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Current Drug Discovery Technologies

Editor-in-Chief

ISSN (Print): 1570-1638
ISSN (Online): 1875-6220

Review Article

Modulation of Gut Microbiota through Dietary Phytochemicals as a Novel Anti-infective Strategy

Author(s): Pavan K. Mujawdiya and Suman Kapur*

Volume 17, Issue 4, 2020

Page: [498 - 506] Pages: 9

DOI: 10.2174/1570163816666191107124214

Price: $65

Abstract

Quorum Sensing (QS) is a phenomenon in which bacterial cells communicate with each other with the help of several low molecular weight compounds. QS is largely dependent on population density, and it triggers when the concentration of quorum sensing molecules accumulate in the environment and crosses a particular threshold. Once a certain population density is achieved and the concentration of molecules crosses a threshold, the bacterial cells show a collective behavior in response to various chemical stimuli referred to as “auto-inducers”. The QS signaling is crucial for several phenotypic characteristics responsible for bacterial survival such as motility, virulence, and biofilm formation. Biofilm formation is also responsible for making bacterial cells resistant to antibiotics.

The human gut is home to trillions of bacterial cells collectively called “gut microbiota” or “gut microbes”. Gut microbes are a consortium of more than 15,000 bacterial species and play a very crucial role in several body functions such as metabolism, development and maturation of the immune system, and the synthesis of several essential vitamins. Due to its critical role in shaping human survival and its modulating impact on body metabolisms, the gut microbial community has been referred to as “the forgotten organ” by O`Hara et al. (2006) [1]. Several studies have demonstrated that chemical interaction between the members of bacterial cells in the gut is responsible for shaping the overall microbial community.

Recent advances in phytochemical research have generated a lot of interest in finding new, effective, and safer alternatives to modern chemical-based medicines. In the context of antimicrobial research various plant extracts have been identified with Quorum Sensing Inhibitory (QSI) activities among bacterial cells. This review focuses on the mechanism of quorum sensing and quorum sensing inhibitors isolated from natural sources.

Keywords: Quorum sensing, gut microbiota, quorum sensing inhibitors, anti-microbial resistance, phytochemicals, gene expression profiles.

Graphical Abstract
[1]
Abisado RG, Benomar S, Klaus JR, et al. Bacterial quorum sensing and microbial community interactions 2018.e02331-17
[http://dx.doi.org/10.1128/mBio.02331-17]
[2]
Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21: 319-46.
[http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131001] [PMID: 16212498]
[3]
Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 2016; 14(9): 576-88.
[http://dx.doi.org/10.1038/nrmicro.2016.89] [PMID: 27510864]
[4]
Brackman G, Coenye T. Quorum sensing inhibitors as anti-biofilm agents. Curr Pharm Des 2015; 21(1): 5-11.
[http://dx.doi.org/10.2174/1381612820666140905114627] [PMID: 25189863]
[5]
Li Y-H, Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel) 2012; 12(3): 2519-38.
[http://dx.doi.org/10.3390/s120302519] [PMID: 22736963]
[6]
Puzari M, Sharma M, Chetia P. Emergence of antibiotic resistant Shigella species: A matter of concern. J Infect Public Health 2017.
[http://dx.doi.org/10.1016/j.jiph.2017.09.025] [PMID: 29066021]
[7]
Ventola CL. The Antibiotic resistance crisis.Part 1: Causes and Threats Pharmacy and Therapeutics 2015; 40(4): 277-83.
[8]
Ventola CL. Biofilm prevention and control by dietary phytochemicals. Microbial pathogens and strategies for combating them: science, technology and education Formatex Research Cente 32-41.
[9]
O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep 2006; 7(7): 688-93.
[http://dx.doi.org/10.1038/sj.embor.7400731] [PMID: 16819463]
[10]
Bacha K, Tariku Y, Gebreyesus F, et al. Antimicrobial and anti-Quorum Sensing activities of selected medicinal plants of Ethiopia: Implication for development of potent antimicrobial agents. BMC Microbiol 2016; 16(1): 139.
[http://dx.doi.org/10.1186/s12866-016-0765-9] [PMID: 27400878]
[11]
Park JS, Ryu EJ, Li L, Choi BK, Kim BM. New bicyclic brominated furanones as potent autoinducer-2 quorum-sensing inhibitors against bacterial biofilm formation. Eur J Med Chem 2017; 137(8): 76-87.
[http://dx.doi.org/10.1016/j.ejmech.2017.05.037] [PMID: 28554093]
[12]
Nizalapur S, Kimyon O, Yee E, et al. Synthesis and biological evaluation of novel acyclic and cyclic glyoxamide based derivatives as bacterial quorum sensing and biofilm inhibitors. Org Biomol Chem 2017; 15(27): 5743-55.
[http://dx.doi.org/10.1039/C7OB01011G] [PMID: 28654117]
[13]
Ryan RP, Dow JM. Diffusible signals and interspecies communication in bacteria. Microbiology 2008; 154(Pt 7): 1845-58.
[http://dx.doi.org/10.1099/mic.0.2008/017871-0] [PMID: 18599814]
[14]
Williams P, Cámara M. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 2009; 12(2): 182-91.
[http://dx.doi.org/10.1016/j.mib.2009.01.005] [PMID: 19249239]
[15]
Musthafa KS, Ravi AV, Annapoorani A, Packiavathy IS, Pandian SK. Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl-homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa. Chemotherapy 2010; 56(4): 333-9.
[http://dx.doi.org/10.1159/000320185] [PMID: 20720417]
[16]
Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol 2015; 31(1): 69-75.
[http://dx.doi.org/10.1097/MOG.0000000000000139] [PMID: 25394236]
[17]
Thompson JA, Oliveira RA, Xavier KB. Chemical conversations in the gut microbiota. Gut Microbes 2016; 7(2): 163-70.
[http://dx.doi.org/10.1080/19490976.2016.1145374] [PMID: 26901101]
[18]
Hsiao WW, Metz C, Singh DP, Roth J. The microbes of the intestine: an introduction to their metabolic and signaling capabilities. Endocrinol Metab Clin North Am 2008; 37(4): 857-71.
[http://dx.doi.org/10.1016/j.ecl.2008.08.006] [PMID: 19026936]
[19]
Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 2014; 12(10): 661-72.
[http://dx.doi.org/10.1038/nrmicro3344] [PMID: 25198138]
[20]
Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977; 31: 107-33.
[http://dx.doi.org/10.1146/annurev.mi.31.100177.000543] [PMID: 334036]
[21]
Berg RD. The indigenous gastrointestinal microflora. Trends Microbiol 1996; 4(11): 430-5.
[http://dx.doi.org/10.1016/0966-842X(96)10057-3] [PMID: 8950812]
[22]
Buffie CG, Jarchum I, Equinda M, et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun 2012; 80(1): 62-73.
[http://dx.doi.org/10.1128/IAI.05496-11] [PMID: 22006564]
[23]
Ubeda C, Taur Y, Jenq RR, et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 2010; 120(12): 4332-41.
[http://dx.doi.org/10.1172/JCI43918] [PMID: 21099116]
[24]
Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008; 453(7195): 620-5.
[http://dx.doi.org/10.1038/nature07008] [PMID: 18509436]
[25]
Maura D, Bandyopadhaya A, Rahme LG. Animal models for Pseudomonas aeruginosa quorum sensing studies. Methods Mol Biol 2018; 1673: 227-41.
[http://dx.doi.org/10.1007/978-1-4939-7309-5_18] [PMID: 29130177]
[26]
Pearson JP, Feldman M, Iglewski BH, Prince A. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect Immun 2000; 68(7): 4331-4.
[http://dx.doi.org/10.1128/IAI.68.7.4331-4334.2000] [PMID: 10858254]
[27]
Harjai K, Gupta RK, Sehgal H. Attenuation of quorum sensing controlled virulence of Pseudomonas aeruginosa by cranberry. Indian J Med Res 2014; 139(3): 446-53.
[PMID: 24820840]
[28]
Huang T, Song X, Zhao K, et al. Quorum-sensing molecules N-acyl homoserine lactones inhibit Trueperella pyogenes infection in mouse model. Vet Microbiol 2018; 213: 89-94.
[http://dx.doi.org/10.1016/j.vetmic.2017.11.029] [PMID: 29292009]
[29]
Simonetti O, Cirioni O, Cacciatore I, et al. Efficacy of the quorum sensing inhibitor FS10 alone and in combination with tigecycline in an animal model of Staphylococcal infected wound. PLoS One 2016; 11(6) e0151956
[http://dx.doi.org/10.1371/journal.pone.0151956] [PMID: 27253706]
[30]
Kalia VC. Quorum sensing inhibitors: an overview. Biotechnol Adv 2013; 31(2): 224-45.
[http://dx.doi.org/10.1016/j.biotechadv.2012.10.004] [PMID: 23142623]
[31]
Jakobsen TH, Bragason SK, Phipps RK, et al. Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol 2012; 78(7): 2410-21.
[http://dx.doi.org/10.1128/AEM.05992-11] [PMID: 22286987]
[32]
Thompson JA, Oliveira RA, Djukovic A, Ubeda C, Xavier KB. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep 2015; 10(11): 1861-71.
[http://dx.doi.org/10.1016/j.celrep.2015.02.049] [PMID: 25801025]
[33]
Sarabhai S, Sharma P, Capalash N. Ellagic acid derivatives from Terminalia chebula Retz. downregulate the expression of quorum sensing genes to attenuate Pseudomonas aeruginosa PAO1 virulence. PLoS One 2013; 8(1) e53441
[http://dx.doi.org/10.1371/journal.pone.0053441] [PMID: 23320085]
[34]
Vandeputte OM, Kiendrebeogo M, Rajaonson S, et al. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 2010; 76(1): 243-53.
[http://dx.doi.org/10.1128/AEM.01059-09] [PMID: 19854927]
[35]
Musthafa KS, Sianglum W, Saising J, Lethongkam S, Voravuthikunchai SP. Evaluation of phytochemicals from medicinal plants of Myrtaceae family on virulence factor production by Pseudomonas aeruginosa. APMIS 2017; 125(5): 482-90.
[http://dx.doi.org/10.1111/apm.12672] [PMID: 28294414]
[36]
Sivaranji M, Krishnan SR, Kannapan A, et al. Curcumin from Curcuma longa affects virulence of Pectobacterium wasabiae and P. carotovorum subsp. carotovorum via quorum sensing regulation. Eur J Plant Pathol 2016; 146: 793-806.
[http://dx.doi.org/10.1007/s10658-016-0957-z]
[37]
Zhao WH, Hu ZQ, Hara Y, Shimamura T. Inhibition by epigallocatechin gallate (EGCg) of conjugative R plasmid transfer in Escherichia coli. J Infect Chemother 2001; 7(3): 195-7.
[http://dx.doi.org/10.1007/s101560100035] [PMID: 11810584]
[38]
Jakobsen TH, van Gennip M, Phipps RK, et al. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob Agents Chemother 2012; 56(5): 2314-25.
[http://dx.doi.org/10.1128/AAC.05919-11] [PMID: 22314537]
[39]
Lihua L, Jianhuit W, Jialini Y, Yayin L, Guanxin L. Effects of allicin on the formation of Pseudomonas aeruginosa biofinm and the production of quorum-sensing controlled virulence factors. Pol J Microbiol 2013; 62(3): 243-51.
[http://dx.doi.org/10.33073/pjm-2013-032] [PMID: 24459829]
[40]
Truchado P, Giménez-Bastida JA, Larrosa M, et al. Inhibition of quorum sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. J Agric Food Chem 2012; 60(36): 8885-94.
[http://dx.doi.org/10.1021/jf301365a] [PMID: 22533445]
[41]
Choo JH, Rukayadi Y, Hwang JK. Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 2006; 42(6): 637-41.
[http://dx.doi.org/10.1111/j.1472-765X.2006.01928.x] [PMID: 16706905]
[42]
Ponnusamy K, Kappachery S, Thekeettle M, Song JH, Kweon JH. Anti-biofouling property of vanillin on Aeromonas hydrophila initial biofilm on various membrane surfaces. World J Microbiol Biotechnol 2013; 29(9): 1695-703.
[http://dx.doi.org/10.1007/s11274-013-1332-2] [PMID: 23539151]
[43]
Ren D, Zuo R, González Barrios AF, et al. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 2005; 71(7): 4022-34.
[http://dx.doi.org/10.1128/AEM.71.7.4022-4034.2005] [PMID: 16000817]
[44]
Giménez-Bastida JA, Truchado P, Larrosa M, et al. Urolithins, ellagitannin metabolites produced by colon microbiota, inhibit Quorum Sensing in Yersinia enterocolitica: Phenotypic response and associated molecular changes. Food Chem 2012; 132(3): 1465-74.
[http://dx.doi.org/10.1016/j.foodchem.2011.12.003] [PMID: 29243637]
[45]
Siraj D, Debanjan J, Tilak RM, et al. Piper betle leaf extract affects 191 the quorum sensing and hence virulence of Pseudomonas aeruginosa 192 PAO1. 3 Biotech 2016; 6: 18
[46]
Siddiqui MF, Sakinah M, Ismail AF, et al. The anti-biofouling effect of Piper betle extract against Pseudomonas aeruginosa and bacterial consortium. Desalination 2012; 288: 24-30.
[http://dx.doi.org/10.1016/j.desal.2011.11.060]
[47]
Packiavathy IA, Agilandeswari P, Musthafa KS, et al. Antibiofilm and quorum sensing inhibitory potential of Cuminum cyminum and its secondary metabolite methyl eugenol against Gram negative bacterial pathogens. Food Res Int 2012; 45: 85-92.
[http://dx.doi.org/10.1016/j.foodres.2011.10.022]
[48]
Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, et al. The flavanone naringenin reduces the production of quorum
[49]
Husain FM, Ahmad I, Al-Thubiani AS, Abulreesh HH, AlHazza IM, Aqil F. Leaf Extracts of Mangifera indica L. inhibit quorum sensing - regulated production of virulence factors and biofilm in test bacteria. Front Microbiol 2017; 8: 727.
[http://dx.doi.org/10.3389/fmicb.2017.00727] [PMID: 28484444]
[50]
Rajasekharan SK, Ramesh S, Satish AS, Lee J. Antibiofilm and anti-β-lactamase activities of burdock root extract and chlorogenic acid against Klebsiella pneumonia. J Microbiol Biotechnol 2017; 27(3): 542-51.
[http://dx.doi.org/10.4014/jmb.1609.09043] [PMID: 27974734]
[51]
Girennavar B, Cepeda ML, Soni KA, et al. Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int J Food Microbiol 2008; 125(2): 204-8.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2008.03.028] [PMID: 18504060]
[52]
Blanco AR, Sudano-Roccaro A, Spoto GC, Nostro A, Rusciano D. Epigallocatechin gallate inhibits biofilm formation by ocular staphylococcal isolates. Antimicrob Agents Chemother 2005; 49(10): 4339-43.
[http://dx.doi.org/10.1128/AAC.49.10.4339-4343.2005] [PMID: 16189116]
[53]
Tan LY, Yin WF, Chan KG. Silencing quorum sensing through extracts of Melicopelunu-ankendaSensors (Basel) 2012; 12(4): 1339-1351
[54]
Singh BN, Singh BR, Singh RL, et al. Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera. Food Chem Toxicol 2009; 47(6): 1109-16.
[http://dx.doi.org/10.1016/j.fct.2009.01.034] [PMID: 19425184]
[55]
Ni N, Choudhary G, Li M, Wang B. Pyrogallol and its analogs can antagonize bacterial quorum sensing in Vibrio harveyi. Bioorg Med Chem Lett 2008; 18(5): 1567-72.
[http://dx.doi.org/10.1016/j.bmcl.2008.01.081] [PMID: 18262415]
[56]
Lagier JC, Million M, Hugon P, et al. Human gut microbiota: repertoire and variations. 2012;2,136. Front Cell Infect Microbiol 2012; 2: 136.
[PMID: 23130351]
[57]
Lawley TD, Walker AW. Intestinal colonization resistance. Immunology 2013; 138(1): 1-11.
[http://dx.doi.org/10.1111/j.1365-2567.2012.03616.x] [PMID: 23240815]
[58]
Casals-Pascual C, Vergara A, Vila J. Intestinal microbiota and antibiotic resistance: Perspectives and solutions. Human Microbiome Journal 2018; 9: 11-5.
[http://dx.doi.org/10.1016/j.humic.2018.05.002]
[59]
Modi SR, Collins JJ, Relman DA. Antibiotics and the gut microbiota. J Clin Invest 2014; 124(10): 4212-8.
[http://dx.doi.org/10.1172/JCI72333] [PMID: 25271726]
[60]
Francino MP. Antibiotics and the human gut microbiome: Dysbioses and accumulation of resistances. Front Microbiol 2016; 6: 1543.
[http://dx.doi.org/10.3389/fmicb.2015.01543] [PMID: 26793178]
[61]
Baron SA, Diene SM, Rolain JM. Human microbiomes and antibiotic resistance. Human Microbiome Journal 2018; 10: 43-52.
[http://dx.doi.org/10.1016/j.humic.2018.08.005]

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