wild animals. Often this species is found in a large variety of healthy farm animals such as pigs, poultry, sheep, goats and horses [99], but also in a broad range of wild animals – rodents, carnivores, monkeys, and even cetaceans and marsupials [100]. However, potentially pathogenic strains are often recovered from farm animals such as pigs, cows and broilers [101], and it is not surprising that members of this species are causative agents of mastitis in dairy cattle (cows and goats) [99,102], as well as of severe epidermitis in piglets [103]. The species was also discovered in goats suffering from ovine rinderpest [104]. It has also been associated with fatal infections in pets (dogs and cats), causing acute respiratory distress syndrome [105] (Table 2).
Different CNS species have been identified as a part of the dominant and subdominant microflora of many kinds of traditional cheeses [106,107] (Table 1). M. sciuri, despite being mainly associated with the ripening of fermented meat products such as cured meats and saussages [88,108,109], it has also been found in French smear cheeses [106], German cheeses [107], Brazilian cheeses [110] and the traditional Middle East Surk cheese [111] (Table 1).
Despite not being especially studied, the role of M. sciuri within the fermented foods ripening could not be very different from that of the other CNS. It has been reported that food-derived staphylococci contribute mainly to the organoleptic properties (Table 3). This function is achieved thanks to the catabolism of carbohydrates and amino acids and the synthesis of esters. Small flavor compound molecules are also produced by some aspects of their proteolytic and lipolytic activities [88,108]. A correlation between the smell and the presence of M. sciuri has been investigated, and it was found that this species, in combination with some yeasts, is responsible for the olfactory characteristics of some green cheeses [112].
Although some sporadic reports of the isolation of M. sciuri strains with probiotic activity [113], in general, because of the species’ relatively strong pathogenic potential, as well as the lack of isolates with attributed GRAS status in the United States or QPS status in the European Union, the question of the health-promoting effects should be considered with great caution.
There are no comparative studies on the genetic lineages and the constitution of pathogenic M. sciuri isolates and those derived from fermented foods, while similar investigations on other CNS are relatively scarce. One of the main concerns of using these bacteria as adjunct cultures is that they usually carry genetic determinants for virulence factors. One type is the presence of genes encoding hemolysins. Still, there are reports that the presence of such factors does not always imply a hemolytic phenotype, and their presence in food-derived CNS is generally sporadic [108]. Another concern is their ability to produce biogenic amines such as cadaverine, putrescine, histamine and tyramine, which could cause food poisoning. However, comparative genomic analysis showed that they usually lack the necessary genes. These findings are greatly supported by the fact that till now, cases of food poisoning due to CNS were never reported [88].
The presence of AR genes could be another indicator of pathogenicity. Within the group of CNS, one of the most predominant AR is the methicillin resistance, encoded by the mecA gene. Interestingly, although the presence has been reported in many M. sciuri isolates, it is usually not sufficient to confer resistance, except if other regulators mec-genes are also present as part of a mobile genetic element known as staphylococcal cassette chromosome (SCCmec) [114]. So, similarly to the other dualistic NSLAB discussed already, the pathogenic potential of the AR genes depends on whether they are located in mobile elements, while the intrinsic AR represent low risk [108]. Additional risk comes from the fact that M. sciuri possesses a vast range of habitats, including wild animals and environments, which could serve as a reservoir for pathogenicity determinants, which in turn could be passed to dairy strains by horizontal genetic transfer [100].

6. Conclusions

Taking into account the considerations above, based on genomic, functional, and physiological analyses, several conclusions for the dualistic NSLAB of the genera Lactococcus, Streptococcus, Weissella and Staphylococcus could be made. First, it is scientifically proven that they contribute to the ripening of the cheeses by influencing the organoleptic and rheological properties. Second, the food-related strains usually differ in their genetic constitution and phenotypic characteristics from the pathogenic strains. Third, many food- and dairy-related strains possess probiotic and health-promoting properties, giving characteristics of a functional food of the products they ferment. Finally, to evaluate the safety of each isolate of these controversial genera, a polyphasic approach should be performed, combining genomic analyses and physiological and functional studies.

Author Contributions

Conceptualization, S.G.D.; methodology, S.G.D.; software, n.a.; validation, n.a.; formal analysis, n.a; investigation, S.G.D.; resources, n.a.; data curation, S.G.D.; writing—original draft preparation, S.G.D.; writing—review and editing, S.G.D.; visualization, n.a.; supervision, n.a.; project administration, S.G.D.; funding acquisition, S.G.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the BULGARIAN NATIONAL SCIENCE FUND, grant number КП-06-66/6 from December 13, 2022.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The author declares no conflict of interest.

References

  1. Hanchi, H.; Mottawea, W.; Sebei, K.; Hammami, R. The Genus Enterococcus: Between Probiotic Potential and Safety Concerns—An Update. Frontiers in Microbiology 2018, 9. [Google Scholar] [CrossRef]
  2. Vendrell, D.; Balcázar, J.L.; Ruiz-Zarzuela, I.; de Blas, I.; Gironés, O.; Múzquiz, J.L. Lactococcus garvieae in fish: A review. Comparative Immunology, Microbiology and Infectious Diseases 2006, 29, 177–198. [Google Scholar] [CrossRef]
  3. Rodrigues, M.X.; Lima, S.F.; Higgins, C.H.; Canniatti-Brazaca, S.G.; Bicalho, R.C. The Lactococcus genus as a potential emerging mastitis pathogen group: A report on an outbreak investigation. Journal of Dairy Science 2016, 99, 9864–9874. [Google Scholar] [CrossRef]
  4. Fefer, J.J.; Ratzan, K.R.; Sharp, S.E.; Saiz, E. Lactococcus garvieae endocarditis: report of a case and review of the literature. Diagnostic Microbiology and Infectious Disease 1998, 32, 127–130. [Google Scholar] [CrossRef]
  5. Kawanishi, M.; Yoshida, T.; Kijima, M.; Yagyu, K.; Nakai, T.; Okada, S.; Endo, A.; Murakami, M.; Suzuki, S.; Morita, H. Characterization of Lactococcus garvieae isolated from radish and broccoli sprouts that exhibited a KG+ phenotype, lack of virulence and absence of a capsule. Letters in Applied Microbiology 2007, 44, 481–487. [Google Scholar] [CrossRef]
  6. Rantsiou, K.; Urso, R.; Iacumin, L.; Cantoni, C.; Cattaneo, P.; Comi, G.; Cocolin, L. Culture-Dependent and -Independent Methods To Investigate the Microbial Ecology of Italian Fermented Sausages. Applied and Environmental Microbiology 2005, 71, 1977–1986. [Google Scholar] [CrossRef]
  7. Coppola, S.; Blaiotta, G.; Ercolini, D.; Moschetti, G. Molecular evaluation of microbial diversity occurring in different types of Mozzarella cheese. Journal of Applied Microbiology 2001, 90, 414–420. [Google Scholar] [CrossRef]
  8. Morea, M.; Baruzzi, F.; Cocconcelli, P.S. Molecular and physiological characterization of dominant bacterial populations in traditional Mozzarella cheese processing. Journal of Applied Microbiology 1999, 87, 574–582. [Google Scholar] [CrossRef]
  9. Fortina, M.G.; Ricci, G.; Acquati, A.; Zeppa, G.; Gandini, A.; Manachini, P.L. Genetic characterization of some lactic acid bacteria occurring in an artisanal protected denomination origin (PDO) Italian cheese, the Toma piemontese. Food Microbiology 2003, 20, 397–404. [Google Scholar] [CrossRef]
  10. Alegría, Á.; Álvarez-Martín, P.; Sacristán, N.; Fernández, E.; Delgado, S.; Mayo, B. Diversity and evolution of the microbial populations during manufacture and ripening of Casín, a traditional Spanish, starter-free cheese made from cow’s milk. International Journal of Food Microbiology 2009, 136, 44–51. [Google Scholar] [CrossRef]
  11. Martín, I.; Rodríguez, A.; Córdoba, J.J. Application of selected lactic-acid bacteria to control Listeria monocytogenes in soft-ripened “Torta del Casar” cheese. LWT 2022, 168, 113873. [Google Scholar] [CrossRef]
  12. Pangallo, D.; Šaková, N.; Koreňová, J.; Puškárová, A.; Kraková, L.; Valík, L.; Kuchta, T. Microbial diversity and dynamics during the production of May bryndza cheese. International Journal of Food Microbiology 2014, 170, 38–43. [Google Scholar] [CrossRef] [PubMed]
  13. LACTIC, T.C.O. Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal pico cheese. Ciências Agrárias, Ramo Tecnologia Alimentar 2017, 102.
  14. Martinovic, A.; Cabal, A.; Nisic, A.; Sucher, J.; Stöger, A.; Allerberger, F.; Ruppitsch, W. Genome Sequences of Lactococcus garvieae and Lactococcus petauri Strains Isolated from Traditional Montenegrin Brine Cheeses. Microbiology Resource Announcements 2021, 10, 10.1128/mra.00546–00521. [Google Scholar] [CrossRef]
  15. Dimov, S.G.; Posheva, V.; Georgieva-Miteva, D.; Peykov, S.; Kitanova, M.; Ilieva, R.; Dimitrov, T.; Iliev, M.; Gotcheva, V.; Strateva, T. Artisanal cheeses relying on spontaneous fermentation as sources of unusual microbiota – The example of the Bulgarian ‘mehovo sirene’ skin bag cheese. International Journal of Dairy Technology 2023. [Google Scholar] [CrossRef]
  16. Gezginc, Y.; Karabekmez-Erdem, T.; Tatar, H.D.; Dağgeçen, E.C.; Ayman, S.; Akyol, İ. Metagenomics and volatile profile of Turkish artisanal Tulum cheese microbiota. Food Bioscience 2022, 45, 101497. [Google Scholar] [CrossRef]
  17. Dimov, S.G.; Gyurova, A.; Zagorchev, L.; Dimitrov, T.; Georgieva-Miteva, D.; Peykov, S. NGS-Based Metagenomic Study of Four Traditional Bulgarian Green Cheeses from Tcherni Vit. LWT 2021, 152, 112278. [Google Scholar] [CrossRef]
  18. Dimov, S.G. The unusual microbiota of the traditional Bulgarian dairy product Krokmach – A pilot metagenomics study. International Journal of Dairy Technology 2022, 75, 139–149. [Google Scholar] [CrossRef]
  19. Fernández, E.; Alegría, Á.; Delgado, S.; Mayo, B. Phenotypic, genetic and technological characterization of Lactococcus garvieae strains isolated from a raw milk cheese. International Dairy Journal 2010, 20, 142–148. [Google Scholar] [CrossRef]
  20. Fortina, M.G.; Ricci, G.; Foschino, R.; Picozzi, C.; Dolci, P.; Zeppa, G.; Cocolin, L.; Manachini, P.L. Phenotypic typing, technological properties and safety aspects of Lactococcus garvieae strains from dairy environments. Journal of Applied Microbiology 2007, 103, 445–453. [Google Scholar] [CrossRef]
  21. Martín, I.; Rodríguez, A.; García, C.; Córdoba, J.J. Evolution of Volatile Compounds during Ripening and Final Sensory Changes of Traditional Raw Ewe’s Milk Cheese “Torta del Casar” Maturated with Selected Protective Lactic Acid Bacteria. Foods 2022, 11, 2658. [Google Scholar]
  22. Abdelfatah, E.N.; Mahboub, H.H.H. Studies on the effect of Lactococcus garvieae of dairy origin on both cheese and Nile tilapia (O. niloticus). International Journal of Veterinary Science and Medicine 2018, 6, 201–207. [Google Scholar] [CrossRef] [PubMed]
  23. Björck, L.; Rosén, C.-G.; Marshall, V.; Reiter, B. Antibacterial Activity of the Lactoperoxidase System in Milk Against Pseudomonads and Other Gram-Negative Bacteria. Applied Microbiology 1975, 30, 199–204. [Google Scholar] [CrossRef] [PubMed]
  24. Villani, F.; Aponte, M.; Blaiotta, G.; Mauriello, G.; Pepe, O.; Moschetti, G. Detection and characterization of a bacteriocin, garviecin L1-5, produced by Lactococcus garvieae isolated from raw cow’s milk. Journal of Applied Microbiology 2001, 90, 430–439. [Google Scholar] [CrossRef] [PubMed]
  25. Ovchinnikov, K.V.; Chi, H.; Mehmeti, I.; Holo, H.; Nes, I.F.; Diep, D.B. Novel Group of Leaderless Multipeptide Bacteriocins from Gram-Positive Bacteria. Applied and Environmental Microbiology 2016, 82, 5216–5224. [Google Scholar] [CrossRef] [PubMed]
  26. Silva, S.P.M.; Ribeiro, S.C.; Teixeira, J.A.; Silva, C.C.G. Application of an alginate-based edible coating with bacteriocin-producing Lactococcus strains in fresh cheese preservation. LWT 2022, 153, 112486. [Google Scholar] [CrossRef]
  27. Fortina, M.G.; Ricci, G.; Borgo, F. A Study of Lactose Metabolism in Lactococcus garvieae Reveals a Genetic Marker for Distinguishing between Dairy and Fish Biotypes. Journal of Food Protection 2009, 72, 1248–1254. [Google Scholar] [CrossRef]
  28. Foschino, R.; Nucera, D.; Volponi, G.; Picozzi, C.; Ortoffi, M.; Bottero, M.T. Comparison of Lactococcus garvieae strains isolated in northern Italy from dairy products and fishes through molecular typing. Journal of Applied Microbiology 2008, 105, 652–662. [Google Scholar] [CrossRef]
  29. King, J.S. Streptococcus Uberis: A Review of its Role as a Causative Organism of Bovine Mastitis I. Characteristics of the Organism. British Veterinary Journal 1981, 137, 36–52. [Google Scholar] [CrossRef]
  30. Williams, A.M.; Collins, M.D. Molecular taxonomic studies on Streptococcus uberis types I and II. Description of Streptococcus parauberis sp. nov. Journal of Applied Bacteriology 1990, 68, 485–490. [Google Scholar] [CrossRef]
  31. Domeénech, A.; Derenaáandez-Garayzábal, J.F.; Pascual, C.; Garcia, J.A.; Cutuli, M.T.; Moreno, M.A.; Collins, M.D.; Dominguez, L. Streptococcosis in cultured turbot, Scopthalmus maximus (L.), associated with Streptococcus parauberis. Journal of Fish Diseases 1996, 19, 33–38. [Google Scholar] [CrossRef]
  32. Al Bulushi, I.M.; Poole, S.E.; Barlow, R.; Deeth, H.C.; Dykes, G.A. Speciation of Gram-positive bacteria in fresh and ambient-stored sub-tropical marine fish. International Journal of Food Microbiology 2010, 138, 32–38. [Google Scholar] [CrossRef] [PubMed]
  33. Currás, M.; Magariños, B.; Toranzo, A.E.; Romalde, J.L. Dormancy as a survival strategy of the fish pathogen Streptococcus parauberis in the marine environment. Diseases of Aquatic Organisms 2002, 52, 129–136. [Google Scholar] [CrossRef] [PubMed]
  34. Leigh, J.A. Streptococcus uberis: A Permanent Barrier to the Control of Bovine Mastitis? The Veterinary Journal 1999, 157, 225–238. [Google Scholar] [CrossRef] [PubMed]
  35. Di Domenico, E.G.; Toma, L.; Prignano, G.; Pelagalli, L.; Police, A.; Cavallotti, C.; Torelli, R.; Sanguinetti, M.; Ensoli, F. Misidentification of Streptococcus uberis as a Human Pathogen: A Case Report and Literature Review. International Journal of Infectious Diseases 2015, 33, 79–81. [Google Scholar] [CrossRef]
  36. Huan, S.J.K.W.; Tan, J.S.W.; Chin, A.Y.H. Streptococcus parauberis infection of the hand. Journal of Hand Surgery (European Volume) 2021, 46, 83–84. [Google Scholar] [CrossRef]
  37. Zaman, K.; Thakur, A.; Sree, V.; Kaushik, S.; Gautam, V.; Ray, P. Post-traumatic endophthalmitis caused by Streptococcus parauberis: First human. Indian Journal of Medical Microbiology 2016, 34, 382–384. [Google Scholar] [CrossRef]
  38. Klijn, N.; Weerkamp, A.H.; Vos, W.M.d. Detection and characterization of lactose-utilizing Lactococcus spp. in natural ecosystems. Applied and Environmental Microbiology 1995, 61, 788–792. [Google Scholar] [CrossRef]
  39. Flórez, A.B.; Mayo, B. Microbial diversity and succession during the manufacture and ripening of traditional, Spanish, blue-veined Cabrales cheese, as determined by PCR-DGGE. International Journal of Food Microbiology 2006, 110, 165–171. [Google Scholar] [CrossRef]
  40. Edalatian, M.R.; Najafi, M.B.H.; Mortazavi, S.A.; Alegría, Á.; Nassiri, M.R.; Bassami, M.R.; Mayo, B. Microbial diversity of the traditional Iranian cheeses Lighvan and Koozeh, as revealed by polyphasic culturing and culture-independent approaches. Dairy Science & Technology 2012, 92, 75–90. [Google Scholar] [CrossRef]
  41. Fuka, M.M.; Wallisch, S.; Engel, M.; Welzl, G.; Havranek, J.; Schloter, M. Dynamics of Bacterial Communities during the Ripening Process of Different Croatian Cheese Types Derived from Raw Ewe’s Milk Cheeses. PLOS ONE 2013, 8, e80734. [Google Scholar] [CrossRef]
  42. Mangia, N.P.; Fancello, F.; Deiana, P. Microbiological characterization using combined culture dependent and independent approaches of Casizolu pasta filata cheese. Journal of Applied Microbiology 2016, 120, 329–345. [Google Scholar] [CrossRef] [PubMed]
  43. Fusco, V.; Quero, G.M.; Poltronieri, P.; Morea, M.; Baruzzi, F. Autochthonous and Probiotic Lactic Acid Bacteria Employed for Production of “Advanced Traditional Cheeses”. Foods 2019, 8, 412. [Google Scholar] [CrossRef] [PubMed]
  44. France, T.C.; O’Mahony, J.A.; Kelly, A.L. The Plasmin System in Milk and Dairy Products. In Agents of Change: Enzymes in Milk and Dairy Products; Kelly, A.L., Larsen, L.B., Eds.; Springer International Publishing: Cham, 2021; pp. 11–55. [Google Scholar] [CrossRef]
  45. Aminifar, M.; Hamedi, M.; Emam-Djomeh, Z.; Mehdinia, A. Investigation on proteolysis and formation of volatile compounds of Lighvan cheese during ripening. Journal of Food Science and Technology 2014, 51, 2454–2462. [Google Scholar] [CrossRef] [PubMed]
  46. Dan, T.; Wang, D.; Wu, S.; Jin, R.; Ren, W.; Sun, T. Profiles of Volatile Flavor Compounds in Milk Fermented with Different Proportional Combinations of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus. Molecules 2017, 22, 1633. [Google Scholar] [PubMed]
  47. Yang, C.; Zhao, F.; Hou, Q.; Wang, J.; Li, M.; Sun, Z. PacBio sequencing reveals bacterial community diversity in cheeses collected from different regions. Journal of Dairy Science 2020, 103, 1238–1249. [Google Scholar] [CrossRef]
  48. Tulini, F.L.; Hymery, N.; Haertlé, T.; Le Blay, G.; De Martinis, E.C.P. Screening for antimicrobial and proteolytic activities of lactic acid bacteria isolated from cow, buffalo and goat milk and cheeses marketed in the southeast region of Brazil. Journal of Dairy Research 2016, 83, 115–124. [Google Scholar] [CrossRef]
  49. Muruzović, M.Ž.M.; Katarina, G.; Žugić-Petrović, T.D.; Čomić, L.R. In vitro evaluation of the antimicrobial potential of Streptococcus uberis isolated from a local cheese from Southeastern Serbia. Veterinarski Arhiv 2018, 88, 521–534. [Google Scholar] [CrossRef]
  50. Collins, M.D.; Samelis, J.; Metaxopoulos, J.; Wallbanks, S. Taxonomic studies on some leuconostoc-like organisms from fermented sausages: description of a new genus Weissella for the Leuconostoc paramesenteroides group of species. Journal of Applied Bacteriology 1993, 75, 595–603. [Google Scholar] [CrossRef]
  51. Abriouel, H.; Lerma, L.L.; Casado Muñoz, M.d.C.; Montoro, B.P.; Kabisch, J.; Pichner, R.; Cho, G.-S.; Neve, H.; Fusco, V.; Franz, C.M.A.P. , et al. The controversial nature of the Weissella genus: technological and functional aspects versus whole genome analysis-based pathogenic potential for their application in food and health. Frontiers in Microbiology 2015, 6. [Google Scholar] [CrossRef]
  52. Olano, A.; Chua, J.; Schroeder, S.; Minari, A.; Salvia, M.L.; Hall, G. Weissella confusa</i> (Basonym:Lactobacillus confusus</i>) Bacteremia: a Case Report. Journal of Clinical Microbiology 2001, 39, 1604–1607. [Google Scholar] [CrossRef]
  53. Flaherty, J.D.; Levett, P.N.; Dewhirst, F.E.; Troe, T.E.; Warren, J.R.; Johnson, S. Fatal Case of Endocarditis Due to Weissella confusa. Journal of Clinical Microbiology 2003, 41, 2237–2239. [Google Scholar] [CrossRef] [PubMed]
  54. Vela, A.I.; Porrero, C.; Goyache, J.; Nieto, A.; Sánchez, B.; Briones, V.; Moreno, M.A.; Domínguez, L.; Fernández-Garayzábal, J.F. Weissella confusa infection in primate (Cercopithecus mona). Emerg Infect Dis 2003, 9, 1307–1309. [Google Scholar] [CrossRef] [PubMed]
  55. Nam, H.; Ha, M.; Bae, O.; Lee, Y. Effect of Weissella confusa Strain PL9001 on the Adherence and Growth of Helicobacter pylori. Applied and Environmental Microbiology 2002, 68, 4642–4645. [Google Scholar] [CrossRef]
  56. Teixeira, C.G.; Fusieger, A.; Martins, E.; Freitas, R.d.; Vakarelova, M.; Nero, L.A.; Carvalho, A.F.d. Biodiversity and technological features of Weissella isolates obtained from Brazilian artisanal cheese-producing regions. LWT 2021, 147, 111474. [Google Scholar] [CrossRef]
  57. Kumari, M.; Kumar, R.; Singh, D.; Bhatt, S.; Gupta, M. Physiological and genomic characterization of an exopolysaccharide-producing Weissella cibaria CH2 from cheese of the western Himalayas. Food Bioscience 2020, 35, 100570. [Google Scholar] [CrossRef]
  58. Fusco, V.; Quero, G.M.; Cho, G.-S.; Kabisch, J.; Meske, D.; Neve, H.; Bockelmann, W.; Franz, C.M.A.P. The genus Weissella: taxonomy, ecology and biotechnological potential. Frontiers in Microbiology 2015, 6. [Google Scholar] [CrossRef]
  59. Björkroth, K.J.; Schillinger, U.; Geisen, R.; Weiss, N.; Hoste, B.; Holzapfel, W.H.; Korkeala, H.J.; Vandamme, P. Taxonomic study of Weissella confusa and description of Weissella cibaria sp. nov., detected in food and clinical samples. International Journal of Systematic and Evolutionary Microbiology 2002, 52, 141–148. [Google Scholar] [CrossRef]
  60. Jang, H.-J.; Kang, M.-S.; Yi, S.-H.; Hong, J.-Y.; Hong, S.-P. Comparative Study on the Characteristics of Weissella cibaria CMU and Probiotic Strains for Oral Care. Molecules 2016, 21, 1752. [Google Scholar] [CrossRef]
  61. Yu, H.-S.; Lee, N.-K.; Choi, A.-J.; Choe, J.-S.; Bae, C.H.; Paik, H.-D. Antagonistic and antioxidant effect of probiotic Weissella cibaria JW15. Food Science and Biotechnology 2019, 28, 851–855. [Google Scholar] [CrossRef]
  62. Masoud, W.; Vogensen, F.K.; Lillevang, S.; Abu Al-Soud, W.; Sørensen, S.J.; Jakobsen, M. The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR. International Journal of Food Microbiology 2012, 153, 192–202. [Google Scholar] [CrossRef]
  63. Morea, M.; Baruzzi, F.; Cappa, F.; Cocconcelli, P.S. Molecular characterization of the Lactobacillus community in traditional processing of Mozzarella cheese. International Journal of Food Microbiology 1998, 43, 53–60. [Google Scholar] [CrossRef] [PubMed]
  64. Escobar-Zepeda, A.; Sanchez-Flores, A.; Quirasco Baruch, M. Metagenomic analysis of a Mexican ripened cheese reveals a unique complex microbiota. Food Microbiology 2016, 57, 116–127. [Google Scholar] [CrossRef] [PubMed]
  65. Cibik, R.; Lepage, E.; Tailliez, P. Molecular Diversity of Leuconostoc mesenteroides and Leuconostoc citreumIsolated from Traditional French Cheeses as Revealed by RAPD Fingerprinting, 16S rDNA Sequencing and 16S rDNA Fragment Amplification. Systematic and Applied Microbiology 2000, 23, 267–278. [Google Scholar] [CrossRef] [PubMed]
  66. Londoño-Zapata, A.F.; Durango-Zuleta, M.M.; Sepúlveda-Valencia, J.U.; Moreno Herrera, C.X. Characterization of lactic acid bacterial communities associated with a traditional Colombian cheese: Double cream cheese. LWT - Food Science and Technology 2017, 82, 39–48. [Google Scholar] [CrossRef]
  67. Gerasi, E.; Litopoulou-Tzanetaki, E.; Tzanetakis, N. Microbiological study of Manura, a hard cheese made from raw ovine milk in the Greek island Sifnos. International Journal of Dairy Technology 2003, 56, 117–122. [Google Scholar] [CrossRef]
  68. Ercan, D.; Korel, F.; Orşahin, H. Microbiological quality of artisanal Sepet cheese. International Journal of Dairy Technology 2014, 67, 384–393. [Google Scholar] [CrossRef]
  69. Li, J.; Huang, Q.; Zheng, X.; Ge, Z.; Lin, K.; Zhang, D.; Chen, Y.; Wang, B.; Shi, X. Investigation of the Lactic Acid Bacteria in Kazak Cheese and Their Contributions to Cheese Fermentation. Frontiers in Microbiology 2020, 11. [Google Scholar] [CrossRef]
  70. Malaka, R.; Laga, A.; Ako, A.; Zakariah, M.; Mauliah, F.U. Quality and storage time of traditional dangke cheese inoculated with indigenous lactic acid bacteria isolated from Enrekang District, South Sulawesi, Indonesia. Biodiversitas Journal of Biological Diversity 2022, 23. [Google Scholar]
  71. Aboubacar, M.R.M.; Owino, W.; Mbogo, K. Characterization and antibiotic profiles of lactic acid bacteria isolated from “tchoukou” traditional milk cheeses produced in the Zinder region of Niger Republic, West Africa.
  72. Lynch, K.M.; McSweeney, P.L.H.; Arendt, E.K.; Uniacke-Lowe, T.; Galle, S.; Coffey, A. Isolation and characterisation of exopolysaccharide-producing Weissella and Lactobacillus and their application as adjunct cultures in Cheddar cheese. International Dairy Journal 2014, 34, 125–134. [Google Scholar] [CrossRef]
  73. Kariyawasam, K.M.G.M.M.; Jeewanthi, R.K.C.; Lee, N.K.; Paik, H.D. Characterization of cottage cheese using Weissella cibaria D30: Physicochemical, antioxidant, and antilisterial properties. Journal of Dairy Science 2019, 102, 3887–3893. [Google Scholar] [CrossRef]
  74. Teixeira, C.G.; Fusieger, A.; Milião, G.L.; Martins, E.; Drider, D.; Nero, L.A.; de Carvalho, A.F. Weissella: An Emerging Bacterium with Promising Health Benefits. Probiotics and Antimicrobial Proteins 2021, 13, 915–925. [Google Scholar] [CrossRef]
  75. Teixeira, C.G.; Silva, R.R.d.; Fusieger, A.; Martins, E.; Freitas, R.d.; Carvalho, A.F.d. The Weissella genus in the food industry: A review. Research, Society and Development 2021, 10, e8310514557. [Google Scholar] [CrossRef]
  76. Lynch, K.M.; Lucid, A.; Arendt, E.K.; Sleator, R.D.; Lucey, B.; Coffey, A. Genomics of Weissella cibaria with an examination of its metabolic traits. Microbiology 2015, 161, 914–930. [Google Scholar] [CrossRef] [PubMed]
  77. Kavitake, D.; Devi, P.B.; Shetty, P.H. Overview of exopolysaccharides produced by Weissella genus – A review. International Journal of Biological Macromolecules 2020, 164, 2964–2973. [Google Scholar] [CrossRef] [PubMed]
  78. Benhouna, I.S.; Heumann, A.; Rieu, A.; Guzzo, J.; Kihal, M.; Bettache, G.; Champion, D.; Coelho, C.; Weidmann, S. Exopolysaccharide produced by Weissella confusa: Chemical characterisation, rheology and bioactivity. International Dairy Journal 2019, 90, 88–94. [Google Scholar] [CrossRef]
  79. Teixeira, C.G.; Rodrigues, R.d.S.; Yamatogi, R.S.; Lucau-Danila, A.; Drider, D.; Nero, L.A.; de Carvalho, A.F. Genomic Analyses of Weissella cibaria W25, a Potential Bacteriocin-Producing Strain Isolated from Pasture in Campos das Vertentes, Minas Gerais, Brazil. Microorganisms 2022, 10, 314. [Google Scholar] [CrossRef]
  80. Apostolakos, I.; Paramithiotis, S.; Mataragas, M. Functional and Safety Characterization of Weissella paramesenteroides Strains Isolated from Dairy Products through Whole-Genome Sequencing and Comparative Genomics. Dairy 2022, 3, 799–813. [Google Scholar] [CrossRef]
  81. Ndagano, D.; Lamoureux, T.; Dortu, C.; Vandermoten, S.; Thonart, P. Antifungal Activity of 2 Lactic Acid Bacteria of the Weissella Genus Isolated from Food. Journal of Food Science 2011, 76, M305–M311. [Google Scholar] [CrossRef]
  82. Valerio, F.; Favilla, M.; De Bellis, P.; Sisto, A.; de Candia, S.; Lavermicocca, P. Antifungal activity of strains of lactic acid bacteria isolated from a semolina ecosystem against Penicillium roqueforti, Aspergillus niger and Endomyces fibuliger contaminating bakery products. Systematic and Applied Microbiology 2009, 32, 438–448. [Google Scholar] [CrossRef]
  83. Kwak, S.H.; Cho, Y.M.; Noh, G.M.; Om, A.S. Cancer Preventive Potential of Kimchi Lactic Acid Bacteria (Weissella cibaria, Lactobacillus plantarum). J Cancer Prev 2014, 19, 253–258. [Google Scholar] [CrossRef]
  84. Su-Bin, A.; Ho-Eun, P.; Sang-Myeong, L.; So-Young, K.; Mi-Yae, S.; Wan-Kyu, L. Characteristics and immuno-modulatory effects of Weissella cibaria JW15 isolated from Kimchi, Korea traditional fermented food, for probiotic use. Journal of Biomedical Research 2013, 14, 206–211. [Google Scholar]
  85. Quattrini, M.; Korcari, D.; Ricci, G.; Fortina, M.G. A polyphasic approach to characterize Weissella cibaria and Weissella confusa strains. Journal of Applied Microbiology 2020, 128, 500–512. [Google Scholar] [CrossRef] [PubMed]
  86. Patel, S.; Mathivanan, N.; Goyal, A. Bacterial adhesins, the pathogenic weapons to trick host defense arsenal. Biomedicine & Pharmacotherapy 2017, 93, 763–771. [Google Scholar] [CrossRef]
  87. Wang, L.; Si, W.; Xue, H.; Zhao, X. A fibronectin-binding protein (FbpA) of Weissella cibaria inhibits colonization and infection of Staphylococcus aureus in mammary glands. Cellular Microbiology 2017, 19, e12731. [Google Scholar] [CrossRef] [PubMed]
  88. Heo, S.; Lee, J.-H.; Jeong, D.-W. Food-derived coagulase-negative Staphylococcus as starter cultures for fermented foods. Food Science and Biotechnology 2020, 29, 1023–1035. [Google Scholar] [CrossRef] [PubMed]
  89. Kloos, W.E.; Schleifer, K.H.; Smith, R.F. Characterization of Staphylococcus sciuri sp.nov. and Its Subspecies1. International Journal of Systematic and Evolutionary Microbiology 1976, 26, 22–37. [Google Scholar] [CrossRef]
  90. Madhaiyan, M.; Wirth, J.S.; Saravanan, V.S. Phylogenomic analyses of the Staphylococcaceae family suggest the reclassification of five species within the genus Staphylococcus as heterotypic synonyms, the promotion of five subspecies to novel species, the taxonomic reassignment of five Staphylococcus species to Mammaliicoccus gen. nov., and the formal assignment of Nosocomiicoccus to the family Staphylococcaceae. International Journal of Systematic and Evolutionary Microbiology 2020, 70, 5926–5936. [Google Scholar] [CrossRef]
  91. Shittu, A.; Lin, J.; Morrison, D.; Kolawole, D. Isolation and molecular characterization of multiresistant Staphylococcus sciuri and Staphylococcus haemolyticus associated with skin and soft-tissue infections. Journal of Medical Microbiology 2004, 53, 51–55. [Google Scholar] [CrossRef]
  92. Stepanović, S.; Dakić, I.; Morrison, D.; Hauschild, T.; Ježek, P.; Petráš, P.; Martel, A.; Vuković, D.; Shittu, A.; Devriese, L.A. Identification and Characterization of Clinical Isolates of Members of the <i>Staphylococcus sciuri</i> Group. Journal of Clinical Microbiology 2005, 43, 956–958. [Google Scholar] [CrossRef]
  93. Hedin, G.; Widerström, M. Endocarditis due toStaphylococcus sciuri. European Journal of Clinical Microbiology and Infectious Diseases 1998, 17, 673–675. [Google Scholar] [CrossRef]
  94. Toshinobu Horii, Y.S.T.K.T.K.M.M. Intravenous Catheter-related Septic Shock Caused by Staphylococcus sciuri and Escherichia vulneris. Scandinavian Journal of Infectious Diseases 2001, 33, 930–932. [Google Scholar] [CrossRef] [PubMed]
  95. Sands, K.; Carvalho, M.J.; Spiller, O.B.; Portal, E.A.R.; Thomson, K.; Watkins, W.J.; Mathias, J.; Dyer, C.; Akpulu, C.; Andrews, R. , et al. Characterisation of Staphylococci species from neonatal blood cultures in low- and middle-income countries. BMC Infectious Diseases 2022, 22, 593. [Google Scholar] [CrossRef]
  96. Benz, M.S.; Scott, I.U.; Flynn, H.W.; Unonius, N.; Miller, D. Endophthalmitis isolates and antibiotic sensitivities: a 6-year review of culture-proven cases. American Journal of Ophthalmology 2004, 137, 38–42. [Google Scholar] [CrossRef]
  97. Frederic Wallet, L.S.E.B.M.R.-D.P.D.R.J.C. Peritonitis Due to Staphylococcus sciuri in a Patient on Continuous Ambulatory Peritoneal Dialysis. Scandinavian Journal of Infectious Diseases 2000, 32, 697–698. [Google Scholar] [CrossRef] [PubMed]
  98. Stepanović, S.; Ježek, P.; Dakić, I.; Vuković, D.; Seifert, L. Staphylococcus sciuri: an unusual cause of pelvic inflammatory disease. International Journal of STD & AIDS 2005, 16, 452–453. [Google Scholar] [CrossRef]
  99. Devriese, L.A. Staphylococci in healthy and diseased animals. Journal of Applied Bacteriology 1990, 69, 71S–80S. [Google Scholar] [CrossRef]
  100. Nemeghaire, S.; Argudín, M.A.; Feßler, A.T.; Hauschild, T.; Schwarz, S.; Butaye, P. The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Veterinary Microbiology 2014, 171, 342–356. [Google Scholar] [CrossRef]
  101. Nemeghaire, S.; Vanderhaeghen, W.; Argudín, M.A.; Haesebrouck, F.; Butaye, P. Characterization of methicillin-resistant Staphylococcus sciuri isolates from industrially raised pigs, cattle and broiler chickens. Journal of Antimicrobial Chemotherapy 2014, 69, 2928–2934. [Google Scholar] [CrossRef]
  102. Rahman, M.T.; Kobayashi, N.; Alam, M.M.; Ishino, M. Genetic analysis of mecA homologues in Staphylococcus sciuri strains derived from mastitis in dairy cattle. Microbial drug resistance 2005, 11, 205–214. [Google Scholar] [CrossRef]
  103. Chen, S.; Wang, Y.; Chen, F.; Yang, H.; Gan, M.; Zheng, S.J. A Highly Pathogenic Strain of Staphylococcus sciuri Caused Fatal Exudative Epidermitis in Piglets. PLOS ONE 2007, 2, e147. [Google Scholar] [CrossRef]
  104. Adegoke, G.O. Comparative characteristics of Staphylococcus sciuri, Staphylococcus lentus and Staphylococcus gallinarum isolated from healthy and sick hosts. Veterinary Microbiology 1986, 11, 185–189. [Google Scholar] [CrossRef] [PubMed]
  105. Sacramento, A.G.; Fuga, B.; Monte, D.F.M.; Cardoso, B.; Esposito, F.; Dolabella, S.S.; Barbosa, A.A.T.; Zanella, R.C.; Cortopassi, S.R.G.; da Silva, L.C.B.A. , et al. Genomic features of mecA-positive methicillin-resistant Mammaliicoccus sciuri causing fatal infections in pets admitted to a veterinary intensive care unit. Microbial Pathogenesis 2022, 171, 105733. [Google Scholar] [CrossRef] [PubMed]
  106. Irlinger, F.; Morvan, A.; El Solh, N.; Bergere, J.L. Taxonomic Characterization of Coagulase-Negative Staphylococci in Ripening Flora from Traditional French Cheeses. Systematic and Applied Microbiology 1997, 20, 319–328. [Google Scholar] [CrossRef]
  107. Klempt, M.; Franz, C.M.A.P.; Hammer, P. Characterization of coagulase-negative staphylococci and macrococci isolated from cheese in Germany. Journal of Dairy Science 2022, 105, 7951–7958. [Google Scholar] [CrossRef] [PubMed]
  108. Van der Veken, D.; Leroy, F. Prospects for the applicability of coagulase-negative cocci in fermented-meat products using omics approaches. Current Opinion in Food Science 2022, 48, 100918. [Google Scholar] [CrossRef]
  109. Charmpi, C.; Thamsborg, K.K.M.; Mikalsen, S.-O.; Magnussen, E.; Sosa Fajardo, A.; Van der Veken, D.; Leisner, J.J.; Leroy, F. Bacterial species diversity of traditionally ripened sheep legs from the Faroe Islands (skerpikjøt). International Journal of Food Microbiology 2023, 386, 110023. [Google Scholar] [CrossRef] [PubMed]
  110. Endres, C.M.; Moreira, E.; de Freitas, A.B.; Castel, A.P.D.; Graciano, F.; Mann, M.B.; Frazzon, A.P.G.; Mayer, F.Q.; Frazzon, J. Evaluation of Enterotoxins and Antimicrobial Resistance in Microorganisms Isolated from Raw Sheep Milk and Cheese: Ensuring the Microbiological Safety of These Products in Southern Brazil. Microorganisms 2023, 11, 1618. [Google Scholar] [CrossRef]
  111. Esen, Y.; Çetin, B. Bacterial and yeast microbial diversity of the ripened traditional middle east surk cheese. International Dairy Journal 2021, 117, 105004. [Google Scholar] [CrossRef]
  112. Bockelmann, W. Development of defined surface starter cultures for the ripening of smear cheeses. International Dairy Journal 2002, 12, 123–131. [Google Scholar] [CrossRef]
  113. Naqqash, T.; Wazir, N.; Aslam, K.; Shabir, G.; Tahir, M.; Shaikh, R.S. First report on the probiotic potential of Mammaliicoccus sciuri isolated from raw goat milk. Bioscience of Microbiota, Food and Health 2022, 41, 149–159. [Google Scholar] [CrossRef]
  114. Veken, D.V.d.; Hollanders, C.; Verce, M.; Michiels, C.; Ballet, S.; Weckx, S.; Leroy, F. Genome-Based Characterization of a Plasmid-Associated Micrococcin P1 Biosynthetic Gene Cluster and Virulence Factors in Mammaliicoccus sciuri IMDO-S72. Applied and Environmental Microbiology 2022, 88, e02088–e02021. [Google Scholar] [CrossRef] [PubMed]
Table 1. Some examples of NSLAB with controversial nature participating in cheese ripening.
Table 1. Some examples of NSLAB with controversial nature participating in cheese ripening.
Genus Species Some examples of cheeses References
Lactococcus Lc. garvieae Italian mozzarella cheeses
Italian Toma Piemontese cheese
Spanish Casín cheese
Spanish “Torta del Casar” cheese
Slovakian May bryndza cheese
Azorean Pico cheese
Montenegrian brine cheeses
Bulgarian and Turkish Tulum cheeses
Bulgarian “Green” cheese
Bulgarian Krokmach cheese
[7,8]
[9]
[10]
[11]
[12]
[13]
[14]
[15,16]
[17]
[18]
Streptococcus Str. uberis Italian Mozzarella cheese
Spanish Casín cheese
Italian Casizolu cheese
[8]
[10]
[42]
Str. parauberis Spanish Cabrales cheese
Spanish Casín cheese
Iranian Lighvan and Koozeh cheese
Slovenian raw milk cheeses
Slovakian May bryndza cheese
Italian Casizolu cheeseItalian Giuncata cheese
Italian Caciotta Leccese cheese
Bulgarian and Turkish Tulum cheeses
[39]
[10]
[40]
[41]
[12]
[42]
[43]
[43]
[15,16]
Weissella W. hellenica Danish raw milk cheeses
a type of Croatian cheese
Brazilian artisanal cheeses
Italian Mozzarella cheese
[62]
[41]
[56]
[63]
W. confusa Turkish Sepet cheese
a type of Kazak cheese
a type of Indonesian cheese
[68]
[69]
[70]
W. paramesenteroides a type of Mexican ripened cheese
some traditional French cheeses
Columbian double cream cheese
Greek Manura cheese
Turkish Sepet cheese
[64]
[65]
[66]
[67]
[68]
W. cibaria Afrikan Tchoukou cheese
Western Himalayan cheese
[71]
[57]
Mammalicoccus M. sciuri French smear cheeses
some German cheeses
some Brazilian cheeses
Middle East Surk cheese
[106]
[107]
[110]
[111]
Table 2. Examples of pathogenicity of the bacteria investigated in this study.
Table 2. Examples of pathogenicity of the bacteria investigated in this study.
diseased Pathogenicity References
Lc. garvieae fish lactococcosis
bovine mastitis
endocarditis in immunocompromised and old persons
[2]
[3]
[4]
Str. uberis bovine mastitis
occasional human infections
[29]
[35]
Str. parauberis bovine mastitis
fish pathogen
rare cases of infection in humans
[30]
[31]
[36,37]
W. hellenica no records
W. confusa bacteremia
endocarditis
deadly infections in primates
[52]
[53]
[54]
W. paramesenteroides no records
W. cibaria bacteremias in humans
otitis in dogs
[58]
[59]
M. sciuri human wound infections
urinary tract infections
endocarditis in humans
sepsis in humans
endophtalmitis in humans
peroitonitis in humans
plevric inflammatory disease in humans
mastitis in cows and goats
epidermitis in piglets
presence in ovine rinderpest suffering animals
respiratory distress syndrome in cats and dogs
[91]
[92]
[93]
[94,95]
[96]
[97]
[98]
[99,102]
[103]
[104]
[105]
Table 3. Contribution to the ripening and health-promoting effects of the NSLAB investigated in this study.
Table 3. Contribution to the ripening and health-promoting effects of the NSLAB investigated in this study.
Species Contribution to the ripening References Health-promoting and probiotic effects References
Lc. garvieae palatability
sensorial characteristics
lactose fermentationaroma
[19]
[20]
[20]
[21]
inhibition of pathogens [11,22,23,24,25]
Str. uberis streptokinase induced proteolysis [44] inhibition of pathogens [48,59]
Str. parauberis streptokinase induced proteolysis
organoleptic properties
[45]
[47]
Weissella spp. contribution to the rheological properties by EPS production
coagulation of the milk proteins
organoleptic properties
[57,75]
[56,76]
[56,72]
synthesis of EPS
bacteriocins production
hydrogen peroxide production
inhibition of H. pylori
antifungal activities
chemopreventive effects
anti-obesity effects
antiviral activity
[51,57,74,75,77,78]
[74,79,80]
[51,60]
[55]
[81,82]
[83]
[84]
[51]
M. sciuri organoleptic properties [88,108,112] no definitive data
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