You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Dairy Spoilage and Pseudomonas spp.
Edit
This entry is adapted from the peer-reviewed paper 10.3390/foods10123088

The refrigerated fresh foods tend to quickly deteriorate along its production and marketing, mainly due to the action of psychrotrophic spoilage microorganisms such as pseudomonads. These bacteria cause discolouration, texture loss and unpleasant flavours, with fatal implications for the quality and shelf life of products. Refirgerated fresh dairy products as well as fresh foods are steadly threatened by these microorganisms against which most control strategies are uneffective.

pseudomonads dairy products spoilage traits biofilm quorum sensing metabolic pathways QS inhibitors

1. Introduction

The increasing global population has contributed to making food insecurity one of the global challenges; in fact, more than 820 million people in the world suffer food scarcity [1], which negatively impacts mental, social, and physical well-being [2]. This crucial issue has been further worsened by the COVID-19 pandemic [3]. Thus, in response to the urgent and increasing global demand for food, several strategies and measures have been proposed by the official authorities [4]; some of these are aimed at reducing food losses and waste at different stages of the food production and supply chains, including the prevention of food loss during processing, the transformation of perishable raw materials into shelf-stable products, the extension of the shelf-life through packaging and processing innovation, the introduction of clear date labels or storage, and the prevention of food spoilage [5]. Spoilage is a deterioration process caused by microbiological, chemical, and physical changes that makes the food product unacceptable for the consumer and causes significant economic losses for the food industry.
In the dairy sector, the application of low temperatures has allowed the extension of the shelf-life and marketing of various fresh dairy products. However, naturally occurring bacteria, such as pseudomonads, have increasingly become a real concern for cold-stored fresh dairy products because of their ability to grow and adapt themselves to low temperatures. They are responsible for visible spoilage traits (discolorations, structure loss, rheology changes) and non-visible defects (protein breakdown, off-odours, and off-flavours), which significantly reduce the quality and shelf-life of dairy products.
Pseudomonas spp. contamination routes have been largely studied, especially for milk or milk-based beverages [6][7]. In contrast, how these bacteria manage to contaminate cheeses even made from pasteurized milk is still much debated. Since these are environmental microorganisms generally present in the soil, the main sources of contamination are surfaces, water, and obviously, exposure to air. Pseudomonads contamination occurs at each step of the manufacturing process of dairy products and it becomes more persistent and resistant to sanification procedures when bacterial cells grow as biofilm [8]. In addition, increasing amounts of enzymes (proteases and lipases) and the activation of metabolic pathways correlated to spoilage traits (e.g., pigments biosynthesis) have been found in biofilm rather than in the fluctuating state [9]. Regardless of this evidence, the mechanisms responsible for the production and the activation of spoilage enzymes, metabolites, and pathways are still poorly explored. Most of them are quorum sensing (QS) regulated, suggesting its potential role in dairy spoilage [10][11][12]. To confirm this, different molecule signals have been detected in spoiled products, where they affect microbial biodiversity and metabolic activities [13][14]. Thus, the most recent and innovative preservation strategies aim to intercept and inhibit this communication system, rather than to exert antimicrobial activity [12][15]. However, to the best of researchers' knowledge, studies based on the application of QS inhibitors (QSI) to improve the shelf-life of dairy products are performed sporadically [16][17], and most in vitro and in situ studies are focused on pseudomonads isolated from fish [18][19][20]. This knowledge gap highlights the need to explore more deeply the metabolic activities and their regulation of dairy spoilage; this in order to identify the specific markers or novel molecular targets to apply in innovative control strategies, and in so doing reducing food losses and waste in the dairy sector.

2. Pseudomonas spp. as Major Cause of Spoilage in Dairy Chain

Due to their metabolic versatility and adaptation, Pseudomonas spp. are widely occurring in dairy products. Although they optimally grow at higher temperatures, some pseudomonad species are also favoured by refrigeration temperatures of fresh foods due to their ability to increase the proportion of unsaturated fatty acids in the lipid phase of their membranes, making them more fluid [21]. This dual ability enables these bacteria to better compete with the natural microbiota of cold-stored fresh foods, and even adapt themselves under inappropriate storage conditions. Unlike other psychrotrophs, pseudomonads show a generation time at 0–7 °C shorter than at the optimal growth temperature [22]. With regard to their need for oxygen, they can grow even in anoxic atmospheres with high percentages of CO2 [23]. Due to the high content of nutritional compounds and water and pH neutrality, milk and fresh dairy products are optimal matrices for pseudomonads. The spoilage traits strictly depend on species, food characteristics, storage conditions, and adaptation ability [24]; indeed, Pseudomonas species grow and become dominant thanks to the expression of a number of determinants (such as enzymes, pigments) addressed to enhance competition and adaptation of the bacteria. In this regard, Table 1 and Figure 1 show some of the spoilage traits caused by Pseudomonas spp. in dairy products under cold-storage conditions, which are better described in the following sections.
Foods 10 03088 g001 550
Figure 1. Spoilage traits in dairy products under cold storage conditions: (A) discolorations of dairy products contaminated by Pseudomonas spp.; (B) proteolysis of HM Mozzarella cheeses inoculated with P. fluorescens strains (Quintieri L., Caputo L., Brasca M., Fanelli F., unpublished).
Table 1. Spoilage traits on dairy products by Pseudomonas spp.
Table
 

Proteolysis

      

Milk creaming, sediment formation, gelation, bitterness

 P. fluorescens,
P. weihenstephanensis,
P. proteolytica,
Pseudomonas spp.		 UHT milk [25][26][27]
P. panacis Skimmed milk [28]
P. azotoformans Raw milk [29][30]
P. gessardii Milk [26][31]
P. proteolytica
P. fluorescens Unpasteurized goat milk [32]
Pseudomonas spp. Non-bovine raw milk [33]

Bitterness, Mozzarella skin wrinkling/peeling, cheese softness, sediment formation

 P. lundensis,
P gessardii		 Mozzarella cheese, skimmed milk [31]
P. fluorescens Crescenza cheese [34]
P. fluorescens,
P. fragi		 Mozzarella cheese [31]
P. fluorescens,
P. putida		 Cheddar cheese [25]

Discoloration

      

Blue

 P. fluorescens,
P. lactis		 Mozzarella cheese [8][35]
P. fluorescens Latin-style fresh cheeses [36][37]
P. carnis,
Pseudomonas spp.		 Brazilian fresh soft cheese [38]
P. fluorescens Mozzarella processing fluids [39]

Orange or

Orange-red-brown

 P. aureofaciens,
P. gessardii,
P. putida biovar II		 Mozzarella cheese [40]

Greenish

 P. fluorescens

Fluorescent

(yellow-green)

 P. fluorescens,
P. putida,
P. palleronii

Grayish

 P. azotoformans HTST milk [41]
  P. fragi Milk [40]

Black

 P. mephitica,
P. nigrifaciens		 Butter [42]

Lipolysis

      

Rancidity

off-flavors

straw-berry flavor bitterness

soapy

 Pseudomonas spp.,
P. fluorescens		 Sterilized milk [43][44][45]
P. fluorescens Ripened semi-hard cheese [46][47]
P. fragi,
P. putrefaciens,
Pseudomonas spp.		 Cream, butter [44][48][49]
Pseudomonas spp. Domiati cheese [50]
Pseudomonas spp. Soft cheese [51]

Modification of rennet coagulation time and curd firmness

 Pseudomonas spp.,
P. fluorescens		 Cheese
Cheddar cheese		 [44][52]

2.1. Spoilage Traits Caused by Proteolytic and Lipolytic Activities

In raw milk, psychrotrophic bacteria, such as P. fluorescens, P. fragi, P. lactis, P. putida, and P. gessardii, are frequent[26][31]. Although these bacteria become inactive after milk pasteurization and sterilization, their extracellular proteases are highly thermostable, and retain the ability to degrade milk proteins, causing bitterness and age gelation in ultra-high temperature (UHT) milk [53]. The proteases released in the milk lead to the extensive breakdown of k-casein to para-k-casein, influencing rennet coagulation [54]. In turn, plasminogen and plasmin are liberated from casein micelles causing additional proteolysis of αS1-αS2-casein and β-casein, affecting milk texture and flavour [55], but even cheese yield [56]. Among the extracellular proteases produced by Pseudomonas, the alkaline zinc metalloprotease AprX retains its activity even after boiling for 10 min, showing a high resistance to heat [57][58].
In fresh cheeses, especially in Mozzarella cheese stored in the governing liquid, the growth of Pseudomonas and other psychrotrophic commensal bacteria are not counteracted by any inhibiting factor; consequently, their proteases have a dramatic impact on protein structure and quality of these cheeses during cold storage [31][59]. In these conditions, the outer part of high moisture Mozzarella cheese inoculated with a spoilage P. fluorescens strain showed a quick hydrolysis of α- and β-caseins and the increase of free amino acid content in governing liquid[60]. Casein loss results in the wrinkling of the Mozzarella skin and in the weakening of its structure, thus the cheese slowly collapses in on itself [31].
The high content of pseudomonads in raw milk and its late pasteurization before production of pickled cheeses, such as Domiati, Feta and Turkish White cheeses, result in huge loss of protein in the brine during storage [50][61]. In turn, catabolism of free amino acids by Pseudomonas strains associated with the dairy environment could fuel several metabolic pathways, among which the production of volatile compounds through transaminases and other hydrolases is detrimental for the quality and shelf-life of fresh cheese [62]. Psychrotrophic pseudomonads also synthesize lipases causing no less serious damage than those produced by proteases [63]; the lipases of psychrotrophic pseudomonads are more active at 4–7 °C than lipases from mesophilic microorganisms and, similar to pseudomonads proteases, show a high stability at temperatures of pasteurization and UHT treatments. Based on these characteristics, the activity of lipases, regardless of the producing strains, can severely damage the quality and shelf-life of especially raw milk as well as high-fat content dairy products during their storage at low temperatures. In fact, they catalyse the hydrolysis of triglycerides to free fatty acids and glycerol [64]. Depending on the length of the fatty acids chain, pseudomonad lipases can lead to the release of C4 and C8 fatty acids associated with rancid flavour and odours; in contrast, free medium-chain fatty acids (C10-C12) produce a soapy flavour. In milk, lipases produced by P. fragi can create strawberry-like odour due to ethyl butyrate and ethyl hexanoate esters [62][65].
Butter is one of the dairy products most sensitive to the activity of lipases and phospholipases by psychrotrophic pseudomonads (P. putrefaciens, P. nigrificans, P. fragi, and P. fluorescens) [61], which can cause a colour change on the surface (surface stain) and rancidity: P. putrefaciens and P. nigrificans are able to grow on the surface of butter and produce a black discoloration and a putrid odour within 7–10 days of storage at refrigeration temperature [42]; a skunk-like smell is also developed in butter by P. mephitica [66], while P. fragi and, rarely, P. fluorescens can turn the butter rancid [48].

2.2. Discoloration as a Spoilage Trait

Among all the spoilage defects recorded on cold-stored dairy products, the one concerning discoloration is certainly the most studied in the last decade. Indeed, several cases of anomalous discoloration on Mozzarella cheese were due to the contamination by P. putida (reddish discoloration [67]), P. fluorescens biovar IV and P. libanensis (bluish discoloration [40]), P. gessardii (yellow and purple spots [40]), and P. fluorescens (greenish and fluorescent discoloration [68]), thanks to the production of different pigments (pyoverdine, pyocyanin, pyorubin, and pyomelanin [69]).
In 2010, starting from the European outbreak reported by RASFF’s (Rapid Alert System for Food and Feed), alerting to hundreds of different Mozzarella cheese lots with blue discoloration [70], the concern related to the risk of coloured taints on cheese surface has grown in importance, mostly for dairy companies that need to prevent or trace these spoilage events [71][72]. A method to screen and counteract the synthesis of blue-pigmenting strains was developed by Caputo et al. [60]; the authors also identified the strain (P. lactis ITEM17298) and pigment (leucoindigoidine that oxides to blue indigoidine) responsible for the cheese defects [60][73][74]. The work of Caputo and colleagues [60] also proved that the entry into the production cycle of pigmenting pseudomonads leads to the appearance of anomalous taints on Mozzarella cheese even after 2 days of storage. The spoiled product was immediately withdrawn from the market in accordance with current legislation, since it negatively impacts the consumer’s choice and compliance with the original characteristics of the product [75].
In milk and fresh cheeses, pseudomonads synthesize and secrete siderophores to overcome iron starvation; these molecules (pyoverdine, pyochelin, pseudomonine, quinolobactin, etc.) work as low-molecular-weight iron chelators causing the appearance of diffusible yellow greenish or fluorescent pigmentation in milk and fresh dairy products [68].

3. QS-Regulated Spoilage Traits in Dairy-Borne Pseudomonas spp.

The advances in technological methodologies used to study the evolution of QS systems in the different growth conditions and time of incubation allowed researchers to shed a light on several spoilage activities in QS-regulated biofilms: several AHLs have been indeed detected in foods spoiled by psychrotrophic bacteria; in addition, AHLs concentration was proved to increase with the degree of food spoilage [13][14]. A deep analysis of the QS spoilage-related genes and pathways is reported below and for P. fluorescens and P. lactis also displayed in Figure 2a,b.
Figure 2. Major spoilage traits regulated by quorum sensing systems reported for (a) P. fluorescens and (b) P. lactis. N-(3-Hydroxybutanoyl)-L-homoserine lactone (C4-HSL); N-hexanoyl-homoserine lactone (C6-HSL); N-3-oxo-octanoyl-L-Homoserine lactone (C8-HSL); N-decanoylhomoserine lactone (C10-AHL); N-dodecanoyl-L-Homoserine lactone (C12-HSL); N-(3-hydroxy-7-cis-tetradecenoyl)-Homoserine lactone (3-OH-C14:1-AHL); 3′,5′ Cyclic diguanylic acid (c-di-GMP); two-component system GacA/two-component system GacS (gacA/gacS); RNA polymerase sigma factor RpoS (RpoS); acyl-homoserine-lactone synthase/transcriptional activator protein PhzR (phzI/phzR); acyl homoserine lactone synthase/LuxR family transcriptional regulator (luxI/luxR); acyl-homoserine-lactone synthase/transcriptional regulatory protein PcoR (pcoI/pcoR); triacylglycerol lipase (lipS); periplasmic serine endoprotease DegP-like (mucD); Metalloprotease AprX (aprX); two-componenent system BarA/UvrY-regulatory subunit (barA/uvrY); acyl-homoserine-lactone synthase esaR (esaR); cyl-homoserine-lactone synthase/transcriptional activator protein LasR (lasI/lasR); acyl-homoserine-lactone synthase/regulatory protein RhlR (rh/I/rh/R); lipoyl synthase (lipA); exopolysaccharide (EPS).

3.1. Proteases, Lipases and Phospholipases

Hydrolytic enzymes are usually produced in the late exponential/early stationary growth phase when the organisms have reached comparatively high cell densities (>106 cfu/mL) and can be released from the biofilms into the milk without bacterial detachment.[76]
Recently, RNA-sequencing was employed to explore the involvement of QS in dairy spoilage caused by P. azotoformans. Fifteen pathways among those analysed were significantly affected by C6-HSL [13]; these latter included cell division, energy metabolism, and nutrient uptake, which are crucial for bacterial survival and adaptation in the food processing environment. Some of the genes upregulated by C6-HSL were elongation factors and sec/yajC/yidC, responsible for protein synthesis and secretion, respectively; the type VI secretion system T4SS used for the transport of proteins and DNA across the cell envelope; and lipS, mucD, and the probable periplasmic serine endoprotease DegP-like (PputW619_1070). In Gram-negative bacteria (e.g., E. coli), DegP serine endoproteases are involved in regulated intramembrane proteolysis (RIP) cleaving transmembrane proteins to liberate a cytosolic domain of proteins able to modify gene transcription, such as the two-component regulatory system CpxA/CpxR, which responds to envelope stress response [77].
In milk, the AHLs signal molecules (C4-HSL and 3OC8-HSL) from Pseudomonas species, such as P. azotoformans, were found to change their particle size distribution, and lead to the destabilization of UHT milk during storage; this feature, as well as off taste and off odour, was putatively attributed to the production of QS-regulated heat-resistant proteases and lipases produced by psychrotrophic bacteria [13][78]. Indeed, AHLs and other AHL-related products from Pseudomonas species have been shown to increase the activity of the aprX promoter; the activity was instead repressed in presence of the enzyme AHL lactonase hydrolysing AHLs [35][57]. Post-transcriptional regulation, under the control of the GacS/GacA two-component regulatory system, was also suggested to take place in the expression and secretion of protease in this system [57]. AprX is mainly secreted by the species P. fluorescens, but it has also been detected in various other species found in raw milk such as P. fragi, P. tolaasii, P. rhodesiae, P. gessardii, P. proteolytica, P. brenneri, or P. chlororaphis. Recently, the genomic analysis of three P. lactis individuals isolated from dairy products identified several protease genes (aprA, prsDE, prtAB), positioned in a QS-regulated operon previously associated with milk spoilage by P. fluorescens [73]; aprA was described as 98% similar to the peptidase aprX [79]. AprA and AprX hydrolyse the four types of casein (αs1, αs2, β, and κ) with a large activity spectrum, and generally exhibit activity in a large range of pH (4.5–10), with optimum activity between 7.5 and 9, as well as across temperatures (0–55 °C), with optimal activity between 37 and 47 °C [80].
Liu et al. [81] reported that the sigma factor RpoS, a positive regulator of two AHL synthase genes and three coding for LuxR-like transcription factors, is a key regulator of spoilage activity by P. fluorescens. Under food-processing conditions (exposure to heat, cold, salt, acid, and preservatives), it positively regulates the extracellular protease activities and the total volatile basic nitrogen production; thus, its monitoring during food processing and storage is considered a useful strategy to ensure the quality and safety of the final food.
In several species of Pseudomonas spp. (e.g., P. fluorescens and P. psychrophila) the production of lipases were regulated by C4-HSLs; these latter increased the proteases and lipases production in pasteurized milk after incubation at 48 °C for 18 h and caused milk spoilage [11]; moreover, the occurrence of AHLs in heat-treated milk demonstrated that they retained all or at least part of their activities, including the modulation of Pseudomonas spp. growth [82].
Few studies report the regulation of lipase genes and include P. aeruginosa; in this strain the expression of the lipase genes was controlled by the RhlR/I system and Gac system [83]. In P. lactis and P. fluorescens [35][79], isolated by dairy products, the activity of lipase included in aprX-lipA operon were by the homologue of the E. coli envZ-ompR affected by environmental osmolarity and regulating biofilm formation [84].
The phospholipase C of P. fluorescens is a heat-stable enzyme, presenting high residual activity after pasteurization and UHT treatment; it is able to hydrolyse intact milk fat globules by increasing the lipase activity. Similar to lipases and proteases, phospholipase C activity is highest in the stationary growth phase and is regulated by the Gac system [85].

3.2. Pigments

Dairy products often appear discoloured due to the biosynthesis of pigments (pyoverdine or fluorescein, pyorubin, pyomelanin, pyocyanin, and indigoidine) by some Pseudomonas species [86]; pigment synthesis is putatively orchestrated to counteract the increased oxidative stress that pseudomonads undergo at low temperatures [86], as well as to modulate the transition to planktonic to biofilm state, to act as antimicrobials against other microorganisms or as signalling molecules and virulence factors [35].
By combining different omics approaches, it was possible to identify the genomic locus unique to blue pigmenting Pseudomonas spp. [9][73]. The “blue branch” of the P. fluorescens phylogenetic tree include strains harbouring a genomic locus, indicated by Andreani et al. [72] as the c4_BAR (Contig 4 Blue Accessory Region); this region was described as containing 16 genes (16 Kb), including those coding for the trp accessory genes trpD, trpF, trpA, and trpC. Quintieri et al. [73] identified this region also in other pseudomonads; the analysis of the genomic context of the flanking regions suggested this region as a hotspot for genomic island integration. Quintieri’s group revealed the pathway related to the blue indigoidine synthesis by its inhibition in the presence of lactoferrin-derived antibiofilm peptides [9][35]. In Gram-negative bacteria, such as Roseobacter spp., indigoidine synthesis was modulated by C8-HSLs [87] through a multi-layered control exercised by a LuxRI-like system integrated with c-di-GMP [88][89]; pigment production was found to confer a competitive advantage to this strain when grown in co-culture with other microorganisms [88].
In addition to leucoindigoidine, the P. lactis ITEM 17298 harboured genes associated with the synthesis of the dark pigment pyomelanin from homogentisate (HGA) [35][73]. The metabolic route correlated to pyomelanin synthesis crossed the QS-regulated shikimate pathway, producing chorismate from D-erythrose 4-phosphate, a pentose phosphate intermediate; then, chorismate was converted to tryptophan. This latter pathway was recently associated with indigo derivate pigments by Andreani et al. [72][90].
In P. aeruginosa, Lan et al. [89] identified the oxidative stress sensing and response ospR (oxidative stress response and pigment production Regulator) gene, which binds to the promoter region of homogentisate 1,2-dioxygenase (hmgA) and affects its expression; the hmgA gene is involved in pyomelanin production. Orthologues of ospR are also present in P. fluorescens strains while they are absent in other pseudomonads such as P. putida, P. syringae, and P. entomophila. In addition to protection against oxidative stress, ospR plays multiple regulatory roles as a transcriptional regulator of β-lactam-resistant and QS-related genes (e.g., phzM, phzS) [89].
Pseudomonas spp. also produced fluorescent pigments on the cheese surface [91], putatively correlated to the synthesis of fluorescent siderophores, well known as pyoverdines (Pvds) or pseudobactins, which are involved in iron uptake and storage [9]; providing iron to the cell is especially important during the lag phase of growth, when the total siderophore concentration could be low. After binding its specific receptor, iron-bound pyoverdines act as signalling molecules that trigger the expression of several genes, e.g., those involved in the secretion of toxins responsible for virulence in pathogenic strains or for competitive advantage in the presence of other Pseudomonas spp. Moreover, pseudomonads pyoverdines can mediate proteases and lipases activities during spoilage [10][92][93].
As described by Machado et al. [80], who reported the inhibition of pyoverdine synthesis and proteases by applying a natural plant extract able to intercept the QS systems (las and rhl) involved in their expression, the identification and application of QS inhibitors to counteract pseudomonads growth, spoilage, or pathogenesis represents a promising preservation technique to improve the shelf-life of foods.

3.3. Off Flavours

Both milk fats and proteins release the elements responsible for the off flavours associated with dairy products. In particular, milk fats and triglycerides release short-chain fatty acids and keto and hydroxy acids that can react, leading to a bitter, soapy taste in fluid milk [64]; in addition, unsaturated fatty acids and phospholipids are substrates for autoxidation reactions. In contrast, proteins are a source of sulphur compounds and amino acids; the first ones are responsible for the cooked flavour in heated milk, whereas the second ones react with reducing sugars through the non-enzymatic browning reaction that produces caramel-like flavours [94]. As discussed above, fats and proteins hydrolysis occur thanks to the activity of protease and lipases, positively affected by QS; the kind and amount of released off-flavour compounds depend on the activated enzyme and substrate.
For example, the presence of exogenous C6-HSL in milk inoculated with P. azotoformans increased the lipolysis of fat in milk with a consequent higher content of volatile compounds (acetone, 2-heptanone, 2-butanone, and 2-pentanone) and acids (acetic acid, hexanoic acid, and octanoic acid) [13]. Likewise, hydrophobic peptides, derived by the hydrolysis of casein and responsible for the bitter off flavours, were released by QS-regulated AprX [9][95], as previously described.
Free amino acids are also substrates for the production, by pseudomonads decarboxylases, of biogenic amines (BAs, e.g., monoamines tyramine, histamine, cadaverine, and putrescine), a group of toxic compounds that can negatively affect the sensory properties of dairy products during storage; e.g., cadaverine and histamine impart a putrid and pungent flavour to milk [96]. It has been reported that in Pseudomonas spp. some BAs (such as putrescine) act as signalling molecules, triggering the attachment and biofilm formation; they also protect bacteria against radiation and oxidative stress and contribute to the development of antibiotic resistance and pathogenesis [97]. The effect of exogenous C4-HSL, C6-HSL, C8-HSL, C12-HSL, and C14-HSL on total volatile basic nitrogen (TVB-N), which reflect the accumulation of biogenic amines, was demonstrated by Li et al.[14] in aquatic products inoculated with P. fluorescens.

4. Conclusion

Food spoilage causes losses of billions of dollars worldwide every year with severe economic and social impacts. In dairy sector new and sustanable strategies are needed to control spoilage of fresh dairy products during their storg at low temperatures. With the evidence of Pseudomonas spp. contamination as a major cause of dairy decay, this entry has deeply investigated all the well-known issues, focusing for the first time on the role of microbial cross-talk in the evolution of spoilage events. Indeed, recently, molecule signals involved in QS have been detected in spoiled products where they affect microbial biodiversity and metabolic activities; these could be exploited as useful markers to monitor the quality of dairy products under storage and prevent spoilage events using natural antimicrobials and QS inhibitors.

References

  1. FAO; IFAD; UNICEF; WFP; WHO. The State of Food Security and Nutrition in the World 2019. Safeguarding against Economic Slowdowns and Downturns; FAO: Rome, Italy, 2019; p. 239.
  2. Grimaccia, E.; Naccarato, A. Food insecurity in Europe: A gender perspective. Soc. Ind. Res. 2020, 1–19.
  3. Laborde, D.; Martin, W.; Swinnen, J.; Vos, R. COVID-19 risks to global food security. Science 2020, 369, 500–502.
  4. UN General Assembly, Transforming Our World: The 2030 Agenda for Sustainable Development, 21 October 2015, A/RES/70/1. Available online: https://www.refworld.org/docid/57b6e3e44 (accessed on 3 November 2021).
  5. Santeramo, F.G.; Lamonaca, E. Food Loss–Food Waste–Food Security: A New Research Agenda. Sustainability 2021, 13, 4642.
  6. Martin, N.H.; Boor, K.J.; Wiedmann, M. Effect of post-pasteurization contamination on fluid milk quality. J. Dairy Sci. 2018, 101, 861–870.
  7. Martin, N.H.; Torres-Frenzel, P.; Wiedmann, M. Controlling dairy product spoilage to reduce food loss and waste. J. Dairy Sci. 2020, 104, 1251–1261.
  8. Rossi, C.; Serio, A.; Chaves-López, C.; Anniballi, F.; Auricchio, B.; Goffredo, E.; Cenci-Goga, B.T.; Lista, F.; Fillo, S.; Paparella, A. Biofilm formation, pigment production and motility in Pseudomonas spp. isolated from the dairy industry. Food Cont. 2018, 86, 241–248.
  9. Quintieri, L.; Zühlke, D.; Fanelli, F.; Caputo, L.; Liuzzi, V.C.; Logrieco, A.F.; Hirschfeld, C.; Becher, D.; Riedel, K. Proteomic analysis of the food spoiler Pseudomonas fluorescens ITEM 17298 reveals the antibiofilm activity of the pepsin-digested bovine lactoferrin. Food Microbiol. 2019, 82, 177–193.
  10. Brown, A.G.; Luke, R.K.J. Siderophore production and utilization by milk spoilage Pseudomonas species. J. Dairy Sci. 2010, 93, 1355–1363.
  11. Jamuna, B.A.; Ravishankar, R.V. Quorum sensing regulation and inhibition of exoenzyme production and biofilm formation in the food spoilage bacteria Pseudomonas psychrophila PSPF19. Food Biotechnol. 2014, 28, 293–308.
  12. Machado, I.; Silva, L.R.; Giaouris, E.D.; Melo, L.F.; Simões, M. Quorum sensing in food spoilage and natural-based strategies for its inhibition. Food Res. Int. 2020, 127, 108754.
  13. Yuan, L.; Wang, N.; Sadiq, F.A.; He, G. RNA sequencing reveals the involvement of quorum sensing in dairy spoilage caused by psychrotrophic bacteria. LWT 2020, 127, 109384.
  14. Li, T.; Wang, D.; Ren, L.; Mei, Y.; Ding, T.; Li, Q.; Chen, H.; Li, J. Involvement of exogenous N-acyl-homoserine lactones in spoilage potential of Pseudomonas fluorescens isolated from refrigerated turbot. Front. Microbiol. 2019, 10, 2716.
  15. Hassan, S.; Ahmad, T.; Bashir, M.; Kiran, G.S.; Selvin, J. Novel Perspectives on the Quorum Sensing Inhibitors (QSIs)/Quorum Quenchers (QQs) in Food Preservation and Spoilage. In Implication of Quorum Sensing and Biofilm Formation in Medicine, Agriculture and Food Industry; Bramhachari, P.V., Ed.; Springer: Singapore, 2019; pp. 269–298.
  16. Bai, A.J.; Vittal, R.R. Quorum sensing inhibitory and anti-biofilm activity of essential oils and their in vivo efficacy in food systems. Food Biotechnol. 2014, 28, 269–292.
  17. Shobharani, P.; Agrawal, R. Interception of quorum sensing signal molecule by furanone to enhance shelf life of fermented milk. Food Cont. 2010, 21, 61–69.
  18. Myszka, K.; Tomaś, N.; Wolko, Ł.; Szwengiel, A.; Grygier, A.; Nuc, K.; Majcher, M. In situ approaches show the limitation of the spoilage potential of Juniperus phoenicea L. essential oil against cold-tolerant Pseudomonas fluorescens KM24. Appl. Microbiol. Biotechnol. 2021, 105, 4255–4268.
  19. Wang, Y.; Feng, L.; Lu, H.; Zhu, J.; Kumar, V.; Liu, X. Transcriptomic analysis of the food spoilers Pseudomonas fluorescens reveals the antibiofilm of carvacrol by interference with intracellular signaling processes. Food Cont. 2021, 127, 108115.
  20. Wang, Y.; Wang, Y.; Chen, J.; Koseki, S.; Yang, Q.; Yu, H.; Fu, L. Screening and preservation application of quorum sensing inhibitors of Pseudomonas fluorescens and Shewanella baltica in seafood products. LWT 2021, 149, 111749.
  21. Gill, C.O.; Suisted, J.R. The effects of temperature and growth rate on the proportion of unsaturated fatty acids in bacterial lipids. J. Gen. Microbiol. 1978, 104, 31–36.
  22. Neumeyer, K.; Ross, T.; McMeekin, T.A. Development of a predictive model to describe the effects of temperature and water activity on the growth of spoilage pseudomonads. Int. J. Food Microbiol. 1997, 38, 45–54.
  23. Stoops, J.; Maes, P.; Claes, J.; Van Campenhout, L. Growth of Pseudomonas fluorescens in modified atmosphere packaged tofu. Lett. Appl. Microbiol. 2012, 54, 195–202.
  24. Nicodeme, M.; Grill, J.P.; Humbert, G.; Gaillard, J.L. Extracellular protease activity of different Pseudomonas strains: Dependence of proteolytic activity on culture conditions. J. Appl. Microbiol. 2005, 99, 641–648.
  25. Law, B.A.; Andrews, A.T.; Sharpe, M.E. Gelation of ultra-high-temperature-sterilized milk by proteases from a strain of Pseudomonas fluorescens isolated from raw milk. J. Dairy Res. 1977, 44, 145–148.
  26. De Jonghe, V.; Coorevits, A.; Van Hoorde, K.; Messens, W.; Van Landschoot, A.; De Vos, P.; Heyndrickx, M. Influence of storage conditions on the growth of Pseudomonas species in refrigerated raw milk. Appl. Environ. Microbiol. 2011, 77, 460–470.
  27. Stoeckel, M.; Lidolt, M.; Achberger, V.; Glück, C.; Krewinkel, M.; Stressler, T.; von Neubeck, M.; Wenning, M.; Scherer, S.; Fischer, L.; et al. Growth of Pseudomonas weihenstephanensis, Pseudomonas proteolytica and Pseudomonas sp. in raw milk: Impact of residual heat-stable enzyme activity on stability of UHT milk during shelf-life. Int. Dairy J. 2016, 59, 20–28.
  28. Volk, V.; Glück, C.; Leptihn, S.; Ewert, J.; Stressler, T.; Fischer, L. Two heat resistant endopeptidases from Pseudomonas species with destabilizing potential during milk storage. J. Agric. Food Chem. 2018, 67, 905–915.
  29. Machado, S.G.; da Silva, F.L.; Bazzolli, D.M.; Heyndrickx, M.; Costa, P.M.D.A.; Vanetti, M.C.D. Pseudomonas spp. and Serratia liquefaciens as predominant spoilers in cold raw milk. J. Food Sci. 2015, 80, M1842–M1849.
  30. Yuan, L.; Sadiq, F.A.; Liu, T.J.; Li, Y.; Gu, J.S.; Yang, H.Y.; He, G.Q. Spoilage potential of psychrotrophic bacteria isolated from raw milk and the thermo-stability of their enzymes. J. Zhejiang Univ. Sci. B 2018, 19, 630–642.
  31. Baruzzi, F.; Lagonigro, R.; Quintieri, L.; Morea, M.; Caputo, L. Occurrence of non-lactic acid bacteria populations involved in protein hydrolysis of cold-stored high moisture Mozzarella cheese. Food Microbiol. 2012, 30, 37–44.
  32. Scatamburlo, T.M.; Yamazi, A.K.; Cavicchioli, V.Q.; Pieri, F.A.; Nero, L.A. Spoilage potential of Pseudomonas species isolated from goat milk. J. Dairy Sci. 2015, 98, 759–764.
  33. Meng, L.; Liu, H.; Dong, L.; Zheng, N.; Xing, M.; Zhang, Y.; Zhao, S.; Wang, J. Identification and proteolytic activity quantification of Pseudomonas spp. isolated from different raw milks at storage temperatures. J. Dairy Sci. 2018, 101, 2897–2905.
  34. Ottaviani, F.; Disegna, L. Muffe e lieviti nei prodotti e negli ambienti caseari. Latte 1987, 12, 779–811.
  35. Quintieri, L.; Caputo, L.; De Angelis, M.; Fanelli, F. Genomic Analysis of Three Cheese-Borne Pseudomonas lactis with Biofilm and Spoilage-Associated Behavior. Microorganisms 2020, 8, 1208.
  36. Martin, N.H.; Murphy, S.C.; Ralyea, R.D.; Wiedmann, M.; Boor, K.J. When cheese gets the blues: Pseudomonas fluorescens as the causative agent of cheese spoilage. J. Dairy Sci. 2011, 94, 3176–3183.
  37. Carrascosa, C.; Millán, R.; Jaber, J.R.; Lupiola, P.; del Rosario-Quintana, C.; Mauricio, C.; Sanjuán, E. Blue pigment in fresh cheese produced by Pseudomonas fluorescens. Food Cont. 2015, 54, 95–102.
  38. da Silva Rodrigues, R.; Machado, S.G.; de Carvalho, A.F.; Nero, L.A. Pseudomonas sp. as the causative agent of anomalous blue discoloration in Brazilian fresh soft cheese (Minas Frescal). Int. Dairy J. 2021, 117, 105020.
  39. Carminati, D.; Bonvini, B.; Rossetti, L.; Zago, M.; Tidona, F.; Giraffa, G. Investigation on the presence of blue pigment-producing Pseudomonas strains along a production line of fresh mozzarella cheese. Food Cont. 2019, 100, 321–328.
  40. Cantoni, C.; Soncini, G.; Milesi, S.; Cocolin, L.; Iacumin, L.; Comi, G. Colorazioni anomale e rigonfiamento di formaggi fusi e mozzarelle. Ind. Aliment. 2006, 45, 276–281.
  41. Evanowski, R.L.; Reichler, S.J.; Kent, D.J.; Martin, N.H.; Boor, K.J.; Wiedmann, M. Pseudomonas azotoformans causes gray discoloration in HTST fluid milk. J. Dairy Sci. 2017, 100, 7906–7909.
  42. Kornacki, J.L.; Flowers, R.S.; Bradley, J.R.L. Microbiology of Butter. In Applied Dairy Microbiology, 2nd ed.; Marcel Dekker, Inc.: New York, NY, USA, 2001; pp. 127–150.
  43. Deeth, H.C.; Fitz-Gerald, C.H. Lipolytic enzymes and hydrolytic rancidity. In Advanced Dairy Chemistry Volume 2 Lipids; Springer: Boston, MA, USA, 2006; pp. 481–556.
  44. Samaržija, D.; Zamberlin, Š.; Pogačić, T. Psychrotrophic bacteria and their negative effects on milk and dairy products quality. Mljekarstvo: J. Dairy Prod. Proc. Imp. 2012, 62, 77–95.
  45. Kumar, H.; Franzetti, L.; Kaushal, A.; Kumar, D. Pseudomonas fluorescens: A potential food spoiler and challenges and advances in its detection. Ann. Microbiol. 2019, 69, 873–883.
  46. Corsetti, A.; Rossi, J.; Gobbetti, M. Interactions between yeasts and bacteria in the smear surface-ripened cheeses. Int. J. Food Microbiol. 2001, 69, 1–10.
  47. Fox, P.F.; Stepaniak, L. Isolation and some properties of extracellular heat-stable lipases from Pseudomonas fluorescens strain AFT 36. J. Dairy Res. 1983, 50, 77–89.
  48. Jay, J.M.; Loessner, M.J.; Golden, D.A. Modern Food Microbiology; Springer: New York, NY, USA, 2005.
  49. McPhee, J.D.; Griffiths, M.W. Pseudomonas spp. In Encyclopaedia of Dairy Sciences; Roginski, H., Fuquay, W.J., Fox, F.P., Eds.; Academic Press: New York, NY, USA, 2002; Volume 4, pp. 2340–2350.
  50. Hammad, A.M. Spoilage potential of Pseudomonas spp. isolated from domiati cheese. Assiut Vet. Med. J. 2015, 61, 18–23.
  51. Farkye, N.Y.; Vedamuthu, E.R. Microbiology of soft cheeses. In Dairy Microbiology Handbook. The Microbiology of Milk and Milk Products; Robinson, R.K., Ed.; John Wiley and Sons: Hoboken, NJ, USA, 2002; pp. 479–513.
  52. Paludetti, L.F.; Kelly, A.L.; Gleeson, D. Effect of thermoresistant protease of Pseudomonas fluorescens on rennet coagulation properties and proteolysis of milk. J. Dairy Sci. 2020, 103, 4043–4055.
  53. Stuknytė, M.; Decimo, M.; Colzani, M.; Silvetti, T.; Brasca, M.; Cattaneo, S.; Aldini, G.; De Noni, I. Extracellular thermostable proteolytic activity of the milk spoilage bacterium Pseudomonas fluorescens PS19 on bovine caseins. J. Dairy Sci. 2016, 99, 4188–4195.
  54. D’Incecco, P.; Brasca, M.; Rosi, V.; Morandi, S.; Ferranti, P.; Picariello, G.; Pellegrino, L. Bacterial proteolysis of casein leading to UHT milk gelation: An applicative study. Food Chem. 2019, 292, 217–226.
  55. Crudden, A.; Fox, P.F.; Kelly, A.L. Factors affecting the hydrolytic action of plasmin in milk. Int. Dairy J. 2005, 15, 305–313.
  56. Mara, O.; Roupie, C.; Duffy, Y.A.; Kelly, A.L. The Curd-forming Properties of Milk as affected by the action of plasmin. Int. Dairy J. 1998, 8, 807–812.
  57. Liu, M.; Wang, H.; Griffiths, M.W. Regulation of alkaline metalloprotease promoter by N-acyl homoserine lactone quorum sensing in Pseudomonas fluorescens. J. Appl. Microbiol. 2007, 103, 2174–2184.
  58. Liao, C.H.; McCallus, D.E. Biochemical and genetic characterization of an extracellular protease from Pseudomonas fluorescens CY091. Appl. Environ. Microbiol. 1998, 64, 914–921.
  59. Quintieri, L.; Pistillo, B.R.; Caputo, L.; Favia, P.; Baruzzi, F. Bovine lactoferrin and lactoferricin on plasma-deposited coating against spoilage Pseudomonas spp. Inn. Food Sci. Emerg. Technol. 2013, 20, 215–222.
  60. Caputo, L.; Quintieri, L.; Bianchi, D.M.; Decastelli, L.; Monaci, L.; Visconti, A.; Baruzzi, F. Pepsin-digested bovine lactoferrin prevents Mozzarella cheese blue discoloration caused by Pseudomonas fluorescens. Food Microbiol. 2015, 46, 15–24.
  61. Ledenbach, L.H.; Marshall, R.T. Microbiological spoilage of dairy products. In Compendium of the Microbiological Spoilage of Food and Beverages Industries; Doyle, M.P., Sperber, W.H., Eds.; Springer: New York, NY, USA, 2009; pp. 41–68.
  62. Morales, P.; Fernandez-Garcia, E.; Nunez, M. Production of volatile compounds in cheese by Pseudomonas fragi strains of dairy origin. J. Food Prot. 2005, 68, 1399–1407.
  63. Deeth, H.C. Lipases from Milk and Other Sources. In Agents of Change. Food Engineering Series; Kelly, A.L., Larsen, L.B., Eds.; Springer: Cham, Switzerland, 2021.
  64. Decimo, M.; Brasca, M.; Ordóñez, J.A.; Cabeza, M.C. Fatty acids released from cream by psychrotrophs isolated from bovine raw milk. Int. J. Dairy Technol. 2017, 70, 339–344.
  65. Deeth, H.C.; Fitzgerald, C.H. Lipolytic enzymes and hydrolytic rancidity in milk and milk products. In Developments in Dairy Chemistry; Fox, P.F., Ed.; Elsevier: Amsterdam, The Netherlands; Applied Science Publishers: London, UK, 1983; Volume 2, pp. 195–239.
  66. Ghoddusi, H.; Özer, B. Microbiology of cream, butter, ice cream and related products. In Dairy Microbiology and Biochemistry–Recent Developments; Ozer, B., Akdemir-Evrendilek, G., Eds.; CRC Press: Boca Raton, FL, USA, 2014; pp. 245–270.
  67. Soncini, G.; Marchisio, E.; Cantoni, C. Causes of chromatic alterations in Mozzarella cheese. Ind. Alim. 1998, 37, 850–855.
  68. Franzetti, L.; Scarpellini, M. Characterisation of Pseudomonas spp. isolated from foods. Annals Microbiol. 2007, 57, 39–47.
  69. Palleroni, N.J.; Genus, I. Pseudomonas Migula 1894. In Bergey’s Manual of Systematic Bacteriology, 2nd ed.; Brenner, D.J., Krieg, N.R., Staley, J.T., Eds.; The Proteobacteria, Part B, The Gammaproteobacteria; Springer: New York, NY, USA, 2005; Volume 2, pp. 323–379.
  70. RASFF. Rapid Alert System for Food and Feed. Annual Report. 2010. Available online: https://op.europa.eu/en/publication-detail/-/publication/7de58882-f5c5-4e28-b8b5-0ebf9836dbdf/language-en/format-PDF/source-174744260 (accessed on 12 December 2020).
  71. Nogarol, C.; Acutis, P.L.; Bianchi, D.M.; Maurella, C.; Peletto, S.; Gallina, S.; Adriano, D.; Zuccon, F.; Borrello, S.; Caramelli, M.; et al. Molecular characterization of Pseudomonas fluorescens isolates involved in the Italian “blue mozzarella” event. J. Food Prot. 2013, 76, 500–504.
  72. Andreani, N.A.; Martino, M.E.; Fasolato, L.; Carraro, L.; Montemurro, F.; Mioni, R.; Bordin, P.; Cardazzo, B. Tracking the blue: A MLST approach to characterise the Pseudomonas fluorescens group. Food Microbiol. 2014, 39, 116–126.
  73. Quintieri, L.; Fanelli, F.; Zühlke, D.; Caputo, L.; Logrieco, A.F.; Albrecht, D.; Riedel, K. Biofilm and pathogenesis-related proteins in the foodborne P. fluorescens ITEM 17298 with distinctive phenotypes during cold storage. Front. Microbiol. 2020, 11, 991.
  74. Fanelli, F.; Liuzzi, V.C.; Quintieri, L.; Mulè, G.; Baruzzi, F.; Logrieco, A.F.; Caputo, L. Draft genome sequence of Pseudomonas fluorescens strain ITEM 17298, associated with cheese spoilage. Genome Announc. 2017, 5, e01141–e01217.
  75. European Commission. Regulation (EU) 2019/1381 of the European Parliament and of the Council of 20 June 2019 on the transparency and sustainability of the EU risk assessment in the food chain. Off. J. Eur. Comm. 2019, L231, 1–28.
  76. Teh, K.H.; Flint, S.; Palmer, J.; Andrewes, P.; Bremer, P.; Lindsay, D. Biofilm—An unrecognised source of spoilage enzymes in dairy products? Int. Dairy J. 2014, 34, 32–40.
  77. Wettstadt, S.; Llamas, M.A. Role of regulated proteolysis in the communication of bacteria with the environment. Front. Mol. Biosci. 2020, 7, 586497.
  78. Bai, A.J.; Vittal, R.R. Bacterial quorum sensing and food industry. Compr. Rev. Food Sci. Food Saf. 2011, 10, 183–193.
  79. McCarthy, C.N.; Woods, R.G.; Beacham, I.R. Regulation of the aprX-lipA operon of Pseudomonas fluorescens B52: Differential regulation of the proximal and distal genes, encoding protease and lipase, by ompR-envZ. FEMS Microbiol. Lett. 2004, 241, 243–248.
  80. Machado, S.G.; Baglinière, F.; Marchand, S.; Van Coillie, E.; Vanetti, M.C.; De Block, J.; Heyndrickx, M. The biodiversity of the microbiota producing heat-resistant enzymes responsible for spoilage in processed bovine milk and dairy products. Front. Microbiol. 2017, 8, 302.
  81. Liu, X.; Ji, L.; Wang, X.; Li, J.; Zhu, J.; Sun, A. Role of RpoS in stress resistance, quorum sensing and spoilage potential of Pseudomonas fluorescens. Int. J. Food Microbiol. 2018, 270, 31–38.
  82. Ammor, M.S.; Flórez, A.B.; van Hoek, A.H.; de Los Reyes-Gavilán, C.G.; Aarts, H.J.; Margolles, A.; Mayo, B. Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria. J. Mol. Microbiol. Biotechnol. 2008, 14, 6–15.
  83. Rosenau, F.; Jaeger, K.E. Bacterial lipases from Pseudomonas: Regulation of gene expression and mechanisms of secretion. Biochimie 2000, 82, 1023–1032.
  84. Prigent-Combaret, C.; Brombacher, E.; Vidal, O.; Ambert, A.; Lejeune, P.; Landini, P.; Dorel, C. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 2001, 183, 7213–7223.
  85. Sacherer, P.; Défago, G.; Haas, D. Extracellular protease and phospholipase C are controlled by the global regulatory gene gacA in the biocontrol strain Pseudomonas fluorescens CHA0. FEMS Microbiol. Lett. 1994, 116, 155–160.
  86. Quintieri, L.; Fanelli, F.; Caputo, L. Antibiotic resistant Pseudomonas spp. spoilers in fresh dairy products: An underestimated risk and the control strategies. Foods 2019, 8, 372.
  87. Armes, A.C.; Buchan, A. Cyclic di-GMP is integrated into a hierarchical quorum sensing network regulating antimicrobial production and biofilm formation in Roseobacter clade member Rhodobacterales Strain Y4I. Front. Mar. Sci. 2021, 8, 681551.
  88. Cude, W.N.; Buchan, A. Acyl-homoserine lactone-based quorum sensing in the Roseobacter clade: Complex cell-to-cell communication controls multiple physiologies. Front. Microbiol. 2013, 4, 336.
  89. Lan, L.; Murray, T.S.; Kazmierczak, B.I.; He, C. Pseudomonas aeruginosa OspR is an oxidative stress sensing regulator that affects pigment production, antibiotic resistance and dissemination during infection. Mol. Microbiol. 2010, 75, 76–91.
  90. Andreani, N.A.; Carraro, L.; Zhang, L.; Vos, M.; Cardazzo, B. Transposon mutagenesis in Pseudomonas fluorescens reveals genes involved in blue pigment production and antioxidant protection. Food Microbiol. 2019, 82, 497–503.
  91. Reichler, S.J.; Martin, N.H.; Evanowski, R.L.; Kovac, J.; Wiedmann, M.; Orsi, R.H. A century of gray: A genomic locus found in 2 distinct Pseudomonas spp. is associated with historical and contemporary color defects in dairy products worldwide. J. Dairy Sci. 2019, 102, 5979–6000.
  92. Bishop, T.F.; Martin, L.W.; Lamont, I.L. Activation of a cell surface signaling pathway in Pseudomonas aeruginosa requires ClpP protease and new sigma factor synthesis. Front. Microbiol. 2017, 8, 2442.
  93. Wilderman, P.J.; Vasil, A.I.; Johnson, Z.; Wilson, M.J.; Cunliffe, H.E.; Lamont, I.L.; Vasil, M.L. Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa. Infect. Immun. 2001, 69, 5385–5394.
  94. Azzara, C.D.; Campbell, L.B. Off-flavors of dairy products. In Developments in Food Science; Off-Flavors in Foods and Beverages; Charalambous, G., Ed.; Elsevier: Amsterdam, The Netherlands, 1992; pp. 329–374.
  95. Andreani, N.A.; Carraro, L.; Fasolato, L.; Balzan, S.; Lucchini, R.; Novelli, E.; Cardazzo, B. Characterisation of the thermostable protease AprX in strains of Pseudomonas fluorescens and impact on the shelf-life of dairy products: Preliminary results. Ital. J. Food Saf. 2016, 5, 6175.
  96. Gloria, M.B.A.; Saraiva, P.R.; Rigueira, J.C.; Brandao, S.C. Bioactive amines changes in raw and sterilised milk inoculated with Pseudomonas fluorescens stored at different temperatures. Int. J. Dairy Technol. 2011, 64, 45–51.
  97. Luengo, J.M.; Olivera, E.R. Catabolism of biogenic amines in Pseudomonas species. Environ. Microbiol. 2020, 22, 1174–1192.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Agriculture, Dairy & Animal Science
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Leonardo Caputo
View Times: 3.5K
Revisions: 3 times (View History)
Update Date: 19 Apr 2022
Table of Contents
Academic Video Service
Feedback