Next Article in Journal
Mucosa-Associated Oscillospira sp. Is Related to Intestinal Stricture and Post-Operative Disease Course in Crohn’s Disease
Next Article in Special Issue
The Multi-Strain Probiotic OMNi-BiOTiC® Active Reduces the Duration of Acute Upper Respiratory Disease in Older People: A Double-Blind, Randomised, Controlled Clinical Trial
Previous Article in Journal
Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 11
Issue 3
10.3390/microorganisms11030793
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Anti-Quorum Sensing Activity of Probiotics: The Mechanism and Role in Food and Gut Health

by
Mohammed Kamal Salman
,
Jumana Abuqwider
and
Gianluigi Mauriello
*
Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy
*
Author to whom correspondence should be addressed.
Microorganisms 2023, 11(3), 793; https://doi.org/10.3390/microorganisms11030793
Submission received: 2 February 2023 / Revised: 17 March 2023 / Accepted: 17 March 2023 / Published: 20 March 2023
(This article belongs to the Special Issue Beneficial Microbiota and Disease)
Review Reports Versions Notes

Abstract

:
Background: Quorum sensing (QS) is a cell-to-cell communication mechanism that occurs between inter- and intra-bacterial species and is regulated by signaling molecules called autoinducers (AIs). It has been suggested that probiotics can exert a QS inhibitory effect through their metabolites. Purpose: To provide an overview of (1) the anti-QS activity of probiotics and its mechanism against foodborne pathogenic and spoilage bacteria; (2) the potential role of the QS of probiotics in gut health; and (3) the impact of microencapsulation on QS. Results: Lactobacillus species have been extensively studied for their anti-QS activity and have been found to effectively disrupt QS in vitro. However, their effectiveness in a food matrix is yet to be determined as they interfere with the AI receptor or its synthesis. QS plays an important role in both the biofilm formation of probiotics and pathogenic bacteria. Moreover, in vitro and animal studies have shown that QS molecules can modulate cytokine responses and gut dysbiosis and maintain intestinal barrier function. In this scenario, microencapsulation was found to enhance AI activity. However, its impact on the anti-QS activity of probiotics and its underlying mechanism remains unclear. Conclusions: Probiotics are potential candidates to block QS activity in foodborne pathogenic and food spoilage bacteria. Microencapsulation increases QS efficacy. However, more research is still needed for the identification of the QS inhibitory metabolites from probiotics and for the elucidation of the anti-QS mechanism of probiotics (microcapsules and free cells) in food and the human gut.

1. Introduction

Quorum sensing (QS) is the mechanism that bacterial cells use for inter- and intra-species communication after the cell density reaches a specific threshold. This communication is signaled through molecules produced by the cells and named autoinducer (AI) molecules. When these molecules are accumulated at a specific threshold of concentration, they bind to a detector protein that initiates the QS transduction pathway. This ultimately leads to the genes responsible for pathogenicity, spoilage, and biofilm formation being expressed [1]. There are three common QS systems, which are employed by bacteria to regulate gene expression. The first is the luxRI-type QS system that is used by most Gram-negative bacteria. This QS system is mediated through acyl homoserine lactone (AHL) molecules, which are synthesized by the luxI gene as AIs. These then bind to the LuxR-type protein encoded by the luxR gene to form an AHL–LuxR complex, which activates the target gene expression [2]. The second is a two-component QS signaling system that is used by most Gram-positive species. This QS system is peptide-mediated and termed an accessory gene regulator (Agr) or Agr-like QS system. The AI peptide (AIP) is produced by agrD and processed by agrB for transportation into the agrCA pathway (two-component signaling cascade), in which a membrane-bound histidine kinase is synthesized by agrC to detect AIP. This initiates a series of phosphorylation that ultimately leads to the transcriptional regulator kinase (synthesized by agrA) being phosphorylated, which triggers the expression of the target genes [3]. A third major QS system is the AI-2/LuxS homolog that is shown both in Gram-negative and Gram-positive bacteria. AI-2 is synthesized by luxS, which then binds to the AI-2 receptor according to the type of bacteria [4]. A fourth type of autoinducer is AI-3, which was discovered in Escherichia coli as a regulator of virulence factors. This type of AI is produced through a series of reactions induced by threonine dehydrogenase and aminoacyl-tRNA synthetases [4].
Microbiome–microbiome crosstalk in the food and gut through QS plays a role in food quality and gut health, which is important for the food industry and medical therapy [5,6]. QS is involved in microbial pathogenesis and biofilm formation in food products, which is deemed a concern for public health and food safety. For example, milk can be contaminated with pathogenic Gram-positive bacteria such as Listeria monocytogenes that use peptides (i.e., AIP) as QS signaling molecules to trigger gene expression for biofilm formation [7]. Biofilm formation and microbial enzymatic activity (e.g., pectinolytic, proteolytic, and lipolytic) are factors of food spoilage, which can be regulated by QS. As a matter of fact, Pseudomonas and Enterobacteriaceae can spoil milk by the proteolytic activity, whose expression is regulated by the luxRI-type QS system [8,9]. Spoilage in meat and vegetables is also caused by Gram-negatives, where homoserine lactone (HSL) acts as a signaling molecule to QS [8]. Several studies have shown the positive effect of probiotics on food safety and quality through anti-QS activity [10,11,12].
In addition, the regulation of intestinal homeostasis and inflammation is also controlled by the QS of gut microbiota. It is worth noting that pathogenic bacteria can boost their survival in the gut by forming biofilms, which are regulated by QS [13]. Hence, QS acts as a mediator between gut microbiota and intestinal health [13]. Interestingly, QS inhibition could be one of the mechanisms by which probiotics modulate the gut microbiome and alleviate the harmful health effects of pathogenic bacteria. With QS playing a dual role in both food quality and gut health, disrupting QS could improve food quality and promote gut health. This could potentially be achieved by using probiotics as QS inhibitors (QSIs). Furthermore, the use of probiotics as QSIs may also be considered an alternative therapy to combat antimicrobial bacterial resistance [14]. Many QSIs from different sources were investigated against foodborne pathogenic and food spoilage bacteria. Plant sources of phytochemicals and bioactive compounds, bee products, and bacteria were found effective in disrupting the QS pathway and biofilm formation by spoilage and pathogenic Gram-negative and Gram-positive microorganisms [8,11,15]. As well described in the literature, the QS inhibition could be classified in one of the following mechanisms: (1) repressing the gene encoding the AI synthase; (2) inactivation of AI signals through quorum quenching (QQ) enzymes, (e.g., hydrolysis of the lactone bond in AHL); and (3) interfering with signal receptors in QS networks [14].
There is a growing body of research on the role and mechanism of QS in regulating bacterial biofilm formation and pathogenesis. The food industry is increasingly interested in the use of probiotics for food functionalization and bio-preservation. Therefore, this review has a dual purpose. Firstly, it aims to provide an up-to-date overview of the anti-QS activity of probiotics against foodborne pathogens and spoilage bacteria. Secondly, it aims to offer insights into future perspectives for the potential use of probiotics in food products to enhance food quality and gut health by inhibiting QS. The results of this review will serve as a foundation for further investigations to fill the knowledge gap regarding the role of QS in food quality and human health.

2. Mechanism of QS Inhibition

In the last decade, there has been growing attention to unveil the mechanism that probiotics use to alter QS activity in foodborne pathogenic and spoilage bacteria. Probiotics, in particular lactic acid bacteria (LAB), are the most studied microorganisms as a promising source of QSIs. The interference with the LuxRI-type, Agr-like, and AI-2/LuxS-type QS systems would result in the repression of virulence genes responsible for pathogenicity, food spoilage, and biofilm formation. In the two sections below, the mechanism of QS disruption in foodborne pathogenic and spoilage bacteria is discussed in detail.

2.1. Probiotics as QSIs in Foodborne Pathogenic Bacteria

It is well reported that LAB have a bactericidal effect through the secretion of organic acids, hydrogen peroxide, and bacteriocins, which affect the growth or the survival of pathogenic bacteria [16]. Interestingly, the detrimental effects of foodborne pathogenic bacteria can be reversed by disrupting the QS mechanism, without their growth/survival necessarily being impacted [8]. Numerous probiotics are demonstrated as QSIs through interference with the QS signaling pathway of the target bacteria [11]. LAB are the most studied QSI bacteria against a range of common pathogenic bacteria, which rely on QS for biofilm formation and the expression of virulence factors [11].
In Table 1, potential probiotic LAB and non-LAB are described as QSIs. Generally, the interference of QSI with one of the QS pathway components would lead to the downregulation of QS-related genes and the inactivation of QS.
Various strains of Lb. acidophilus exhibited anti-QS activity towards C. difficile, Staph. Aureus, and E. coli [18,24,27] through the inhibition of AI-2 production or downregulation of biofilm-related genes without an influence on AI-2 synthesis. However, the anti-QS compounds in these studies are not well identified. Other similar studies found that the biofilm-related genes in E. coli and P. aeruginosa were under-expressed by the activity of EPS and DKP produced by the strains of Lb. acidophilus A4 and CRL 730, respectively [25,29]. The anti-biofilm and anti-QS activity of probiotics against Salmonella was also observed, but the QSIs were not identified [35,36,37,38,39]. In these studies, EPS might be produced by the lactobacillus species as the QSI. This was suggested according to the study of Xu et al. (2020) [40], which found that the biofilm formation of S. Typhimurium was repressed by the action of EPS synthesized by Lb. coryniformis NA-3. Even though not investigated, EPS from the Lactobacillus species could play a role in the interference with the QS in Salmonella through the downregulation of the genes encoding the QS regulator proteins [35,36,38,39,40]. Unfortunately, the mechanisms behind the QS inhibition against E. coli and Salmonella were not well identified. Hypothetically, the QSIs antagonize the QS regulator proteins, which modulate the expression of virulence genes. This was proposed according to the outcomes in other studies that used molecular docking and bioinformatic methods. The chemically produced QSIs interact with the amino acid sequence of the cognate regulator proteins (LsrR and SdiA), which, in part, mediates QS in Salmonella and E. coli [54,55]. The binding of phosphorylated AI-2 (AI-2-P) with its cognate protein LsrR leads to the inactivation of LsrR, which regulates transcription of the lsr operon that controls the cell uptake of AI-2 and pathogenicity [56]. Therefore, QSIs antagonize the LsrR protein by blocking AI-2-P binding, making active LsrR that leads to the repression of the lsr operon. Another potential QSI mechanism is the binding of the QSI with SdiA amino acids. This interaction will prevent AHL by binding the SdiA receptor, which works as a transcriptional regulator for QS-related virulence genes [56].
Staph. aureus is one of the common causative factors for foodborne pathogenesis and infectious mortality globally. It is expected that there is a 10 to 30% mortality rate of SAB (Staph. aureus bacteremia) cases, and this is exacerbated by the ability of Staph. aureus to develop resistance to antibiotics [57]. In comparison with QS in other bacterial species, Staph. aureus encompasses 13 QS pathways, each one associated with a different virulence mechanism [58]. The blocking of QS in Staph. aureus could be a surrogate of antibiotic treatment to control virulence expression and infection treatment. Several studies found that probiotics or their metabolites have a QS inhibitory effect against Staph. aureus. As a matter of fact, cyclo-dipeptides produced by Lb. reuteri showed repression activity on Staph. aureus pathogenicity elements, such as the Agr system, tst gene, and SaeRS QS system [20]. A cross-sectional study revealed an agr-inhibitory effect via B. subtilis-produced lipopeptide (fengycin) [21]. In this study, 200 nasal swapes and fecal samples were collected from a Thai population living in different areas and were analyzed for Staph. aureus and B. subtilis colonization. There was a positive relationship between the presence of B. subtilis and the absence of Staph. aureus. Furthermore, agr activity declined when the B. subtilis culture filtrate was incubated with the Staph. aureus reporter strain, and the synthesis of virulence factors (phenol-soluble modulins, α-toxin, and Panton–Valentine leucocidin) was also suppressed [21]. Accordingly, the two-component signaling (fsr) in E. faecalis was disrupted by the inhibitory effect of B. subtilis ZK3814-secreted lipopeptides (surfactin and fengycin). The result was that the expression of proteolytic activity-related genes (gelE/sprE) was quenched.
Other anti-QS unraveled compounds are the biosurfactants synthesized by Lb. helveticus and P. pentosaceus, which were shown to reduce biofilm formation by B. subtilis, P. aeruginosa, Staph. aureus, and E. coli [22,42]. While the anti-QS activity of the biosurfactant from P. pentosaceus was not investigated in-depth [42], Jiang et al. (2019) [22] found that the biosurfactant from Lb. helveticus reduced in Staph. aureus the expression of dltB, which is a regulatory gene in the two-component signaling system GraRS that controls the resistance to cationic antimicrobial peptides (CAMB), which is a defense system that a host employs against microbial infection. The response regulator genes agrA and sarA that are involved in the regulation of biofilm formation were also repressed. Interestingly, the in vivo experiment showed that the anti-biofilm activity also reduced the hemolytic activity of Staph. aureus. Peculiarly, the AI-2 release was associated with the inhibition of biofilm formation as found by Ahn et al. (2021) [23]. LPA produced from Lb. plantarum KCTC10887BP reduced the expression of biofilm formation by the induction of AI-2 release. This was confirmed in another study [59], which reported an upregulation of biofilm formation in Staph. aureus RN6390B with mutation in the luxS gene. AI-2 release results in the transcription of the icaR gene, which works as a repressor for the ica operon, and consequently, the expression of the icaA gene that is involved in biofilm formation is deactivated.
Having established the anti-biofilm activity of probiotics, the tooth decay causing-bacterium Str. mutans relies on biofilm formation for adhesion. Several studies show that the anti-QS activity of probiotics is related to the repression of biofilm-related genes and the inhibition of EPS production, which is an important matrix of biofilm formed by Str. mutans. Biosurfactants and a novel compound (iminosugar) were identified as QSIs produced by Lb. rhamnosus and Lb. paragasseri MJM60645, respectively [47,48,49,50,51]. Lb. plantarum-secreted LPA exerted anti-biofilm activity against Str. mutans, E. faecalis, and Str. gordonii [52]. This anti-biofilm activity could be due to the same inductive effect of LPA on AI-2 release that was observed by Yu et al. (2012) [59], albeit the QSI mechanism is not described.
P. aeruginosa is a pathogenic bacterium that causes infections in humans, especially in immunocompromised populations. The treatment of infections with P. aeruginosa is cumbersome due to its resilience to various stress conditions and antibiotic administration and its ability to produce diverse types of EPS matrixes for biofilm formation and cell adhesion [60,61]. There are three QS systems (las, rhl, and pqs) in P. aeruginosa, which are activated for the expression of biofilm formation and virulence factors. LasI, rhlI, and pqsABCDH are synthase genes of the autoinducers N-(3-oxododecanoyl)-HSL, N-butyryl-HSL (C4-HSL), and 2-heptyl-3-hydroxy-4-quinolone (PQS), respectively [62]. Extensive research has been conducted to investigate the QSI by probiotics and their metabolites in vitro. QS was blocked through the degradation of QS signal molecules (AHL) by various species of B. paralicheniformis. Lactonase and acylase were found to degrade the lactone and acyl rings in the QS signal AHL, respectively [33]. Lb. brevis showed anti-QS enzymatic activity by unknown AHL-degrading enzymes [28]. It is noteworthy that as lactonase and acylase only degrade AHLs, these enzymes are only efficient in Gram-negative bacteria, which involve AHL-based QS pathways. Another route of QS inhibition against P. aeruginosa is the antagonization of the receptor proteins. Stigmatellin Y from B. subtilis BR4 interfered with the PQS QS systems by binding with the PqsR protein in competition with the PQS signal molecule and disruption of AHL-signal transduction [32]. Lyophilized postbiotics from Lb. casei disrupted the rhl QS system and downregulated the genes for autoinducer synthase and its cognate regulatory protein, potentially, due to the action of organic acids [31]. When the CFS of Lb. rhamnosus GG was incubated with P. aeruginosa PAO1, there was a decrease in AHL activity and levels [30]. In this study, the authors state that the CFS has inhibited AHL production, potentially by reducing the expression of the AHL-producing gene (lasI), albeit this was not evaluated. Perhaps, Lb. rhamnosus GG reduced the AHL activity through the newly revealed enzyme (acyl-hydrolase); however, this still needs further investigation [63].
Bacteriocins are antimicrobial peptides that are usually secreted from lactic acid bacteria that kill or inhibit the growth of the target pathogenic or spoilage microorganisms. They have lately been linked with the QS mechanism. In Rizzello et al. (2014) [11], QS in Lb. plantarum C2 was involved in the production of plantaricin. Reuterin and lactocin released from Lb. reuteri LR 21 and Lb. curvatus CRL1579, respectively, acted as QSIs [17,49]. Reuterin reduced the expression of the luxS and agrB genes in C. perfringens 13124, which subsequently prevented toxin production by repressing the toxin-producing genes (cpa and pfo). The QSI mechanism of lactocin is not yet demonstrated. However, in Hossain et al. (2021) [56], the expression of the biofilm-regulatory genes of L. monocytogenes ((flaA, fbp, agrA, prfA, and hlyA) was inhibited as an effect of the postbiotics from Lb. curvatus B.67 and Lb. plantarum M.2. Very recently, Lb. curvatus B67 was reported to produce quercetin that shows anti-biofilm activity against Listeria monocytogenes [64]. Reasonably, a QS inhibition activity of quercetin could be hypothesized.
Apart from the QSI mechanism discussed above, it is suggested the QS pathway for biofilm formation could be disrupted by the inhibition of proton motive forces (PMFs) and efflux pumps. PMFs were associated with the release of AIs from cells, and the inactivation of PMFs would lead to the intracellular accumulation of autoinducers and thus, the downregulation of QS-regulatory genes [65]. This was also confirmed when QS peptide export was blocked due to the disruption of PMFs in Str. pneumoniae [66]. In addition, in Sutyak et al. (2011) [67], the inhibitory effect of subtilosin on PMF in Gordonia vaginalis was reported. Therefore, the anti-biofilm activity of B. subtilis KATMIRA1933 against L. monocytogenes could be potentially attributed to the inhibitory effect of subtilosin on PMFs [37].
In summary, probiotics could exhibit QS inhibitory effects by producing and secreting QSIs. These are reported as lipopeptides (such as fengycin and surfactin), lipoproteins (biosurfactants), organic compounds, cyclic peptides, lipoteichoic acid, exopolysaccharides, bacteriocins (such as reuterin and lactocin), and AHL-lytic enzymes. However, in some studies, there was a gap in the identification of QSI compounds or the elaboration of the QS inhibition mechanism when anti-QS activity was shown.
Despite the anti-QS effect of the CFS of probiotics/postbiotics against foodborne pathogens, it is not known whether the same anti-QS activity can be observed if probiotics are investigated as cell cultures. Furthermore, the extensive research on QSI has been conducted in in vitro experiments. In fact, the outcomes of these studies do not necessarily replicate the context in real foods. The chemical composition of food (proteins, lipids, and carbohydrates) might affect the viability and functional properties of probiotics [68].

2.2. Potential Role of Probiotics in QS Inhibition in Food Spoilage Bacteria

Food spoilage is a consequence of physical changes, such as texture change due to drying, chemical reactions, such as oxidation, and microbial activity. Microbial-induced food spoilage can reduce the shelf-life of food by altering its sensory qualities, such as texture, flavor, and taste, due to enzymatic activity (proteolytic, lipolytic, and pectinolytic) and biofilm formation [69]. QS molecules have been detected in different types of food products, including meat, milk, and vegetables, and their presence has been suggested to be involved in microbial food spoilage [8]. The growth of psychrotrophic Gram-negative bacteria, usually isolated from raw milk (e.g., Pseudomonas and Serratia), is associated with biofilm formation and the production of extracellular enzymes that are mediated by the luxI/AHL-type QS system [70]. This has also been confirmed in a transcriptome analysis study that evaluated the effect of exogenous AHLs on the virulence activity of Pseudomonas azotoformans and Serratia liquefaciens in milk. It was observed that the addition of AHLs upregulated the genes responsible for growth, metabolism, and enzymatic activity (protease, lipase, and glycosidase) [71]. Fresh meat contains a complex of several bacterial genera (Enterobacteriaceae, Yersinia, and Pseudomonas) that induce spoilage. In these species, the expression of biofilm formation and virulence factors of spoilage are stimulated by the luxI/AHL-type QS signaling pathways. Proteolytic activity and AHLs with different carbon chain lengths were found in chilled meat products, and this was associated with the growth of Enterobacteriaceae and Pseudomonas. Moreover, the luxS/AI-2-type QS system is known to be implicated by Leuconostoc citreum, a lactic acid bacterium that causes meat spoilage in biofilm formation [9,72,73,74,75]. Post-harvest contamination of vegetables with pectinolytic and proteolytic bacteria could impact the quality of the product and reduce the shelf-life. Pectobacterium carotovorum is one of the common plant pathogenic bacteria that causes soft-rot disease in a wide range of vegetables (potato, onion, tomato, and radish) through enzymatic activity, which is a concern for the agriculture industry and farmers due to the economic loss [76]. The production of pectinolytic and proteolytic enzymes is regulated by QS. It was found that LuxS-mutant Pectobacterium carotovorum reduced the expression of pectate lyase and cellulase in addition to protease enzymes, which demonstrates the role of the luxS/AI-2-type QS system in enzymatic activity expression [77]. Similarly, in LuxS-mutant Erwinia carotovora, there was a four- and three-times decrease in the production of pectate lyase and polygalacturonase compared with the wild-type strain, after 6 and 8 h of growth, respectively [78]. In the same species, another study showed the role of the luxI/AHL-type QS system in the rot–spoilage of bean sprouts by proteolytic and pectinolytic activity. However, when the bean sprouts were inoculated with the luxI-mutant strain, the spoilage took longer to occur compared with sprouts contaminated with the wild-type strain [79]. Shewanella baltica is the primary bacterium that causes fish to deteriorate. It also employs the luxS/AI-2-type QS system to activate genes related to spoilage and biofilm formation through DKPs as signaling molecules for QS induction [80]. Overall, QS plays a crucial role in microbial food spoilage. Therefore, disrupting QS signaling in spoilage bacteria could extend the shelf life of fish products by preventing the expression of virulence factors and biofilm formation. A wide range of QSIs, including plant-derived compounds (such as phenol acids), chemicals such as furanone, and QS signal-degrading enzymes, have been demonstrated [8]. This section explores the potential role of probiotics as a source of QSIs.
Notably, QS inhibition against microbial spoilage is a recent focus of research. As shown in Table 2, only five studies have investigated potential probiotics as a source of QSIs. The anti-QS activity of Bacillus strains was identified through the QQ activity of lactonase and the antagonistic effect of DKPs on QS receptors. Li et al. (2022a) [81] showed that QS promoted the growth of Lb. plantarum ss-128, but they did not investigate its anti-QS activity against spoilage bacteria. Research on the anti-QS activity of lactic acid bacteria against food spoilage bacteria is still lacking.
Spoilage bacteria can cause changes in food quality due to both enzymatic activity and the release of chemical compounds, including volatile organic compounds (VOCs), volatile fatty acids, ethyl esters, aldehydes, and sulfur compounds, which can result in sensory defects such as off-odor, off-flavor, and discoloration [72]. It is unclear, however, whether QS directly influences the expression of these virulence factors.
The interaction between probiotics and spoilage bacteria in food microbiomes has the potential to play a key role in prolonging food shelf-life by modulating the expression of spoilage factors. However, the effect of such an interaction on QS in spoilage bacteria is still not well-researched. If probiotics are found to have an anti-QS effect against spoilage bacteria, this could be a significant step towards replacing chemical preservatives with bio-preservatives and enhancing the efficacy of other preservatives.

3. QS, Biofilm Formation, and Gut Health

It is well-known that probiotics provide health benefits for the host gut through several mechanisms. This section briefly discusses the role of probiotics’ QS system as one of these mechanisms, as summarized in Table 3.
The induction or inhibition of QS signaling is associated with the expression or repression of biofilm-related genes, respectively. In fact, biofilm is necessary for pathogenic bacteria to maintain their growth and infect the host environment [94]. The protective effect of probiotics against pathogenic bacteria in the gut could be attributed to their anti-QS and anti-biofilm activity, as shown in Table 1. Additionally, the QS system is involved in the regulation of biofilm formation by probiotics in the host gut [10]. This forms a biological barrier and maintains intestinal immunity against pathogenic bacteria that cause infection [10]. The importance of the AI-2/luxS-type QS system in biofilm formation and stress resistance of the probiotics (Lactobacillus and Bifidobacterium) was observed. The promotion of AI-2 synthesis by the overexpression of luxS in Lb. paraplantarum L-ZS increased resistance to heat- and bile-salt stress compared with the wild-type strain [95]. Moreover, the biofilm formation of Lb. paraplantarum L-ZS and Bifidobacterium longum NCC2705 was augmented [95,96].
An emerging field of research highlights the ability of QS molecules to modulate the inflammatory response. One type of AHL QS molecule, 3-oxo-C12:2-HSL, was described as anti-inflammatory through the activation of bitter taste receptors and the inactivation of cell signaling cascades (JAK-STAT signaling pathway, NF-κB signaling, and TNF signaling pathway) that upregulate the inflammatory response [86,97]. Additionally, the presence of 3-oxo-C12:2-HSL in the gut was negatively correlated with inflammatory bowel disease (IBD) incidence, indicating the role of this type of AHL as an anti-inflammatory [87]. Another type of QS molecule, AI-2, was recently found to be able to modulate the inflammatory response and gut microbiota composition in vivo [89,90]. In a study by Thompson et al. (2015) [88], a group of mice was induced into dysbiosis by antibiotic administration and then supplemented with genetically engineered E. coli overproducing AI-2. After treatment, the antibiotic effect was reversed, and the abundance of Firmicutes was significantly promoted compared to Bacteroidetes. The authors of this study propose that AI-2 improved the signaling response among the Firmicutes, a recurrent producer of AI-2. In another study [89], a group of early weaning stress-induced piglets was treated with either the wild type (WT) or luxS mutant (ΔluxS) of Lb. rhamnosus GG. The ability of ΔluxS to preserve the gut barrier function was significantly lower than the WT. As previously discussed, this is due to the role of AI-2 in biofilm formation, which the ΔluxS strain lacks to colonize and adhere in the intestine cells. This postulates the role the AI-2/luxS-type QS system has in gut health. Recently, an animal study showed that AI-2 supplementation of mouse pups with necrotizing enterocolitis reduced the expression of pro-inflammatory cytokines and increased the anti-inflammatory cytokine (IL-10) production. Furthermore, AI-2 rebalanced the composition of gut flora. In the mice group treated with AI-2, Lactobacillus was increased, while Helicobacter and Clostridum_sensu_stricto_1 were reduced compared with the not-AI-2-treated group [90]. In another study, the butyl-DPD analog (the precursor for AI-2) was able to alleviate the inflammatory response of human gingival keratinocyte cells when incubated with two Prevotella species. The interleukins’ (IL-6 and IL-8) expression was reduced [91]. Nevertheless, a cross-sectional study in patients with colorectal cancer (CRC) demonstrated the association of AI-2 secreted from gut microbiota with CRC occurrence [92]. In addition, AI-2 from non-pathogenic E. coli mediated the transcription of the cytokine response pathway, which as a result, induced inflammatory interleukin IL-8 through the upregulation of the transcription factor NF-κB pathway that regulates cytokine production [93].
There are chemically synthesized QSIs that can be considered anti-virulence agents for infection treatment. Nevertheless, it is proposed that some species such as E. coli and Salmonella can develop resistance to these QSIs, which is partially due to the opportunity for bacteria to shift from the QS system to another strategy for virulence expression. In the review study by Escobar-Muciño et al. (2022) [55], the ability of bacteria to develop QSI resistance via enhancing the affinity of QS-receptor proteins to QSIs is discussed. In addition, there are critics that were reported to point out the limitations of QSI use as a therapeutic strategy against infectious pathogens [98]. As discussed above, AI-2 signaling is required for biofilm formation for both probiotics and pathogenic bacteria. The interruption of AI-2 signaling using unselective chemical inhibitors, such as furanone, would also act on probiotic gut microbiota, which would then reduce their resistance to pathogenic microorganisms [98]. Furthermore, in Δagr-mutant Staph. aureus, biofilm formation and higher survivability were observed, and in ΔlasR-mutant P. aeruginosa, higher production of pyocyanin (virulence factor) and pro-inflammatory responses have also been reported. These observations might restrict the efficacy of chemical QSIs [99]. Finally, foodborne pathogenic bacteria could develop resistance to QSIs as shown by studies that revealed the ability of P. aeruginosa to develop resistance to antibiotics (carbapenems and azithromycin) that show anti-QS activity [98].
The potentiality to develop resistance to QSI-based therapy is prompting the opening of a new line of investigation to unravel the mechanism of probiotics for use as a substitutive chemical QSI-based therapy against infectious diseases to overcome the microbial QSI resistance.
It can be deduced that QS is an interplay in host–gut microbiome interaction. The health benefit mechanism of probiotics is either by reducing the expression of QS biofilm-related genes of pathogenic bacteria or by direct impact of QS molecules on intestinal cells. However, the results are still contradictory. In Li et al. (2019) [96], AI-2 was suggested to be involved in the progression of CRC and can be used as a marker, whereas as described by the abovementioned studies [92,93,94,95], there is a positive role of AI-2 in the alleviation of pro-inflammatory responses. Furthermore, the AI-2 used in some of the above studies was chemically synthesized and supplemented exogenously in in vivo studies. It will be intriguing to investigate the effect of the AI-2 secretions from probiotics on gut dysbiosis, inflammatory response, and intestine barrier health in in vivo and human studies. In addition, research on the mechanism of probiotic health benefits in the gut via QS is still lacking.

4. Microencapsulation and QS

Probiotic microencapsulation is used to increase stress resistance and cell viability after exposure to the outside environment, such as during passage in the gastrointestinal tract, processing, and storage [99,100]. Microencapsulation of probiotics also boosts the health benefits of probiotics. An animal study found that microcapsules of Lb. plantarum LIP-1 reversed dysbiosis, increased colonization, and reduced lipid concentration in hyperlipidemic rats compared with free cells of LIP-1 [101]. In addition, microencapsulation of Lb. plantarum LN66 increased the survival rate under different packaging conditions and simulated a gastrointestinal environment compared with free cells [102]. It is possible that the microencapsulation mode of action on bacterial behavior is partially regulated by QS. During the incubation of microcapsulated cells, bacteria are grown in aggregates with shorter in-between cell distances than in free cells. This conduces to better AI activity and cell-to-cell communication, that is, the QS efficacy is not the same when bacterial cells are free or encapsulated. This was found in the study by Gao et al. (2016a) [103] when V. harveyi cells were incorporated into microcapsules, and the QS capacity was evaluated in comparison with free cells. The results showed that the luxS gene expression was significantly higher in microencapsulated cells than in free cells, despite the cell density being lower in microcapsules after 12 h of incubation. In contrast, another study found that the viable Lb. plantarum AB-1 cells were significantly higher in microcapsules compared with free cells after 48 h of growth culturing, but the same outcome of enhanced QS was observed [104]. This might be due to different types of bacteria or the experimental design. Moreover, the size of cell aggregates plays a part in the impact of microencapsulation on QS mediated by the spatiality effect. Large cell aggregates demonstrated more effective QS than small cell aggregates (Gao et al., 2016b) [105]. Prominently, bacterial QS can be also regulated by manipulation of the microenvironment inside the microcapsules (diameter, core state, and alginate concentration). Alginate concentration and microcapsule diameter are positively correlated with AI activity and, thus, stronger QS capacity. Furthermore, when the core state of a microcapsule is solid, the size of the cell aggregate is larger than in a liquid core state. As mentioned previously, the QS is more enhanced in large cell aggregates than in small cell aggregates. The underlying mechanism of these microenvironment parameter effects is that the mass transfer of AIs inside the microcapsule is reduced in response to the increase in diameters and alginate concentration and the solidified core state. This makes the AIs restricted inside the microcapsules, which is, in turn, how the interaction of the AIs with cells is facilitated [106]. Considering the impact of microencapsulation on QS efficacy, it would be worth investigating whether the anti-QS and anti-biofilm effect of probiotics can be improved by microencapsulation. Until now, there is only one study that investigated the anti-biofilm activity of Lb. rhamnosus GG microcapsules in co-culture with E. coli [13]. The results indicated that E. coli QS-related genes encoding biofilm formation (lsrK and luxS) were significantly downregulated as a result of the anti-QS activity of the microencapsulated cells of Lb. rhamnosus GG. Interestingly, microcapsules have not only been able to cause a remarkable decline in biofilm formation but also to erase mature biofilm. In a study conducted by Song et al. (2021) [107], the anti-biofilm properties of microencapsulated Lb. rhamnosus GG were confirmed through a proteomic quantitative analysis of a co-culture of E. coli and the microcapsules. The microcapsules disrupted the metabolic pathway of E. coli, resulting in a reduction of biofilm formation and led to decreased expression of genes related to biofilm formation and stress resistance (dnaK and bamE), although it is unclear whether this was due to QS inhibition. However, the efficacy of the anti-QS activity of the microcapsules was not compared to that of free cells, and it is important to determine to what extent the microcapsules enhance anti-QS activity. Furthermore, the QQ compounds were not identified in these studies.

5. Concluding Remarks and Future Perspectives

QS serves a crucial and integral function in bacterial behavior in response to stress and environmental conditions. This makes QS a recent focus of research to maintain food safety and quality. Probiotics can act as QSIs by interfering with the QS activity of the target bacteria through the secretion of metabolites. The microencapsulation of probiotics is a promising strategy to enhance the anti-QS activity of probiotics. However, most of the studies in the literature are in vitro, with little focus on replicating the outcomes in the food matrix. Probiotics, through anti-QS activity, could play a potential role in gut health through the modulation of pro-inflammatory responses and gut microbiota. Taken together, the future research hotspot could be focused on the investigation of the following: (1) the anti-QS activity of probiotics, identification of anti-QS compounds, and their mechanism against foodborne pathogenic and spoilage bacteria in food products; (2) the impact of microencapsulation on the anti-QS activity of probiotics and its mechanism in the food matrix; and (3) the potential role of probiotic QS in the modulation of inflammatory responses and gut microbiota in human studies.

Author Contributions

Conceptualization, M.K.S. and G.M.; writing—original draft preparation, M.K.S.; review and editing, M.K.S. and J.A.; supervision: G.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data is contained within the article.

Conflicts of Interest

The authors declare that there is no conflict of interest.

References

  1. Garg, N.; Manchanda, G.; Kumar, A. Bacterial quorum sensing: Circuits and applications. Antonie Leeuwenhoek 2014, 105, 289–305. [Google Scholar] [CrossRef] [PubMed]
  2. Deep, A.; Chaudhary, U.; Gupta, V. Quorum sensing and bacterial pathogenicity: From molecules to disease. J. Lab. Physicians 2011, 3, 4–11. [Google Scholar] [CrossRef] [PubMed]
  3. Bourret, R.B. Two-Component Signal Transduction; Hoch, J.A., Silhavy, T., Eds.; ASM Press: Washington, WA, USA, 1995; Volume 2. [Google Scholar]
  4. Wu, L.; Luo, Y. Bacterial quorum-sensing systems and their role in intestinal bacteria-host crosstalk. Front. Microbiol. 2021, 12, 611413. [Google Scholar] [CrossRef]
  5. Bai, A.J.; Rai, V.R. Bacterial quorum sensing and food industry. Compr. Rev. Food Sci. Food Saf. 2011, 10, 183–193. [Google Scholar] [CrossRef]
  6. Falà, A.K.; Álvarez-Ordóñez, A.; Filloux, A.; Gahan, C.; Cotter, P.D. Quorum sensing in human gut and food microbiomes: Significance and potential for therapeutic targeting. Front. Microbiol. 2022, 13. [Google Scholar] [CrossRef] [PubMed]
  7. Bai, X.; Nakatsu, C.H.; Bhunia, A.K. Bacterial biofilms and their implications in pathogenesis and food safety. Foods 2021, 10, 2117. [Google Scholar] [CrossRef]
  8. 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. [Google Scholar] [CrossRef]
  9. Martins, M.L.; Pinto, U.M.; Riedel, K.; Vanetti, M.C.D. Quorum sensing and spoilage potential of psychrotrophic Enterobacteriaceae isolated from milk. BioMed Res. Int. 2018, 2018, 2723157. [Google Scholar] [CrossRef] [Green Version]
  10. Davares, A.K.L.; Arsene, M.M.J.; Viktorovna, P.I.; Vyacheslavovna, Y.N.; Vladimirovna, Z.A.; Aleksandrovna, V.E.; Nikolayevich, S.A.; Nadezhda, S.; Anatolievna, G.O.; Nikolaevna, S.I.; et al. Quorum-Sensing Inhibitors from Probiotics as a Strategy to Combat Bacterial Cell-to-Cell Communication Involved in Food Spoilage and Food Safety. Fermentation 2022, 8, 711. [Google Scholar] [CrossRef]
  11. Rizzello, C.G.; Filannino, P.; Di Cagno, R.; Calasso, M.; Gobbetti, M. Quorum-sensing regulation of constitutive plantaricin by Lactobacillus plantarum strains under a model system for vegetables and fruits. Appl. Environ. Microbiol. 2014, 80, 777–787. [Google Scholar] [CrossRef] [Green Version]
  12. Song, H.; Zhang, J.; Qu, J.; Liu, J.; Yin, P.; Zhang, G.; Shang, D. Lactobacillus rhamnosus GG microcapsules inhibit Escherichia coli biofilm formation in coculture. Biotechnol. Lett. 2019, 41, 1007–1014. [Google Scholar] [CrossRef] [PubMed]
  13. Deng, Z.; Luo, X.M.; Liu, J.; Wang, H. Quorum sensing, biofilm, and intestinal mucosal barrier: Involvement the role of probiotic. Front. Cell. Infect. Microbiol. 2020, 10, 538077. [Google Scholar] [CrossRef] [PubMed]
  14. Zhao, X.; Yu, Z.; Ding, T. Quorum-sensing regulation of antimicrobial resistance in bacteria. Microorganisms 2020, 8, 425. [Google Scholar] [CrossRef] [Green Version]
  15. Qais, F.A.; Ahmad, I. Anti-quorum sensing and biofilm inhibitory effect of some medicinal plants against Gram-negative bacterial pathogens: In Vitro and in silico investigations. Heliyon 2022, 8, e11113. [Google Scholar]
  16. Gao, Z.; Daliri, E.B.M.; Wang, J.U.N.; Liu, D.; Chen, S.; Ye, X.; Ding, T. Inhibitory effect of lactic acid bacteria on foodborne pathogens: A review. J. Food Prot. 2019, 82, 441–453. [Google Scholar] [CrossRef] [PubMed]
  17. Xu, Y.; Wang, Y.; Ding, X.; Wang, J.; Zhan, X. Inhibitory effects of reuterin on biofilm formation, quorum sensing and virulence genes of Clostridium perfringens. LWT 2022, 162, 113421. [Google Scholar] [CrossRef]
  18. Yun, B.; Oh, S.; Griffiths, M.W. Lactobacillus acidophilus modulates the virulence of Clostridium difficile. J. Dairy Sci. 2014, 97, 4745–4758. [Google Scholar] [CrossRef] [Green Version]
  19. Yong, C.; Lim, J.; Kim, B.K.; Park, D.J.; Oh, S. Suppressive effect of Lactobacillus fermentum Lim2 on Clostridioides difficile 027 toxin production. Lett. Appl. Microbiol. 2019, 68, 386–3933. [Google Scholar] [CrossRef]
  20. Li, J.; Wang, W.; Xu, S.X.; Magarvey, N.A.; McCormick, J.K. Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc. Natl. Acad. Sci. USA 2011, 108, 3360–3365. [Google Scholar] [CrossRef] [Green Version]
  21. Piewngam, P.; Zheng, Y.; Nguyen, T.H.; Dickey, S.W.; Joo, H.-S.; Villaruz, A.E.; Glose, K.A.; Fisher, E.L.; Hunt, R.L.; Li, B.; et al. Pathogen elimination by probiotic Bacillus via signalling interference. Nature 2018, 562, 532–537. [Google Scholar] [CrossRef]
  22. Jiang, X.; Yan, X.; Gu, S.; Yang, Y.; Zhao, L.; He, X.; Chen, H.; Ge, J.; Liu, D. Biosurfactants of Lactobacillus helveticus for biodiversity inhibit the biofilm formation of Staphylococcus aureus and cell invasion. Future Microbiol. 2019, 14, 1133–1146. [Google Scholar] [CrossRef] [PubMed]
  23. Ahn, K.B.; Baik, J.E.; Yun, C.H.; Han, S.H. Lipoteichoic acid inhibits Staphylococcus aureus biofilm formation. Front. Microbiol. 2018, 9, 327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Kim, J.; Kim, J.; Kim, Y.; Oh, S.; Song, M.; Choe, J.H.; Whang, K.-Y.; Kim, K.H.; Oh, S. Influences of quorum-quenching probiotic bacteria on the gut microbial community and immune function in weaning pigs. Anim. Sci. J. 2018, 89, 412–422. [Google Scholar] [CrossRef] [PubMed]
  25. Kim, Y.; Kim, S.H. Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157: H7. Biochem. Biophys. Res. Commun. 2009, 379, 324–329. [Google Scholar] [CrossRef]
  26. Kim, Y.; Lee, J.W.; Kang, S.G.; Oh, S.; Griffiths, M.W. Bifidobacterium spp. influences the production of autoinducer-2 and biofilm formation by Escherichia coli O157: H7. Anaerobe 2012, 18, 539–545. [Google Scholar] [CrossRef] [PubMed]
  27. Kim, Y.; Oh, S.; Park, S.; Seo, J.B.; Kim, S.H. Lactobacillus acidophilus reduces expression of enterohemorrhagic Escherichia coli O157: H7 virulence factors by inhibiting autoinducer-2-like activity. Food Control. 2008, 19, 1042–1050. [Google Scholar] [CrossRef]
  28. Liang, Y.; Pan, Y.; Li, Q.; Wu, B.; Hu, M. RNA-seq-based transcriptomic analysis of AHL-induced biofilm and pyocyanin inhibition in Pseudomonas aeruginosa by Lactobacillus brevis. Int. Microbiol. 2022, 25, 447–456. [Google Scholar] [CrossRef]
  29. Díaz, M.A.; González, S.N.; Alberto, M.R.; Arena, M.E. Human probiotic bacteria attenuate Pseudomonas aeruginosa biofilm and virulence by quorum-sensing inhibition. Biofouling 2020, 36, 597–609. [Google Scholar] [CrossRef]
  30. Devi, S.; Chhibber, S.; Harjai, K. Optimization of cultural conditions for enhancement of anti-quorum sensing potential in the probiotic strain Lactobacillus rhamnosus GG against Pseudomonas aeruginosa. 3 Biotech 2022, 12, 133. [Google Scholar] [CrossRef]
  31. Azami, S.; Arefian, E.; Kashef, N. Postbiotics of Lactobacillus casei target virulence and biofilm formation of Pseudomonas aeruginosa by modulating quorum sensing. Arch. Microbiol. 2022, 204, 157. [Google Scholar] [CrossRef]
  32. Boopathi, S.; Vashisth, R.; Manoharan, P.; Kandasamy, R.; Sivakumar, N. Stigmatellin Y–An anti-biofilm compound from Bacillus subtilis BR4 possibly interferes in PQS–PqsR mediated quorum sensing system in Pseudomonas aeruginosa. Bioorg. Med. Chem. Lett. 2017, 27, 2113–2118. [Google Scholar] [CrossRef] [PubMed]
  33. Djokic, L.; Stankovic, N.; Galic, I.; Moric, I.; Radakovic, N.; Šegan, S.; Pavic, A.; Senerovic, L. Novel Quorum Quenching YtnP Lactonase from Bacillus paralicheniformis Reduces Pseudomonas aeruginosa Virulence and Increases Antibiotic Efficacy In Vivo. Front. Microbiol. 2022, 13, 1812. [Google Scholar] [CrossRef] [PubMed]
  34. Algburi, A.; Zehm, S.; Netrebov, V.; Bren, A.B.; Chistyakov, V.; Chikindas, M.L. Subtilosin prevents biofilm formation by inhibiting bacterial quorum sensing. Probiotics Antimicrob. Proteins 2017, 9, 81–90. [Google Scholar] [CrossRef] [PubMed]
  35. Lee, J.E.; Lee, N.K.; Paik, H.D. Antimicrobial and anti-biofilm effects of probiotic Lactobacillus plantarum KU200656 isolated from kimchi. Food Sci. Biotechnol. 2021, 30, 97–106. [Google Scholar] [CrossRef]
  36. Merino, L.; Trejo, F.M.; De Antoni, G.; Golowczyc, M.A. Lactobacillus strains inhibit biofilm formation of Salmonella sp. isolates from poultry. Food Res. Int. 2019, 123, 258–265. [Google Scholar] [CrossRef] [PubMed]
  37. Tazehabadi, M.H.; Algburi, A.; Popov, I.V.; Ermakov, A.M.; Chistyakov, V.A.; Prazdnova, E.V.; Weeks, R.; Chikindas, M.L. Probiotic bacilli inhibit Salmonella biofilm formation without killing planktonic cells. Front. Microbiol. 2021, 12, 615328. [Google Scholar] [CrossRef]
  38. Pelyuntha, W.; Chaiyasut, C.; Kantachote, D.; Sirilun, S. Cell-free supernatants from cultures of lactic acid bacteria isolated from fermented grape as biocontrol against Salmonella Typhi and Salmonella Typhimurium virulence via autoinducer-2 and biofilm interference. PeerJ 2019, 7, e7555. [Google Scholar] [CrossRef] [Green Version]
  39. Siddique, A.; Azim, S.; Ali, A.; Adnan, F.; Arif, M.; Imran, M.; Ganda, E.; Rahman, A. Lactobacillus reuteri and Enterococcus faecium from Poultry Gut Reduce Mucin Adhesion and Biofilm Formation of Cephalosporin and Fluoroquinolone-Resistant Salmonella enterica. Animals 2021, 11, 3435. [Google Scholar] [CrossRef]
  40. Xu, X.; Peng, Q.; Zhang, Y.; Tian, D.; Zhang, P.; Huang, Y.; Ma, L.; Qiao, Y.; Shi, B. A novel exopolysaccharide produced by Lactobacillus coryniformis NA-3 exhibits antioxidant and biofilm-inhibiting properties In Vitro. Food Nutr. Res. 2020, 64. [Google Scholar] [CrossRef] [Green Version]
  41. Piewngam, P.; Chiou, J.; Ling, J.; Liu, R.; Pupa, P.; Zheng, Y.; Otto, M. Enterococcal bacteremia in mice is prevented by oral administration of probiotic Bacillus spores. Sci. Transl. Med. 2021, 13, eabf4692. [Google Scholar] [CrossRef]
  42. Adnan, M.; Siddiqui, A.J.; Hamadou, W.S.; Ashraf, S.A.; Hassan, M.I.; Snoussi, M.; Badraoui, R.; Jamal, A.; Bardakci, F.; Awadelkareem, A.; et al. Functional and structural characterization of pediococcus pentosaceus-derived biosurfactant and its biomedical potential against bacterial adhesion, quorum sensing, and biofilm formation. Antibiotics 2021, 10, 1371. [Google Scholar] [CrossRef] [PubMed]
  43. Luan, C.; Jiang, N.; Zhou, X.; Zhang, C.; Zhao, Y.; Li, Z.; Li, C. Antibacterial and anti-biofilm activities of probiotic Lactobacillus curvatus BSF206 and Pediococcus pentosaceus AC1-2 against Streptococcus mutans. Microb. Pathog. 2022, 164, 105446. [Google Scholar] [CrossRef] [PubMed]
  44. Gu, M.; Cheng, J.; Lee, Y.G.; Cho, J.H.; Suh, J.W. Discovery of Novel Iminosugar Compounds Produced by Lactobacillus paragasseri MJM60645 and Their Anti-Biofilm Activity against Streptococcus mutans. Microbiol. Spectr. 2022, 10, e01122-22. [Google Scholar] [CrossRef] [PubMed]
  45. Tahmourespour, A.; Kasra-Kermanshahi, R.; Salehi, R. Lactobacillus rhamnosus biosurfactant inhibits biofilm formation and gene expression of caries-inducing Streptococcus mutans. Dent. Res. J. 2019, 16, 87. [Google Scholar] [CrossRef]
  46. Zhang, G.; Lu, M.; Liu, R.; Tian, Y.; Vu, V.H.; Li, Y.; Liu, B.; Kushmaro, A.; Li, Y.; Sun, Q. Inhibition of Streptococcus mutans biofilm formation and virulence by Lactobacillus plantarum K41 isolated from traditional Sichuan pickles. Front. Microbiol. 2020, 11, 774. [Google Scholar] [CrossRef]
  47. Dong, W.; Cai, Y.; Xu, Z.; Fu, B.; Chen, Q.; Cui, Y.; Ruan, Z.; Liang, Y.; Peng, N.; Zhao, S. Heterologous expression of AHL lactonase AiiK by Lactobacillus casei MCJΔ1 with great quorum quenching ability against Aeromonas hydrophila AH-1 and AH-4. Microb. Cell Factories 2020, 19, 191. [Google Scholar] [CrossRef]
  48. Hossain, M.I.; Mizan, M.F.R.; Roy, P.K.; Nahar, S.; Toushik, S.H.; Ashrafudoulla, M.; Ha, S.D. Listeria monocytogenes biofilm inhibition on food contact surfaces by application of postbiotics from Lactobacillus curvatus B. 67 and Lactobacillus plantarum M. 2. Food Res. Int. 2021, 148, 110595. [Google Scholar] [CrossRef]
  49. Melian, C.; Segli, F.; Gonzalez, R.; Vignolo, G.; Castellano, P. Lactocin AL705 as quorum sensing inhibitor to control Listeria monocytogenes biofilm formation. J. Appl. Microbiol. 2019, 127, 911–920. [Google Scholar] [CrossRef]
  50. Sudan, S.; Li, J. Dispersal of pathogen-associated multispecies biofilm by novel probiotic Bacillus subtilis in a contact-dependent manner. J. Appl. Microbiol. 2022, 133, 2501–2515. [Google Scholar] [CrossRef]
  51. Shangguan, W.; Xie, T.; Zhang, R.; Lu, C.; Han, X.; Zhong, Q. Anti-biofilm potential of kefir-derived Lactobacillus paracasei L10 against Vibrio parahaemolyticus. Lett. Appl. Microbiol. 2021, 73, 750–758. [Google Scholar] [CrossRef]
  52. Lee, D.; Im, J.; Park, D.H.; Jeong, S.; Park, M.; Yoon, S.; Park, J.; Han, S.H. Lactobacillus plantarum Lipoteichoic Acids Possess Strain-Specific Regulatory Effects on the Biofilm Formation of Dental Pathogenic Bacteria. Front. Microbiol. 2021, 12, 758161. [Google Scholar] [CrossRef] [PubMed]
  53. Jeong, D.; Kim, D.H.; Song, K.Y.; Seo, K.H. Antimicrobial and anti-biofilm activities of Lactobacillus kefiranofaciens DD2 against oral pathogens. J. Oral Microbiol. 2018, 10, 1472985. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Xue, T.; Zhao, L.; Sun, H.; Zhou, X.; Sun, B. LsrR-binding site recognition and regulatory characteristics in Escherichia coli AI-2 quorum sensing. Cell Res. 2009, 19, 1258–1268. [Google Scholar] [CrossRef] [PubMed]
  55. Escobar-Muciño, E.; Arenas-Hernández, M.M.; Luna-Guevara, M.L. Mechanisms of Inhibition of Quorum Sensing as an Alternative for the Control of E. coli and Salmonella. Microorganisms 2022, 10, 884. [Google Scholar] [CrossRef]
  56. Zuo, J.; Yin, H.; Hu, J.; Miao, J.; Chen, Z.; Qi, K.; Wang, Z.; Gong, J.; Phouthapane, V.; Jiang, W.; et al. Lsr operon is associated with AI-2 transfer and pathogenicity in avian pathogenic Escherichia coli. Veter. Res. 2019, 50, 109. [Google Scholar] [CrossRef] [Green Version]
  57. Van Hal, S.J.; Jensen, S.O.; Vaska, V.L.; Espedido, B.A.; Paterson, D.L.; Gosbell, I.B. Predictors of mortality in Staphylococcus aureus bacteremia. Clin. Microbiol. Rev. 2012, 25, 362–386. [Google Scholar] [CrossRef] [Green Version]
  58. Bleul, L.; Francois, P.; Wolz, C. Two-component systems of S. aureus: Signaling and sensing mechanisms. Genes 2022, 13, 34. [Google Scholar] [CrossRef]
  59. Yu, D.; Zhao, L.; Xue, T.; Sun, B. Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol. 2012, 12, 288. [Google Scholar] [CrossRef] [Green Version]
  60. Ma, L.; Wang, J.; Wang, S.; Anderson, E.M.; Lam, J.S.; Parsek, M.R.; Wozniak, D.J. Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post-transcriptionally regulated. Environ. Microbiol. 2012, 14, 1995–2005. [Google Scholar] [CrossRef] [Green Version]
  61. Wilson, M.G.; Pandey, S. Pseudomonas Aeruginosa; StatPearls: Treasure Island, FL, USA, 2022. [Google Scholar]
  62. Venturi, V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev. 2006, 30, 274–291. [Google Scholar] [CrossRef] [Green Version]
  63. Manasian, P.; Bustos, A.S.; Pålsson, B.; Håkansson, A.; Peñarrieta, J.M.; Nilsson, L.; Linares-Pastén, J.A. First evidence of Acyl-Hydrolase/Lipase activity from human probiotic bacteria: Lactobacillus rhamnosus GG and Bifidobacterium longum NCC 2705. Front. Microbiol. 2020, 11, 1534. [Google Scholar] [CrossRef]
  64. Toushik, S.H.; Kim, K.; Park, S.-H.; Park, J.-H.; Ashrafudoulla; Ulrich, M.S.I.; Mizan, F.R.; Hossain, I.; Shim, W.-B.; Kang, I.; et al. Prophylactic efficacy of Lactobacillus curvatus B67-derived postbiotic and quercetin, separately and combined, against Listeria monocytogenes and Salmonella enterica ser. Typhimurium on processed meat sausage. Meat Sci. 2023, 197, 109065. [Google Scholar] [CrossRef] [PubMed]
  65. Pearson, J.P.; Van Delden, C.; Iglewski, B.H. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 1999, 181, 1203–1210. [Google Scholar] [CrossRef] [Green Version]
  66. Domenech, A.; Brochado, A.R.; Sender, V.; Hentrich, K.; Henriques-Normark, B.; Typas, A.; Veening, J.W. Proton motive force disruptors block bacterial competence and horizontal gene transfer. Cell Host Microbe 2020, 27, 544–555.e3. [Google Scholar] [CrossRef]
  67. Sutyak Noll, K.; Sinko, P.J.; Chikindas, M.L. Elucidation of the molecular mechanisms of action of the natural antimicrobial peptide subtilosin against the bacterial vaginosis-associated pathogen Gardnerella vaginalis. Probiotics Antimicrob. Proteins 2011, 3, 41–47. [Google Scholar] [CrossRef] [Green Version]
  68. Ranadheera, R.D.C.S.; Baines, S.K.; Adams, M.C. Importance of food in probiotic efficacy. Food Res. Int. 2010, 43, 1–7. [Google Scholar] [CrossRef]
  69. Amit, S.K.; Uddin, M.; Rahman, R.; Islam, S.M.; Khan, M.S. A review on mechanisms and commercial aspects of food preservation and processing. Agric. Food Secur. 2017, 6, 51. [Google Scholar] [CrossRef]
  70. Yuan, L.; Sadiq, F.A.; Burmølle, M.; Liu, T.; He, G. Insights into bacterial milk spoilage with particular emphasis on the roles of heat-stable enzymes, biofilms, and quorum sensing. J. Food Prot. 2018, 81, 1651–1660. [Google Scholar] [CrossRef] [PubMed]
  71. 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. [Google Scholar] [CrossRef]
  72. Pothakos, V.; Devlieghere, F.; Villani, F.; Björkroth, J.; Ercolini, D. Lactic acid bacteria and their controversial role in fresh meat spoilage. Meat Sci. 2015, 109, 66–74. [Google Scholar] [CrossRef]
  73. 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. B 2018, 19, 630–642. [Google Scholar] [CrossRef] [PubMed]
  74. Yang, Q.; Wang, Y.; An, Q.; Sa, R.; Zhang, D.; Xu, R. Research on the role of LuxS/AI-2 quorum sensing in biofilm of Leuconostoc citreum 37 based on complete genome sequencing. 3 Biotech 2021, 11, 189. [Google Scholar] [CrossRef] [PubMed]
  75. Ng, Y.K.; Grasso, M.; Wright, V.; Garcia, V.; Williams, P.; Atkinson, S. The quorum sensing system of Yersinia enterocolitica 8081 regulates swimming motility, host cell attachment, and virulence plasmid maintenance. Genes 2018, 9, 307. [Google Scholar] [CrossRef] [Green Version]
  76. Opara, E.U.; Asuquo, A.A. An overview of characterization and identification of soft rot bacterium Erwinia in some vegetable crops. Greener J. Biol. Sci. 2016, 6, 46–55. [Google Scholar] [CrossRef]
  77. Põllumaa, L.; Alamäe, T.; Mäe, A. Quorum sensing and expression of virulence in pectobacteria. Sensors 2012, 12, 3327–3349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Laasik, E.; Andresen, L.; Mäe, A. Type II quorum sensing regulates virulence in Erwinia carotovora ssp. carotovora. FEMS Microbiol. Lett. 2006, 258, 227–234. [Google Scholar] [CrossRef]
  79. Rasch, M.; Andersen, J.B.; Nielsen, K.F.; Flodgaard, L.R.; Christensen, H.; Givskov, M.; Gram, L. Involvement of bacterial quorum-sensing signals in spoilage of bean sprouts. Appl. Environ. Microbiol. 2005, 71, 3321–3330. [Google Scholar] [CrossRef] [Green Version]
  80. Fu, L.; Wang, C.; Liu, N.; Ma, A.; Wang, Y. Quorum sensing system-regulated genes affect the spoilage potential of Shewanella baltica. Food Res. Int. 2018, 107, 1–9. [Google Scholar] [CrossRef]
  81. Li, Y.; Liu, T.; Meng, X.; Qian, Y.; Yan, S.; Liu, Z. AI-2/Lux-S Quorum Sensing of Lactobacillus plantarum SS-128 Prolongs the Shelf Life of Shrimp (Litopenaeus vannamei): From Myofibril Simulation to Practical Application. Foods 2022, 11, 2273. [Google Scholar] [CrossRef]
  82. Gui, M.; Wu, R.; Liu, L.; Wang, S.; Zhang, L.; Li, P. Effects of quorum quenching by AHL lactonase on AHLs, protease, motility and proteome patterns in Aeromonas veronii LP-11. Int. J. Food Microbiol. 2017, 252, 61–68. [Google Scholar] [CrossRef]
  83. Husain, F.M.; Ahmad, I.; Al-Shabib, N.A.; Khan, M.S.; Mohammed, Y.A.; Althubiani, A.S. Quorum sensing and biofilm inhibition by lactonase producing Bacillus amyloliquefaciens SBF1 strain isolated from date palm rhizosphere of Saudi Arabia. J. Pure Appl. Microbiol. 2016, 10, 1745–1755. [Google Scholar]
  84. Garge, S.S.; Nerurkar, A.S. Attenuation of quorum sensing regulated virulence of Pectobacterium carotovorum subsp. carotovorum through an AHL lactonase produced by Lysinibacillus sp. Gs50. PloS ONE 2016, 11, e0167344. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Kachhadia, R.; Kapadia, C.; Singh, S.; Gandhi, K.; Jajda, H.; Alfarraj, S.; Ansari, M.J.; Danish, S.; Datta, R. Quorum sensing inhibitory and quenching activity of Bacillus cereus RC1 extracts on Soft Rot-Causing Bacteria Lelliottia amnigena. ACS Omega 2022, 7, 25291–25308. [Google Scholar] [CrossRef] [PubMed]
  86. Coquant, G.; Aguanno, D.; Brot, L.; Belloir, C.; Delugeard, J.; Roger, N.; Pham, H.-P.; Briand, L.; Moreau, M.; de Sordi, L.; et al. 3-oxo-C12: 2-HSL, quorum sensing molecule from human intestinal microbiota, inhibits pro-inflammatory pathways in immune cells via bitter taste receptors. Sci. Rep. 2022, 12, 9440. [Google Scholar] [CrossRef] [PubMed]
  87. Landman, C.; Grill, J.P.; Mallet, J.M.; Marteau, P.; Humbert, L.; Le Balc’h, E.; Maubert, M.-A.; Perez, K.; Chaara, W.; Brot, L.; et al. IBD Network. Inter-kingdom effect on epithelial cells of the N-Acyl homoserine lactone 3-oxo-C12: 2, a major quorum-sensing molecule from gut microbiota. PLoS ONE 2018, 13, e0202587. [Google Scholar] [CrossRef] [Green Version]
  88. Thompson, J.A.; Oliveira, R.A.; Djukovic, A.; Ubeda, C.; Xavier, K.B. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 2015, 10, 1861–1871. [Google Scholar] [CrossRef]
  89. Deng, Z.; Dai, J.; Wei, Y.; Ma, Y.; Mao, Y.; Zhang, J.; Hua, W.; Wang, H. Comparison between Lactobacillus rhamnosus GG and LuxS-deficient strain in regulating gut barrier function and inflammation in early-weaned piglets. Front. Immunol. 2022, 13, 1080789. [Google Scholar] [CrossRef]
  90. Ji, Y.-C.; Sun, Q.; Fu, C.-Y.; She, X.; Liu, X.-C.; He, Y.; Ai, Q.; Li, L.-Q.; Wang, Z.-L. Exogenous Autoinducer-2 Rescues Intestinal Dysbiosis and Intestinal Inflammation in a Neonatal Mouse Necrotizing Enterocolitis Model. Front. Cell. Infect. Microbiol. 2021, 11, 694395. [Google Scholar] [CrossRef]
  91. Fteita, D.; Könönen, E.; Gürsoy, M.; Ma, X.; Sintim, H.O.; Gürsoy, U.K. Quorum sensing molecules regulate epithelial cytokine response and biofilm-related virulence of three Prevotella species. Anaerobe 2018, 54, 128–135. [Google Scholar] [CrossRef]
  92. Li, Q.; Peng, W.; Wu, J.; Wang, X.; Ren, Y.; Li, H.; Peng, Y.; Tang, X.; Fu, X. Autoinducer-2 of gut microbiota, a potential novel marker for human colorectal cancer, is associated with the activation of TNFSF9 signaling in macrophages. Oncoimmunology 2019, 8, e1626192. [Google Scholar] [CrossRef]
  93. Zargar, A.; Quan, D.N.; Carter, K.K.; Guo, M.; Sintim, H.O.; Payne, G.F.; Bentley, W.E. Bacterial secretions of nonpathogenic Escherichia coli elicit inflammatory pathways: A closer investigation of interkingdom signaling. Mbio 2015, 6, e00025-15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Vestby, L.K.; Grønseth, T.; Simm, R.; Nesse, L.L. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics 2020, 9, 59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Liu, L.; Wu, R.; Zhang, J.; Li, P. Overexpression of luxS promotes stress resistance and biofilm formation of Lactobacillus paraplantarum L-ZS9 by regulating the expression of multiple genes. Front. Microbiol. 2018, 9, 2628. [Google Scholar] [CrossRef] [PubMed]
  96. Sun, Z.; He, X.; Brancaccio, V.F.; Yuan, J.; Riedel, C.U. Bifidobacteria exhibit LuxS-dependent autoinducer 2 activity and biofilm formation. PLoS ONE 2014, 9, e88260. [Google Scholar] [CrossRef] [Green Version]
  97. Coquant, G.; Grill, J.P.; Seksik, P. Impact of N-acyl-homoserine lactones, quorum sensing molecules, on gut immunity. Front. Immunol. 2020, 11, 1827. [Google Scholar] [CrossRef]
  98. Krzyżek, P. Challenges and limitations of anti-quorum sensing therapies. Front. Microbiol. 2019, 10, 2473. [Google Scholar] [CrossRef] [Green Version]
  99. Desai, K.G.H.; Jin Park, H. Recent developments in microencapsulation of food ingredients. Dry. Technol. 2005, 23, 1361–1394. [Google Scholar] [CrossRef]
  100. Shori, A.B. Microencapsulation improved probiotics survival during gastric transit. HAYATI J. Biosci. 2017, 24, 1–5. [Google Scholar] [CrossRef]
  101. Song, J.J.; Tian, W.J.; Kwok, L.Y.; Wang, Y.L.; Shang, Y.N.; Menghe, B.; Wang, J.G. Effects of microencapsulated Lactobacillus plantarum LIP-1 on the gut microbiota of hyperlipidaemic rats. Br. J. Nutr. 2017, 118, 481–492. [Google Scholar] [CrossRef] [Green Version]
  102. Zhang, M.; Yin, C.; Qian, J. Microencapsulation of Lactobacillus plantarum LN66 and its survival potential under different packaging conditions. J. Microencapsul. 2022, 39, 601–608. [Google Scholar] [CrossRef]
  103. Gao, M.; Song, H.; Liu, X.; Yu, W.; Ma, X. Improved quorum sensing capacity by culturing Vibrio harveyi in microcapsules. J. Biosci. Bioeng. 2016, 121, 406–412. [Google Scholar] [CrossRef]
  104. Yang, X.; Li, J.; Shi, G.; Zeng, M.; Liu, Z. Improving 3-phenyllactic acid production of Lactobacillus plantarum AB-1 by enhancing its quorum-sensing capacity. J. Food Sci. Technol. 2019, 56, 2605–2610. [Google Scholar] [CrossRef] [PubMed]
  105. Gao, M.; Zheng, H.; Ren, Y.; Lou, R.; Wu, F.; Yu, W.; Liu, X.; Ma, X. A crucial role for spatial distribution in bacterial quorum sensing. Sci. Rep. 2016, 6, 34695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  106. Li, C.; Gao, M.; Zheng, G.; Ma, X.; Liu, X.; Yu, W. Enhanced quorum sensing capacity via regulating microenvironment to facilitate stress resistance of probiotic in alginate-based microcapsules. Int. J. Biol. Macromol. 2022, 225, 605–614. [Google Scholar] [CrossRef]
  107. Song, H.; Lou, N.; Liu, J.; Xiang, H.; Shang, D. Label-free quantitative proteomic analysis of the inhibition effect of Lactobacillus rhamnosus GG on Escherichia coli biofilm formation in co-culture. Proteome Sci. 2021, 19, 4. [Google Scholar] [CrossRef] [PubMed]
Table
Table 1. Probiotics involved in the inhibition of QS mechanisms of foodborne pathogenic bacteria.
Table 1. Probiotics involved in the inhibition of QS mechanisms of foodborne pathogenic bacteria.
MicroorganismQSITargetType of StudyMechanismReference
Lb. reuteri LR 21ReuterinC. perfringens 13124In vitroRepression of toxins-producing genes (cpa and pfo) and agrB and luxS.[17]
Lb. acidophilus GP1B CE/CFS C. difficile
(ribotype 027) 		In vitroInhibition of AI-2 production and downregulation of luxS and tcdA, tcdB, and txeR (virulence genes).
Growth inhibition of C. difficile in the colon.		[18]
Lb. fermentum Lim2 Inactivated CE C. difficile 027 In vitro Anti AI-2 activity due to repression of lux gene. Expression of virulence genes also reduced. QSIs are not measured. [19]
Lb. reuteri RC-14CFSStaph. aureus MN8In vitroCyclo-dipeptides inhibited the expression of agr and tst genes as well as disrupting saeRS system.[20]
B. subtilisFengycinStaph. aureusCross-sectional analysis
(Thai population)		Fengycin competes with AIP for binding to agrC.[21]
Lb. helveticus Biosurfactant Staph. aureusIn vitroInhibition of biofilm formation by interfering with AI-2 signaling and biofilm-related genes expression (dltB, sarA, agrA, and icdA).[22]
In vivo Prevention of hemolytic activity through biofilm formation inhibition.
Lb. plantarum KCTC10887BPLPAStaph. aureusIn vitro Biofilm formation was inhibited. LPA induced AI-2 release in Staph. Aureus, which repressed biofilm-related genes.[23]
Lb. acidophillus 30SCN/AE. coli O157:H7 43894In vivoInhibition of AI-2 synthesis and modulation of microbial gut community.[24]
Lb. rhamnosus GG microcapsules N/A E. coli In vitroRepression of lsrK and luxS genes (disruption in AI-2/luxS-typeQS network).[13]
Lb. acidophilus A4EPSE. coli O157:H7 In vitroRepression levels of curli genes (crl, csgA, and csgB) and chemotaxis (cheY) related to biofilm formation.[25]
Bifidobacterium longum ATCC15707 CE E. coli O157:H7In vitro Inhibition of AI-2 activity and virulence gene expression (NifU, DsbA, and FlgI). [26]
Lb. acidophilus A4 N/A E. coli (EHEC) In vitro Downregulation of biofilm-related genes (crl, csgA, and csgB) and chemotaxis (cheY). [27]
Lb. brevis 3M004 N/A P. aeruginosa PA002 biofilm formationIn vitroDegradation of AIs and repression of biofilm formation, pyocyanin, and polysaccharide synthesis-related genes (lasA, lasB, and PhzAB).[28]
Lb. casei CRL 431
Lb. acidophilus CRL 730		DKPsP. aeruginosaIn vitroDKPs compete with AI for binding QS receptors.[29]
Lb. rhamnosus GGCFSP. aeruginosaIn vitroInhibition of AHL synthesis.[30]
Lb. casei PTCC 1608Lyophilized postbioticsP. aeruginosaIn vitroRepression of QS genes controlling biofilm formation and virulence (rhlI, rhlR, and pelf), potentially due to organic acid content.[31]
B. subtilis BR4 Stigmatellin Y P. aeruginosa (ATCC 27853)In vitro Stigmatellin Y competes with PQS signal for binding with PqsR gene, and thus, PqsR-PQS QS pathway is disrupted. [32]
B. paralicheniformis ZP1 Lactonase P. aeruginosaIn vitro Inhibition of biofilm formation due to AHL hydrolysis by lactonase. [33]
B. subtilis KATMIRA1933SubtilisinL. monocytogenes biofilm formation
E. coli biofilm formation		In vitroInhibition of proton motive forces and efflux pumps.[34]
Lb. plantarum C2N/AE. coli DSM 30083
Enterobacter aerogenes DSM 30053
Yersinia enterolitica DSM 4780
Leuconostoc lactis 20202
Ent. durans DSM 20633
B. megaterium F6		In vitroAntibacterial activity by plantaricin produced through QS mechanism. (AI not measured).[11]
Lb. plantarum KU200656CFSStaph. aureus
Listeria monocytogenes
E. coli
S. Typhimurium		In vitroBiofilm-related genes are downregulated by anti-biofilm activity. (Exact QSI mechanism is not measured).[35]
Lb. kefiri 8321 and 83113
Lb. plantarum 83114 		CFSS. Enteritidis 115In vitroBiofilm formation inhibition. (QSI mechanism not investigated).[36]
B. subtilis KATMIRA1933
B. amyloliquefaciens
B-1895		 CE/CFS S. (Thompson, Enteritidis phage type 4, and Hadar) In vitroBiofilm inhibition due to the subtilosin effect. AI/luxS QS pathway is necessary for biofilm formation.[37]
W. viridescens WM33
W. confusa WM36 (LAB) 		CFS S. Typhi and S. TyphimuriumIn vitro Inhibition of AI-2 activity and biofilm formation. [38]
Lb. reuteri PFS4
Ent. faecium PFS13 and
PFS14.		CFSS. Typhimurium and S. EnteritidisIn vitro Inhibition of biofilm formation. (Mechanism not investigated). [39]
Lb. coryniformis NA-3 EPS B. cereus and
S. Typhimurium		In vitroInhibition of biofilm formation. (Mechanism not investigated).[40]
B. subtilis ZK3814 Fengycin and surfactinEnt. faecalis OG1RFIn vitroInhibition of fsr system, which regulates expression of proteolytic activity related-genes (gelE/sprE).[41]
Pd. pentosaceus Crude biosurfactant B. subtilis andStaph. aureus
P. aeruginosa, Staph. aureus, and E. coli		In vitroAnti-QS and anti-biofilm activity.[42]
Lb. curvatus BSF206 and Pd. pentosaceus AC1-2CFSStr. mutansIn vitro Biofilm formation inhibition by downregulation of related genes (tfA, gtfB, ftf, and brpA). (Exact mechanism not known).[43]
Lb. paragasseri MJM60645 Crude extract Str. mutansIn vitro Downregulation of biofilm-associated genes (gtfB, gtfC, gtfD,
gbpB, brpA, spaP, ftf, and smu0630) by iminosugar, a novel chemical compound produced. 		[44]
Lb. rhamnosus GG Biosurfactant Str. mutans In vitro Anti-biofilm activity due to downregulation of biofilm-related genes (gtfB/C and ftf). [45]
Lb. plantarum K41 N/A Str. mutans In vitro and in vivoInhibition of biofilm formation by inhibition of exopolysaccharide production.[46]
Lb. casei MCJΔ1 (expressed with AHL-lactonase AiiK gene) Lactonase Aeromonas hydrophila In vitro Enzymatic QQ activity of lactonase. [47]
Lb. curvatus B.67 and Lb. plantarum M.2 Postbiotics L. monocytogenesIn vitro Repression of biofilm-related genes (flaA, fbp, agrA, prfA, and hlyA). [48]
Lb. curvatus CRL1579LactocinL. monocytogenesIn vitro QSI mechanism not investigated. [49]
B. subtilis-9 N/AE. coli (ETEC), S. Typhimurium, Staph. aureus (MSRA)In vitro Biofilm inhibition in a cell-to-cell contact manner. Biofilm-related genes were repressed in ETEC (bssS, luxS, and ihfB). [50]
Lb. paracasei L10 CFS V. parahaemolyticusIn vitro Biofilm formation significantly inhibited. (Mechanism not investigated). [51]
Lb. plantarum LRCC 5193 LPA Str. mutans, E. faecalis, and Str. Gordonii In vitro Biofilm formation inhibition. (QSI mechanism is suggested but not investigated). [52]
Lb. kefiranofaciens DD2 CFS Str. mutans and Str. sobrinusIn vitroAntibiofilm activity through repression biofilm-associated
genes (ftf, comDE, brpA, and vicR).		[53]
Lb: Lactobacillus; C.: Clostridium; Staph.: Staphylococcus; L.: Listeria; B.: Bacillus; P.: Pseudomonas; Ent.: Enterococcus; Str.: Streptococcus; Pd.: Pediococcus; V.: Vibrio; W.: Weissella; CE: cell extract; CFS: cell-free supernatant; LPA: lipoteichoic acid; N/A: not available; EPS: exopolysaccharides; SaeRS: two-component signaling system; DKP: diketopiperazine; AI: autoinducer; QQ: quorum quenching; PQS: Pseudomonas quinolone signal; BIC: biofilm inhibitory compound; QSI: QS inhibitor.
Table
Table 2. Probiotics involved in the inhibition of QS mechanisms of food spoilage bacteria.
Table 2. Probiotics involved in the inhibition of QS mechanisms of food spoilage bacteria.
MicroorganismQSITargetType of StudyMechanismReference
Lb. plantarum ss-128N/ASpoilage bacterial community (Shewanella, Carnobacterium, and Vagococcus)Food matrix (shrimp)AI-2/LuxS-type QS system promotes growth of Lb. plantarum that reduces PH, protease activity, and growth of spoilage microorganism.[81]
B. sp. AI96LactonaseAeromonas veronii LP-11In vitroSpoilage inhibition due to QS disruption by lactonase. [82]
B. amyloliquefaciens SBF1 Culture extract P. aeruginosa PAO1 In vitroBiofilm inhibition due to anti-QS activity.[83]
Lysinibacillus sp. Gs50LactonasePectobacterium carotovorumFood matrixVegetables soft rot reduced due to QQ of AHLs. [84]
B. cereus RC1DKPsLelliottia amnigenaFood matrix (vegetables)Soft rot decreased due to anti-QS activity. DKPs compete for binding QS receptors with the AI.[85]
Table
Table 3. Association of QS molecules with gut health.
Table 3. Association of QS molecules with gut health.
QS MoleculeSourceType of StudyHealth OutcomesReference
3-oxo-C12:2-HSL SyntheticIn vitroAnti-inflammatory effect.[86]
3-oxo-C12:2 HSLHuman gut microbiotaCross sectional (analysis of fecal samples of patients with IBDs)Positive correlation with normobiosis (increased levels of Firmicutes).[87]
In vitroAnti-inflammatory and positive effect on gut epithelial cell function.
AI-2Mutant E. coli engineered to overproduce AI-2Animal studyIncreased ratio of Firmicutes to Bacteroidetes in antibiotic-treated mice group.[88]
AI-2Lb. rhamnosus GG (LGG)Animal study Protective effect of ΔluxS LGG on intestinal cells is significantly lower than effect of wild-type LGG. [89]
AI-2Exogenous AI-2 added to milkAnimal studyDysbiosis was reversed, and inflammation was ameliorated.[90]
DPD (precursor of AI-2) Exogenous (synthetic)In vitro (co-culture of WCE of Prevotella. intermedia, Prevotella nigrescens, and estradiol with HMK cells)DPD modulated the pro-inflammatory effect of estradiol + and inhibited biofilm formation.[91]
AI-2 Fusobacterium nucleatum Cross-sectional (analysis of fecal, saliva, and serum samples from patients with CRC and healthy people)AI-2 levels are higher in CRC samples compared with control samples.[92]
AI-2 Non-pathogenic E. coli BL21 and W3110 In vitro (co-culture with HCT-cells)Increased expression of pro-inflammatory cytokine IL-8 but downregulated after 24 h.[93]
IBDs: inflammatory bowel diseases; HMK: human gingival keratinocytes; HCT: human colon cancer; CRC: colorectal cancer; WCE: whole cell extract; DPD: dihydroxy-2,3-pentanedione.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Salman, M.K.; Abuqwider, J.; Mauriello, G. Anti-Quorum Sensing Activity of Probiotics: The Mechanism and Role in Food and Gut Health. Microorganisms 2023, 11, 793. https://doi.org/10.3390/microorganisms11030793

AMA Style

Salman MK, Abuqwider J, Mauriello G. Anti-Quorum Sensing Activity of Probiotics: The Mechanism and Role in Food and Gut Health. Microorganisms. 2023; 11(3):793. https://doi.org/10.3390/microorganisms11030793

Chicago/Turabian Style

Salman, Mohammed Kamal, Jumana Abuqwider, and Gianluigi Mauriello. 2023. "Anti-Quorum Sensing Activity of Probiotics: The Mechanism and Role in Food and Gut Health" Microorganisms 11, no. 3: 793. https://doi.org/10.3390/microorganisms11030793

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop