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Quorum-Sensing Inhibitors from Probiotics: Comparison
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Please note this is a comparison between Version 2 by Rita Xu and Version 1 by Joseph Arsebe Arsene Mbarga Mbarga Manga.

Experience-based knowledge has shown that bacteria can communicate with each other through a cell-density-dependent mechanism called quorum sensing (QS). QS controls specific bacterial phenotypes, such as sporulation, virulence and pathogenesis, the production of degrading enzymes, bioluminescence, swarming motility, and biofilm formation. The expression of these phenotypes in food spoiling and pathogenic bacteria, which may occur in food, can have dramatic consequences on food production, the economy, and health.

  • quorum sensing (QS)
  • quorum quenching (QQ)
  • QS inhibitors
  • probiotics

1. Introduction

A few decades after the discovery of bacteria, the idea that bacteria were individualized organisms, and therefore did not communicate with each other, was accepted and established. However, after early research by Kenneth H. Nealson et al. [1] on the luminescence of the Gram-negative bacterium Vibrio fischeri (newly named Aliivibrio fischeri) [2], it became clear that bacteria communicate with each other [1]. Indeed, this research shows that bioluminescence in A. fischeri is induced and closely linked to bacterial density [1]. Later, it was found that this luminescence in A. fischeri is caused by the LuxI/LuxR transcriptional activator and autoinducer system mediating the cell-density-dependent control of Lux gene expression [3]. This communicational regulation, which has since taken the name of quorum sensing, is generally defined as a mechanism of microbial communication owing to a genetic regulation that involves the exchange and sensing of low-molecular-weight signaling compounds called autoinducers (AIs) [4,5][4][5]. Over the last few years, there have been a significant number of studies on the role of QS systems in the formation of various cellular patterns and their behavioral response [6,7][6][7]. Thus, to date, several other bacteria have demonstrated their ability to communicate through QS, and some inter-species communications have even been brought to light [8]. QS can have serious consequences, as it is involved in many important biological processes that can have a detrimental impact on the economy and health, such as sporulation, virulence and pathogenesis, and biofilm formation [9,10][9][10]. The consequences on human health are not discussed here, but economically speaking, phenomena such as biofilm formation can cause enormous losses in the agriculture and food industry [11,12][11][12]. It is well known that biofilms are largely responsible for the contamination of processed products within the food industry [12]. These microbial consortia embedded in self-produced exopolymer matrices [13] adhere to food processing, packaging, and equipment surfaces, and can negatively affect food safety [8,14][8][14]. Recent studies have demonstrated that QS molecules play a major role in the biofilm formation of Gram-positive and Gram-negative bacteria [8]. Although this correlation was not found when studying in vitro biofilms of strains isolated from a raw vegetable processing line, other foodborne bacterial pathogens, such as Salmonella spp., Campylobacter spp., Listeria monocytogenes, Escherichia coli, Staphylococcus aureus, and Bacillus cereus, can attach to various surfaces within the food industry and develop biofilms, leading to concerning hygienic disorders and a severe public health risk [14].
Studies conducted in recent years have suggested that QS inhibition could be an attractive alternative strategy for current bacterial control practices employed in industrial settings [8,14,15][8][14][15]. Unlike conventional antibacterials and sanitizers, instead of killing bacteria, a strategy using QS inhibitors consists of blocking intercellular communication and significantly limiting the expression of phenotypes, such as the formation of biofilms, while reducing the likelihood of resistance development [15,16][15][16]. Several products with important biological functions (e.g., phytochemicals, nanoparticles, halogenated natural furanones, and synthesized derivatives) have already demonstrated their ability to delay the microbial deterioration of foods and defeat important bacterial strains involved in spoilage [8,17][8][17]. However, although several studies have shown that certain strains of probiotics can interfere with the QS system [18[18][19][20],19,20], reports or evidence of their use as QS inhibitors (QSIs) in food preservation are scarce.
According to the Food and Agriculture Organization (FAO) and the World Health Organization (WHO), probiotics are living microorganisms that provide health benefits to their hosts in appropriate doses [21]. Probiotics have applications in a variety of fields, including food processing, animal breeding, and human health [21]. The fact that probiotics are “generally recognized as safe” means that these food additives and their by-products can be used in different processes, including food preservation and the maintenance of industrial food surfaces, since their addition will not have side effects on food safety [22].

2. Quorum Quenching and QS Inhibitors from Probiotics

QS inhibition is due to quorum quenching (QQ) enzymes or, more generally, to other chemicals known as QS inhibitors (QSIs). Whether due to enzymes or other chemicals, the disruption of the QS system commonly takes the name of QQ [22]. QQ has been suggested as a strategy for disrupting a pathogen’s ability to sense its cell density and to modulate the production of virulence factors [22]. Some data suggest that QQ is increasingly recognized as a new strategy used to control specific bacterial phenotypes, such as sporulation, virulence and pathogenesis, bioluminescence, swarming motility, and biofilm formation [15]. As shown in Figure 1 (taken from the review by [8] with the permission of Elsevier), there are several putative ways to inhibit QS (Figure 1): (a) the interruption of AHL signal synthesis by blocking the LuxI-type synthase; (b) the degradation of AHL signal dissemination by enzymes (AHL-acylase and AHL-lactonase), which will impair AHL accumulation; and (c) interference with signal receptors or the blockage of the AHL/LuxR complex [8]. Natural and synthetic QSIs have been intensively studied and are produced by a wide range of organisms, such as plants, some animals from aqueous ecosystems, fungi, and bacteria [71][23].
Fermentation 08 00711 g002
Figure 1. Inhibition of quorum sensing in Gram-negative bacteria: (a) inhibition of AHL synthesis; (b) degradation of AI using enzymes; (c) interference with signal receptors (From [8] with permission from Elsevier; license number: 5433491396764).
To our knowledge, the first QSI discovered was an enzyme called AiiA [72][24]. This enzyme, which was isolated from Bacillus sp. 240B1, is able to inactivate the AI (acylhomoserine lactone (AH2)) of Erwinia carotovora (Pectobacterium carotovorum), significantly decrease extracellular pectolytic enzyme activities, and attenuate the pathogenicity of this strain in potato, eggplant, Chinese cabbage, carrot, celery, cauliflower, and tobacco [72][24]. Later, other microorganisms, including probiotic bacteria, have been reported for their QQ activity [22]. Probiotics are shown to be effective for a variety of diseases, and their various bio-functional effects and potential for industrial application have been characterized and proven in vitro [73][25]. Most QS-inhibiting probiotics belong to the genera Lactobacillus, Bifidobacterium, and Bacillus. Table 1 presents some probiotics that are shown to have QQ activity and that could potentially have industrial applications; in particular, limiting food spoilage by interfering with QS in food-spoiling bacteria. Bacteria of the lactobacillus genus are among the most widely used as probiotics [74][26]. Lactobacilli and other probiotics belonging to the genera Lactococcus, Enterococcus, Pediococcus, Leuconostoc, Streptococcus, Carnobacterium, Fructobacillus, Oenococcus, and Weissella are included in the group of lactic acid bacteria (LAB), which means that they can produce lactic acid and other substances (bacteriocins, hydrogen peroxide, diacyls, and others) that may inhibit the growth of other bacteria [75][27]. LAB and bifidobacteria, or other probiotics for food preservation, have been used since ancient times due to their beneficial properties [75,76][27][28]; however, evidence based on experience reveals that their immunomodulating and antagonistic properties make them applicable in both the clinical field and animal breeding [77][29]. For example, regarding the clinical area, Lactobacillus acidophilus was reported to reduce the duration of diarrhea in children with acute gastroenteritis when administered at a dosage of more than 109 CFU [78][30]. Another strain, L. fermentum, can attenuate the inflammatory process and improve the production of some of the mediators involved in colitis (PGE2, IL-4, IL-6, IL-10, IL-17, TNF- α, IFN-γ, NO) [79][31]. Several other immunomodulatory effects of L. fermentum in vitro, in cell and animal models, and in human trials were extensively reviewed by Zhao et al. [80][32]. Gomi et al. [81][33] conducted a preliminary open trial and a double-blind, placebo-controlled, crossover trial to examine how fermented milk containing the probiotic Bifidobacterium bifidum YIT 10347 affects gastric and lower abdominal symptoms in adults taking no medication. The authors concluded that B. bifidum YIT 10347 could provide health benefits by alleviating gastric symptoms in these subjects [81][33]. Several other clinical benefits of probiotics are well documented in the review by Sánchez et al. [82][34]. In addition, regarding animal breeding, ourthe recent review entitled “The use of probiotics in animal feeding for safe production and as potential alternatives to antibiotics” extensively documented evidence for the effective use of probiotics in animals [77][29]. Probiotics appear to have multiple properties and, although evidence is scarce, their involvement in the regulation of quorum sensing (QS) may bring new solutions in several areas, including food preservation. From ourthe point of view, probiotics inhibiting the growth of other bacteria (including putrefying bacteria) in a medium is not necessarily caused by the inhibition of QS (QSI), but rather by antagonist activity linked to the acidification of the medium and the production of other bacteriocins [75,83][27][35]. However, there is evidence that some probiotics can potentially affect QS mediated by acylated homoserine lactones (AHLs, HSLs) and autoinducer 2 (furanosyl borate diester) [75][27]. As shown in Table 1, several species of lactobacillus (L. plantarum, L. fermentum, L. acidophilus, L. casei, L. brevis, L. reuteri, and L. curvatus), Bifidobacterium (B. longum and B. licheniformis), Bacillus (B. cereus, B. subtilis, and B. pumilus) and Streptococcus (S. salivarius and S. oralis) have already been reported at least once as quorum-quenching (QQ) agents. Although the results reported in Table 1 on the QQ activity of these probiotics are not related to food products, extrapolations in food preservation can be made because most of the pathogens affected by QQ are also known as foodborne pathogens (Table 1). For example, the fact that L. plantarum M.2 and L. curvatus B.67 demonstrated the ability to inhibit swimming motility, biofilm formation, and QS molecules related to biofilms in Listeria monocytogenes [84][36], a foodborne pathogen, could indicate that QSI molecules can be used to solve problems related to this bacterium in the food industry. As a reminder, L. monocytogenes is capable of adhering to food contact surfaces and forming matured biofilms, which are not easy to remove during the cleaning process and may therefore persist during food processing [85][37]. The physical means (for example, pulsed ultraviolet, ozone, and atmospheric cold plasma) employed to reduce the risks of contamination are very often effective but might affect food quality by changing sensory characteristics, such as appearance, color, flavor, and texture [22]. In the same way, the persistence of chemical agents (chlorinated disinfectants and oxidant fungicides) used during cleaning with chemical methods to minimize the growth of L. monocytogenes can have consequences on metabolism and the consumer’s health [75][27]. Therefore, in this context, it is important to seek alternative cleaning routes, subject to additional studies. The results obtained by Hossain et al. on the QQ activity of L. plantarum M.2 and L. curvatus B.67 against QS in L. monocytogenes can be used to suggest and develop new cleaning methods using biological means that are safe for the consumer [84][36].
Table 1. Some probiotic strains with QQ activity and the mechanism involved.
Probiotics Bacteria Inhibited QSI Mechanism References
Genus Species
Bacillus B. subtilis L. monocytogenes

E. coli

Gardnerella vaginalis Inhibits AI-2 activity and biofilm formation [86][38]
B. cereus RC1 Lelliottia amnigena

seudomonas aeruginosa MTCC2297 Inhibits pyocyanin production in P. aeruginosa and modulates the pathogenicity in L. amnigena [87][39]
B. subtilis R-18 Serratia marcescens The bacterial extract inhibits biofilm formation, protease, lipase, and hemolysin production [88][40]
B. subtilis BR4 P. aeruginosa Inhibits biofilm formation [89][41]
B. pumilus P. aeruginosa PAO1 (las, rhl)

S. marcescens (shl). Reduces the accumulation of N-acyl homoserine lactone (AHL) and shows significant inhibition of LasA protease, LasB elastase, caseinase, pyocyanin, pyoverdin, and biofilm formation. [90][42]
Bifidobacterium B. licheniformis DAHB1, Vibrio parahaemolyticus Inhibits biofilm formation in vitro and reduces shrimp intestinal colonization and mortality [91][43]
B. licheniformis T-1 Aeromonas hydrophila Quorum-quenching gene ytnP encodes an acyl-homoserine lactone metallo-β-lactamase [92][44]
B. longum ATCC15707 Escherichia coli 0157:H7 Inhibits AI-2 and reduces biofilm formation [18]
Lactobacillus L. acidophilus 30SC E. coli O157:H7 Inhibits AI-2 [93][45]
L. plantarum M.2,

L. curvatus B.67 L. monocytogenes Inhibits swimming motility, biofilm formation, and expression levels of target genes related to biofilm formation [85][37]
L. plantarum SBR04MA Microbiota of activated sludge Inhibits N-Hexanoyl-L-homoserine lactone (6-HSL) [94][46]
L. plantarum, S. aureus Reduces expression of some genes involved in biofilm formation [95][47]
L. acidophilus GP1B Clostridium difficile Reduces production of AI-2 molecules [20]
L. acidophilus La-5 Escherichia coli 0157:H7 Interferes with QS molecules and reduces adherence and colonization [19]
L. acidophilus NCFM - Not in pathogenic bacteria, but increases adherence of probiotic to intestinal cells by increasing AI-2 in LuxS system [96][48]
L. brevis 3M004 P. aeruginosa Inhibits biofilm formation [97][49]
L. casei Streptococcus mutans Inhibits QS genes vicKR and comCD [98][50]
L. casei ATCC 393,

L. reuteri ATCC23272,

L. plantarum ATCC14917

L. salivarius ATCC11741 Streptococcus mutans Inhibits acyl-homoserine lactone activity and blocks their synthesis [98][50]
L. fermentum Lim2 Clostridium difficile Reduces the AI-2 in QS gene luxS [99][51]
L. plantarum PA 100 P. aeruginosa Inhibits acyl-homoserine lactone activity and blocks their synthesis [100][52]
Streptococcus S. salivarius S. mutans Inhibits biofilm formation in vitro when cultured with S. mutans [101][53]
  S. salivarius K12 C. albicans Inhibits C. albicans aggregation, biofilm formation, and dimorphism. [102][54]
  S. salivarius 24SMB and S. oralis 89a S. aureus, S. epidermidis, S. pyogenes, S. pneumoniae, M. catarrhalis and P. acnes Inhibits biofilm formation in pathogens of the upper respiratory tract [103][55]

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