Quorum-Sensing Inhibitors from Probiotics as a Strategy to Combat Bacterial Cell-to-Cell Communication Involved in Food Spoilage and Food Safety

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. Due to the many reports showing that the use of conventional methods (i.e., antibiotics and sanitizers) to inhibit bacterial growth leads to the emergence of antibiotic resistance, it is necessary to research and exploit new strategies. Several studies have already demonstrated positive results in this direction by inhibiting autoinducers (low-molecular-weight signaling compounds controlling QS) and by other means, leading to QS inhibition via a mechanism called quorum quenching (QQ). Thus far, several QS inhibitors (QSIs) have been isolated from various sources, such as plants, some animals from aqueous ecosystems, fungi, and bacteria. The present study aims to discuss the involvement of QS in food spoilage and to review the potential role of probiotics as QSIs.

[1]  Ibrahim Khelifi,et al.  Optimization of Ethanolic Extraction of Enantia chloranta Bark, Phytochemical Composition, Green Synthesis of Silver Nanoparticles, and Antimicrobial Activity , 2022, Fermentation.

[2]  Pengfei Wan,et al.  Quorum Sensing Molecules in Yeast Wastewater Treatment and Their Regulation of Yeast Cell Morphology , 2022, SSRN Electronic Journal.

[3]  H. Mukhtar,et al.  Exploring the Function of Quorum Sensing Regulated Biofilms in Biological Wastewater Treatment: A Review , 2022, International journal of molecular sciences.

[4]  S. Alfarraj,et al.  Quorum Sensing Inhibitory and Quenching Activity of Bacillus cereus RC1 Extracts on Soft Rot-Causing Bacteria Lelliottia amnigena , 2022, ACS omega.

[5]  Mengjie Wu,et al.  Potential antimicrobial activities of probiotics and their derivatives against Listeria monocytogenes in food field: A review. , 2022, Food research international.

[6]  Xin M. Luo,et al.  AI-2/LuxS Quorum Sensing System Promotes Biofilm Formation of Lactobacillus rhamnosus GG and Enhances the Resistance to Enterotoxigenic Escherichia coli in Germ-Free Zebrafish , 2022, Microbiology spectrum.

[7]  G. Hummer,et al.  Cryo‐EM structures of pentameric autoinducer‐2 exporter from Escherichia coli reveal its transport mechanism , 2022, The EMBO journal.

[8]  M. Azeez,et al.  Quorum Sensing and its Correlation with Virulence Factors , 2022, South Asian Research Journal of Pharmaceutical Sciences.

[9]  D. Steinberg,et al.  Targeting the Holy Triangle of Quorum Sensing, Biofilm Formation, and Antibiotic Resistance in Pathogenic Bacteria , 2022, Microorganisms.

[10]  T. Maeda,et al.  Quorum quenching of autoinducer 2 increases methane production in anaerobic digestion of waste activated sludge , 2022, Applied Microbiology and Biotechnology.

[11]  O. Alegbeleye,et al.  Microbial spoilage of vegetables, fruits and cereals , 2022, Applied Food Research.

[12]  G. Wang,et al.  Quorum Sensing of Lactic Acid Bacteria: Progress and Insights , 2022, Food Reviews International.

[13]  A. Mohanty,et al.  Bacillus subtilis BR4 derived stigmatellin Y interferes Pqs‐PqsR mediated quorum sensing system of Pseudomonas aeruginosa , 2022, Journal of basic microbiology.

[14]  Chao Tian,et al.  A Systematic Review and Meta-Analysis: Lactobacillus acidophilus for Treating Acute Gastroenteritis in Children , 2022, Nutrients.

[15]  M. Chikindas,et al.  Quorum-Sensing Inhibition by Gram-Positive Bacteria , 2022, Microorganisms.

[16]  U. Dobrindt,et al.  A Simple Biosensor-Based Assay for Quantitative Autoinducer-2 Analysis. , 2022, ACS synthetic biology.

[17]  Binbin Wu,et al.  RNA-seq-based transcriptomic analysis of AHL-induced biofilm and pyocyanin inhibition in Pseudomonas aeruginosa by Lactobacillus brevis , 2022, International Microbiology.

[18]  Soumya Pandit,et al.  Phytocompound Mediated Blockage of Quorum Sensing Cascade in ESKAPE Pathogens , 2022, Antibiotics.

[19]  S. Ha,et al.  Listeria monocytogenes biofilm inhibition on food contact surfaces by application of postbiotics from Lactobacillus curvatus B.67 and Lactobacillus plantarum M.2. , 2021, Food research international.

[20]  S. Dashper,et al.  Streptococcus salivarius K12 inhibits Candida albicans aggregation, biofilm formation and dimorphism , 2021, Biofouling.

[21]  X. Tian,et al.  Quorum Sensing in Fungal Species. , 2021, Annual review of microbiology.

[22]  M. Martínez,et al.  The architecture of a mixed fungal-bacterial biofilm is modulated by quorum sensing signals. , 2021, Environmental microbiology.

[23]  H. Dupont,et al.  Potential role of probiotics in reducing Clostridioides difficile virulence: Interference with quorum sensing systems. , 2021, Microbial pathogenesis.

[24]  Razan Marouf,et al.  The use of probiotics in animal feeding for safe production and as potential alternatives to antibiotics , 2021, Veterinary world.

[25]  S. C. Desobgo,et al.  Antagonistic effects of raffia sap with probiotics against pathogenic microorganisms , 2020 .

[26]  L. Melo,et al.  Quorum sensing in food spoilage and natural-based strategies for its inhibition. , 2020, Food research international.

[27]  N. Luplertlop,et al.  Suppression of the pathogenicity of Candida albicans by the quorum-sensing molecules farnesol and tryptophol. , 2019, The Journal of general and applied microbiology.

[28]  Wei Chen,et al.  Lactobacillus fermentum and its potential immunomodulatory properties , 2019, Journal of Functional Foods.

[29]  Sejong Oh,et al.  Suppressive effect of Lactobacillus fermentum Lim2 on Clostridioides difficile 027 toxin production , 2019, Letters in applied microbiology.

[30]  F. Echeverri,et al.  Natural Compounds That Modulate the Development of the Fungus Botrytis cinerea and Protect Solanum lycopersicum , 2019, Plants.

[31]  Zengfu Song,et al.  The Quorum Quenching Bacterium Bacillus licheniformis T-1 Protects Zebrafish against Aeromonas hydrophila Infection , 2019, Probiotics and Antimicrobial Proteins.

[32]  K. Demnerova,et al.  Molecules Autoinducer 2 and cjA and Their Impact on Gene Expression in Campylobacter jejuni , 2019, Journal of Molecular Microbiology and Biotechnology.

[33]  L. Drago,et al.  Probiotics Streptococcus salivarius 24SMB and Streptococcus oralis 89a interfere with biofilm formation of pathogens of the upper respiratory tract , 2018, BMC Infectious Diseases.

[34]  Dimitra C. Banti,et al.  Evaluation of a novel quorum quenching strain for MBR biofouling mitigation. , 2018, Water research.

[35]  M. Burmølle,et al.  Insights into Bacterial Milk Spoilage with Particular Emphasis on the Roles of Heat-Stable Enzymes, Biofilms, and Quorum Sensing. , 2018, Journal of food protection.

[36]  A. V. Ravi,et al.  Inhibition of quorum sensing-mediated virulence in Serratia marcescens by Bacillus subtilis R-18. , 2018, Microbial pathogenesis.

[37]  Josephine R. Chandler,et al.  Bacterial Quorum Sensing and Microbial Community Interactions , 2018, mBio.

[38]  M. Zeng,et al.  Acyl-homoserine-lactones receptor LuxR of Shewanella baltica involved in the development of microbiota and spoilage of refrigerated shrimp , 2018, Journal of Food Science and Technology.

[39]  R. Prasad,et al.  Quorum sensing: A less known mode of communication among fungi. , 2018, Microbiological research.

[40]  Yanbo Wang,et al.  Quorum sensing system-regulated genes affect the spoilage potential of Shewanella baltica. , 2018, Food research international.

[41]  M. Zeng,et al.  Spoilage of refrigerated Litopenaeus vannamei: eavesdropping on Acinetobacter acyl-homoserine lactones promotes the spoilage potential of Shewanella baltica , 2018, Journal of Food Science and Technology.

[42]  L. Tsimring,et al.  Coexistence and Pattern Formation in Bacterial Mixtures with Contact-Dependent Killing. , 2018, Biophysical journal.

[43]  Younghoon Kim,et al.  Influences of quorum-quenching probiotic bacteria on the gut microbial community and immune function in weaning pigs. , 2018, Animal science journal = Nihon chikusan Gakkaiho.

[44]  H. Ashour,et al.  Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries‐inducing Streptococcus mutans , 2018, Journal of Cellular and Molecular Medicine.

[45]  M. Olivares,et al.  Differential intestinal anti-inflammatory effects of Lactobacillus fermentum and Lactobacillus salivarius in DSS mouse colitis: impact on microRNAs expression and microbiota composition. , 2017, Molecular nutrition & food research.

[46]  E. D. De Martinis,et al.  Growth, viability and architecture of biofilms of Listeria monocytogenes formed on abiotic surfaces , 2017, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[47]  S. Vilar,et al.  Furvina inhibits the 3-oxo-C12-HSL-based quorum sensing system of Pseudomonas aeruginosa and QS-dependent phenotypes , 2017, Biofouling.

[48]  B. Skotarczak,et al.  QS – systems communication of Gram-positive bacterial cells , 2017 .

[49]  A. Lourenço,et al.  Probiotics, gut microbiota, and their influence on host health and disease , 2017, Molecular nutrition & food research.

[50]  M. Chikindas,et al.  Subtilosin Prevents Biofilm Formation by Inhibiting Bacterial Quorum Sensing , 2017, Probiotics and Antimicrobial Proteins.

[51]  A. Ray,et al.  The talking language in some major Gram-negative bacteria , 2016, Archives of Microbiology.

[52]  S. Ha,et al.  Variability in biofilm formation correlates with hydrophobicity and quorum sensing among Vibrio parahaemolyticus isolates from food contact surfaces and the distribution of the genes involved in biofilm formation , 2016, Biofouling.

[53]  M. Shemesh,et al.  The LuxS Based Quorum Sensing Governs Lactose Induced Biofilm Formation by Bacillus subtilis , 2016, Front. Microbiol..

[54]  S. Moréra,et al.  Quorum quenching: role in nature and applied developments. , 2016, FEMS microbiology reviews.

[55]  J. Arnason,et al.  Mini Review of Phytochemicals and Plant Taxa with Activity as Microbial Biofilm and Quorum Sensing Inhibitors , 2015, Molecules.

[56]  L. Nielsen,et al.  Quorum-sensing linked RNA interference for dynamic metabolic pathway control in Saccharomyces cerevisiae. , 2015, Metabolic engineering.

[57]  T. Iino,et al.  Health benefits of fermented milk containing Bifidobacterium bifidum YIT 10347 on gastric symptoms in adults. , 2015, Journal of dairy science.

[58]  M. Griffiths,et al.  Lactobacillus acidophilus modulates the virulence of Clostridium difficile. , 2014, Journal of dairy science.

[59]  A. Spiers,et al.  Quorum-Quenching Activity of the AHL-Lactonase from Bacillus licheniformis DAHB1 Inhibits Vibrio Biofilm Formation In Vitro and Reduces Shrimp Intestinal Colonisation and Mortality , 2014, Marine Biotechnology.

[60]  G. Nychas,et al.  Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. , 2014, Meat science.

[61]  T. Benezech,et al.  Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments. , 2014, Food microbiology.

[62]  N. Keller,et al.  Molecular mechanisms of Aspergillus flavus secondary metabolism and development. , 2014, Fungal genetics and biology : FG & B.

[63]  M-J Butel,et al.  Probiotics, gut microbiota and health. , 2014, Medecine et maladies infectieuses.

[64]  A. Logan,et al.  Fermented foods, microbiota, and mental health: ancient practice meets nutritional psychiatry , 2014, Journal of Physiological Anthropology.

[65]  A. Casadevall,et al.  Quorum Sensing-Mediated, Cell Density-Dependent Regulation of Growth and Virulence in Cryptococcus neoformans , 2013, mBio.

[66]  Tim I. Miyashiro,et al.  Quorum Sensing in the Squid-Vibrio Symbiosis , 2013, International journal of molecular sciences.

[67]  Younghoon Kim,et al.  Bifidobacterium spp. influences the production of autoinducer-2 and biofilm formation by Escherichia coli O157:H7. , 2012, Anaerobe.

[68]  N. Keller,et al.  Aspergillus Oxylipin Signaling and Quorum Sensing Pathways Depend on G Protein-Coupled Receptors , 2012, Toxins.

[69]  G. Nychas,et al.  Quorum Sensing in the Context of Food Microbiology , 2012, Applied and Environmental Microbiology.

[70]  Arturo Casadevall,et al.  Quorum sensing in fungi--a review. , 2012, Medical mycology.

[71]  V. Rai,et al.  Bacterial Quorum Sensing and Food Industry , 2011 .

[72]  A. Ghaly,et al.  Fish Spoilage Mechanisms and Preservation Techniques: Review , 2010 .

[73]  S. K. Pandian,et al.  Bacillus pumilus of Palk Bay origin inhibits quorum-sensing-mediated virulence factors in Gram-negative bacteria. , 2010, Research in microbiology.

[74]  Friedrich Götz,et al.  Cell–Cell Communication and Biofilm Formation in Gram‐Positive Bacteria , 2009 .

[75]  N. Ahmed,et al.  AI-2/LuxS Is Involved in Increased Biofilm Formation by Streptococcus intermedius in the Presence of Antibiotics , 2009, Antimicrobial Agents and Chemotherapy.

[76]  T. Klaenhammer,et al.  Role of autoinducer‐2 on the adhesion ability of Lactobacillus acidophilus , 2009, Journal of applied microbiology.

[77]  H. Yonezawa,et al.  Inhibiting effects of Streptococcus salivarius on competence-stimulating peptide-dependent biofilm formation by Streptococcus mutans. , 2009, Oral microbiology and immunology.

[78]  M. Kruppa Quorum sensing and Candida albicans , 2009, Mycoses.

[79]  M. Griffiths,et al.  Effect of Molecules Secreted by Lactobacillus acidophilus Strain La-5 on Escherichia coli O157:H7 Colonization , 2008, Applied and Environmental Microbiology.

[80]  G. Nychas,et al.  Insights into the role of quorum sensing in food spoilage. , 2008, Journal of food protection.

[81]  U. Pinto,et al.  Detection of acylated homoserine lactones in gram-negative proteolytic psychrotrophic bacteria isolated from cooled raw milk , 2007 .

[82]  K. Kwon-Chung,et al.  TUP1 disruption in Cryptococcus neoformans uncovers a peptide‐mediated density‐dependent growth phenomenon that mimics quorum sensing , 2007, Molecular microbiology.

[83]  D. Hogan Talking to Themselves: Autoregulation and Quorum Sensing in Fungi , 2006, Eukaryotic Cell.

[84]  J. Ryu,et al.  Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer. , 2005, Journal of food protection.

[85]  Bonnie L. Bassler,et al.  Interference with AI-2-mediated bacterial cell–cell communication , 2005, Nature.

[86]  G. Perdigón,et al.  Interference of Lactobacillus plantarum with Pseudomonas aeruginosa in vitro and in infected burns: the potential use of probiotics in wound treatment. , 2005, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[87]  L. Gram,et al.  Involvement of Bacterial Quorum-Sensing Signals in Spoilage of Bean Sprouts , 2005, Applied and Environmental Microbiology.

[88]  M. Bölker,et al.  Genetic Analysis of Biosurfactant Production in Ustilago maydis , 2005, Applied and Environmental Microbiology.

[89]  L. Gram,et al.  Nonbioluminescent Strains of Photobacterium phosphoreum Produce the Cell-to-Cell Communication Signal N-(3-Hydroxyoctanoyl)homoserine Lactone , 2005, Applied and Environmental Microbiology.

[90]  G. Fink,et al.  Tyrosol is a quorum-sensing molecule in Candida albicans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[91]  L. Stepaniak Dairy enzymology , 2004 .

[92]  S. Molin,et al.  Quorum-sensing-directed protein expression in Serratia proteamaculans B5a. , 2003, Microbiology.

[93]  Lone Gram,et al.  Food spoilage--interactions between food spoilage bacteria. , 2002, International journal of food microbiology.

[94]  N. A. Whitehead,et al.  Quorum-sensing in Gram-negative bacteria. , 2001, FEMS microbiology reviews.

[95]  Y. Dong,et al.  AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[96]  W. Fuqua,et al.  A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite , 1994, Journal of bacteriology.

[97]  K. Nealson,et al.  Cellular Control of the Synthesis and Activity of the Bacterial Luminescent System , 1970, Journal of bacteriology.