Inhibitory effect of norharmane on Serratia marcescens NJ01 quorum sensing-mediated virulence factors and biofilm formation

References

• Al-Shabib NA, Husain FM, Khan RA, Khan MS, Alam MZ, Ansari FA, Laeeq S, Zubair M, Shahzad SA, Khan JM, Alsalme A, Ahmad I. 2019. Interference of phosphane copper (I) complexes of β-carboline with quorum sensing regulated virulence functions and biofilm in foodborne pathogenic bacteria: a first report. Saudi J Biol Sci. 26:308–316. doi:10.1016/j.sjbs.2018.04.013
   PubMed Web of Science ®Google Scholar
• Bakkiyaraj D, Sivasankar C, Pandian SK. 2012. Inhibition of quorum sensing regulated biofilm formation in Serratia marcescens causing nosocomial infections. Bioorg Med Chem Lett. 22:3089–3094. doi:10.1016/j.bmcl.2012.03.063
   PubMed Web of Science ®Google Scholar
• Bjarnsholt T, Ciofu O, Molin S, Givskov M, Hoiby N. 2013. Applying insights from biofilm biology to drug development - can a new approach be developed? Nat Rev Drug Discov. 12:791–808. doi:10.1038/nrd4000
   PubMed Web of Science ®Google Scholar
• Brackman G, Cos P, Maes L, Nelis HJ, Coenye T. 2011. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother. 55:2655–2661. doi:10.1128/AAC.00045-11
   PubMed Web of Science ®Google Scholar
• Bruton BD, Mitchell F, Fletcher J, Pair SD, Wayadande A, Melcher U, Brady J, Bextine B, Popham TW. 2003. Serratia marcescens, a phloem-colonizing, squash bug -transmitted bacterium: causal agent of cucurbit yellow vine disease. Plant Dis. 87:937–944. doi:10.1094/PDIS.2003.87.8.937
   PubMed Web of Science ®Google Scholar
• Cheng WJ, Zhou JW, Zhang PP, Luo HZ, Tang S, Li JJ, Deng SM, Jia AQ. 2020. Quorum sensing inhibition and tobramycin acceleration in Chromobacterium violaceum by two natural cinnamic acid derivatives. Appl Microbiol Biotechnol. 104:5025–5037. doi:10.1007/s00253-020-10593-0
   PubMed Web of Science ®Google Scholar
• Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol. 41:435–464. doi:10.1146/annurev.mi.41.100187.002251
   PubMed Web of Science ®Google Scholar
• Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science. 284:1318–1322. doi:10.1126/science.284.5418.1318
   PubMed Web of Science ®Google Scholar
• Coulthurst SJ, Williamson NR, Harris AKP, Spring DR, Salmond GPC. 2006. Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology (Reading). 152:1899–1911. doi:10.1099/mic.0.28803-0
   PubMed Web of Science ®Google Scholar
• Courtois S, Cappellano CM, Ball M, Francou F-X, Normand P, Helynck G, Martinez A, Kolvek SJ, Hopke J, Osburne MS, et al. 2003. Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol. 69:49–55. doi:10.1128/aem.69.1.49-55.2003
   PubMed Web of Science ®Google Scholar
• Devi KR, Srinivasan S, Ravi AV. 2018. Inhibition of quorum sensing-mediated virulence in Serratia marcescens by Bacillus subtilis R-18. Microb Pathog. 120:166–175. doi:10.1016/j.micpath.2018.04.023
   PubMed Web of Science ®Google Scholar
• El-Mowafy SA, Abd El Galil KH, El-Messery SM, Shaaban MI. 2014. Aspirin is an efficient inhibitor of quorum sensing, virulence and toxins in Pseudomonas aeruginosa. Microb Pathog. 74:25–32. doi:10.1016/j.micpath.2014.07.008
   PubMed Web of Science ®Google Scholar
• Fekrirad Z, Kashef N, Arefian E. 2019. Photodynamic inactivation diminishes quorum sensing-mediated virulence factor production and biofilm formation of Serratia marcescens. World J Microbiol Biotechnol. 35:191. doi:10.1007/s11274-019-2768-9
   PubMed Web of Science ®Google Scholar
• Fux CA, Costerton JW, Stewart PS, Stoodley P. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34–40. doi:10.1016/j.tim.2004.11.010
   PubMed Web of Science ®Google Scholar
• Gillis A, Rodríguez M, Santana MA. 2014. Serratia marcescens associated with bell pepper (Capsicum annuum L.) soft-rot disease under greenhouse conditions. Eur J Plant Pathol. 138:1–8. doi:10.1007/s10658-013-0300-x
   Web of Science ®Google Scholar
• Gopu V, Meena CK, Shetty PH. 2015. Quercetin influences quorum sensing in food borne bacteria: in-vitro and in-silico evidence. PLoS One. 10:e0134684. doi:10.1371/journal.pone.0134684
   PubMed Web of Science ®Google Scholar
• Gowrishankar S, Duncun Mosioma N, Karutha Pandian S. 2012. Coral-associated bacteria as a promising antibiofilm agent against methicillin-resistant and -susceptible Staphylococcus aureus biofilms. Evid Based Complement Alternat Med. 2012:862374. doi:10.1155/2012/862374
   PubMed Web of Science ®Google Scholar
• Gutierrez-Roman MI, Holguin-Melendez F, Bello-Mendoza R, Guillen-Navarro K, Dunn MF, Huerta-Palacios G. 2012. Production of prodigiosin and chitinases by tropical Serratia marcescens strains with potential to control plant pathogens. World J Microbiol Biotechnol. 28:145–153. doi:10.1007/s11274-011-0803-6
   PubMed Web of Science ®Google Scholar
• Hansen MC, Palmer RJ, White DC. 2000. Flowcell culture of Porphyromonas gingivalis biofilms under anaerobic conditions. J Microbiol Methods. 40:233–239. doi:10.1016/S0167-7012(00)00126-3
   PubMed Web of Science ®Google Scholar
• Hentzer M, Givskov M. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest. 112:1300–1307. doi:10.1172/jci200320074
   PubMed Web of Science ®Google Scholar
• Jayathilake PG, Jana S, Rushton S, Swailes D, Bridgens B, Curtis T, Chen J. 2017. Extracellular polymeric substance production and aggregated bacteria colonization influence the competition of microbes in biofilms. Front Microbiol. 8:1865. doi:10.3389/fmicb.2017.01865
   PubMed Web of Science ®Google Scholar
• Jones RN. 2010. Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis. 51 Suppl 1:S81–S87. doi:10.1086/653053
   PubMed Web of Science ®Google Scholar
• Kalpana BJ, Aarthy S, Pandian SK. 2012. Antibiofilm activity of α-amylase from Bacillus subtilis S8-18 against biofilm forming human bacterial pathogens . Appl Biochem Biotechnol. 167:1778–1794. doi:10.1007/s12010-011-9526-2
   PubMed Web of Science ®Google Scholar
• Kida Y, Inoue H, Shimizu T, Kuwano K. 2007. Serratia marcescens serralysin induces inflammatory responses through protease-activated receptor 2. Infect Immun. 75:164–174. doi:10.1128/IAI.01239-06
   PubMed Web of Science ®Google Scholar
• Labbate M, Queck SY, Koh KS, Rice SA, Givskov M, Kjelleberg S. 2004. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J Bacteriol. 186:692–698. doi:10.1128/jb.186.3.692-698.2004
   PubMed Web of Science ®Google Scholar
• Lee JH, Kim YG, Shim SH, Lee J. 2017. Antibiofilm activities of norharmane and its derivatives against Escherichia coli O157:H7 and other bacteria. Phytomedicine. 36:254–261. doi:10.1016/j.phymed.2017.10.013
   PubMed Web of Science ®Google Scholar
• Liu GY, Nizet V. 2009. Color me bad: microbial pigments as virulence factors. Trends Microbiol. 17:406–413. doi:10.1016/j.tim.2009.06.006
   PubMed Web of Science ®Google Scholar
• Luo HZ, Guan Y, Yang R, Qian GL, Yang XH, Wang JS, Jia AQ. 2020. Growth inhibition and metabolomic analysis of Xanthomonas oryzae pv. oryzae treated with resveratrol. BMC Microbiol. 20:117. doi:10.1186/s12866-020-01803-w
   PubMed Web of Science ®Google Scholar
• Mitrofanova O, Mardanova A, Evtugyn V, Bogomolnaya L, Sharipova M. 2017. Effects of Bacillus serine proteases on the bacterial biofilms. Biomed Res Int. 2017:8525912. doi:10.1155/2017/8525912
   PubMed Web of Science ®Google Scholar
• Monden K, Ando E, Iida M, Kumon H. 2002. Role of fosfomycin in a synergistic combination with ofloxacin against Pseudomonas aeruginosa growing in a biofilm. J Infect Chemother. 8:218–226. doi:10.1007/s10156-002-0186-6
   PubMedGoogle Scholar
• Morohoshi T, Shiono T, Takidouchi K, Kato M, Kato N, Kato J, Ikeda T. 2007. Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone. Appl Environ Microbiol. 73:6339–6344. doi:10.1128/AEM.00593-07
   PubMed Web of Science ®Google Scholar
• Packiavathy IA, Priya S, Pandian SK, Ravi AV. 2014. Inhibition of biofilm development of uropathogens by curcumin - an anti-quorum sensing agent from Curcuma longa. Food Chem. 148:453–460. doi:10.1016/j.foodchem.2012.08.002
   PubMed Web of Science ®Google Scholar
• Padmavathi AR, Abinaya B, Pandian SK. 2014. Phenol, 2,4-bis(1,1-dimethylethyl) of marine bacterial origin inhibits quorum sensing mediated biofilm formation in the uropathogen Serratia marcescens. Biofouling. 30:1111–1122. doi:10.1080/08927014.2014.972386
   PubMed Web of Science ®Google Scholar
• Park YH, Lee SG, Ahn DJ, Kwon TR, Park SU, Lim HS, Bae HH. 2012. Diversity of fungal endophytes in various tissues of Panax ginseng Meyer cultivated in Korea. J Ginseng Res. 36:211–217. doi:10.5142/jgr.2012.36.2.211
   PubMed Web of Science ®Google Scholar
• Petersen LM, Tisa LS. 2013. Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Can J Microbiol. 59:627–640. doi:10.1139/cjm-2013-0343
   PubMed Web of Science ®Google Scholar
• Ramanathan S, Ravindran D, Arunachalam K, Arumugam VR. 2018. Inhibition of quorum sensing-dependent biofilm and virulence genes expression in environmental pathogen Serratia marcescens by petroselinic acid. Antonie Van Leeuwenhoek. 111:501–515. doi:10.1007/s10482-017-0971-y
   PubMed Web of Science ®Google Scholar
• Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christophersen C, Steinberg P, Kjelleberg S, Givskov M. 2000. How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology (Reading). 146:3237–3244. doi:10.1099/00221287-146-12-3237
   PubMed Web of Science ®Google Scholar
• Ravindran D, Ramanathan S, Arunachalam K, Jeyaraj GP, Shunmugiah KP, Arumugam VR. 2018. Phytosynthesized silver nanoparticles as antiquorum sensing and antibiofilm agent against the nosocomial pathogen Serratia marcescens: an in vitro study. J Appl Microbiol. 124:1425–1440. doi:10.1111/jam.13728
   PubMed Web of Science ®Google Scholar
• Salini R, Pandian SK. 2015. Interference of quorum sensing in urinary pathogen Serratia marcescens by Anethum graveolens. Pathog Dis. 73:ftv038. doi:10.1093/femspd/ftv038
   PubMed Web of Science ®Google Scholar
• Sethupathy S, Ananthi S, Selvaraj A, Shanmuganathan B, Vigneshwari L, Balamurugan K, Mahalingam S, Pandian SK. 2017. Vanillic acid from Actinidia deliciosa impedes virulence in Serratia marcescens by affecting S-layer, flagellin and fatty acid biosynthesis proteins. Sci Rep. 7:16328. doi:10.1038/s41598-017-16507-x
   PubMed Web of Science ®Google Scholar
• Sethupathy S, Shanmuganathan B, Kasi PD, Karutha Pandian S. 2016. Alpha-bisabolol from brown macroalga Padina gymnospora mitigates biofilm formation and quorum sensing controlled virulence factor production in Serratia marcescens. J Appl Phycol. 28:1987–1996. doi:10.1007/s10811-015-0717-z
   Web of Science ®Google Scholar
• She P, Luo Z, Chen L, Wu Y. 2019. Efficacy of levofloxacin against biofilms of Pseudomonas aeruginosa isolated from patients with respiratory tract infections in vitro. Microbiologyopen. 8:e00720. doi:10.1002/mbo3.720
   PubMed Web of Science ®Google Scholar
• Shimuta K, Ohnishi M, Iyoda S, Gotoh N, Koizumi N, Watanabe H. 2009. The hemolytic and cytolytic activities of Serratia marcescens phospholipase A (PhlA) depend on lysophospholipid production by PhlA. BMC Microbiol. 9:261. doi:10.1186/1471-2180-9-261
   PubMed Web of Science ®Google Scholar
• Slater H, Crow M, Everson L, Salmond GP. 2003. Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol. 47:303–320. doi:10.1046/j.1365-2958.2003.03295.x
   PubMed Web of Science ®Google Scholar
• Solano C, Echeverz M, Lasa I. 2014. Biofilm dispersion and quorum sensing. Curr Opin Microbiol. 18:96–104. doi:10.1016/j.mib.2014.02.008
   PubMed Web of Science ®Google Scholar
• Srinivasan R, Mohankumar R, Kannappan A, Karthick Raja V, Archunan G, Karutha Pandian S, Ruckmani K, Veera Ravi A. 2017. Exploring the anti-quorum sensing and antibiofilm efficacy of phytol against Serratia marcescens associated acute pyelonephritis infection in wistar rats. Front Cell Infect Microbiol. 7:498. doi:10.3389/fcimb.2017.00498
   PubMed Web of Science ®Google Scholar
• Srinivasan R, Vigneshwari L, Rajavel T, Durgadevi R, Kannappan A, Balamurugan K, Pandima Devi K, Veera Ravi A. 2018. Biogenic synthesis of silver nanoparticles using Piper betle aqueous extract and evaluation of its anti-quorum sensing and antibiofilm potential against uropathogens with cytotoxic effects: an in vitro and in vivo approach. Environ Sci Pollut Res Int. 25:10538–10554. doi:10.1007/s11356-017-1049-0
   PubMed Web of Science ®Google Scholar
• Sybiya Vasantha Packiavathy IA, Agilandeswari P, Musthafa KS, Karutha Pandian S, Veera Ravi A. 2012. Antibiofilm and quorum sensing inhibitory potential of Cuminum cyminum and its secondary metabolite methyl eugenol against Gram negative bacterial pathogens. Food Res Int. 45:85–92. doi:10.1016/j.foodres.2011.10.022
   Web of Science ®Google Scholar
• Teasdale ME, Liu J, Wallace J, Akhlaghi F, Rowley DC. 2009. Secondary metabolites produced by the marine bacterium Halobacillus salinus that inhibit quorum sensing-controlled phenotypes in gram-negative bacteria. Appl Environ Microbiol. 75:567–572. doi:10.1128/AEM.00632-08
   PubMed Web of Science ®Google Scholar
• Wang XQ, Bi T, Li XD, Zhang LQ, Lu SE. 2015. First report of corn whorl rot caused by Serratia marcescens in China. J Phytopathol. 163:1059–1063. doi:10.1111/jph.12366
   Web of Science ®Google Scholar
• Wang S, Wang Y, Liu W, Liu N, Zhang Y, Dong G, Liu Y, Li Z, He X, Miao Z, et al. 2014. Novel carboline derivatives as potent antifungal lead compounds: design, synthesis, and biological evaluation. ACS Med Chem Lett. 5:506–511. doi:10.1021/ml400492t
   PubMed Web of Science ®Google Scholar
• Zhang J, Rui X, Wang L, Guan Y, Sun X, Dong M. 2014. Polyphenolic extract from Rosa rugosa tea inhibits bacterial quorum sensing and biofilm formation. Food Control. 42:125–131. doi:10.1016/j.foodcont.2014.02.001
   Web of Science ®Google Scholar
• Zhang X, Wu D, Guo T, Ran T, Wang W, Xu D. 2018. Differential roles for ArcA and ArcB homologues in swarming motility in Serratia marcescens FS14. Antonie Van Leeuwenhoek. 111:609–617. doi:10.1007/s10482-017-0981-9
   PubMed Web of Science ®Google Scholar
• Zhou J, Bi S, Chen H, Chen T, Yang R, Li M, Fu Y, Jia AQ. 2017. Anti-biofilm and antivirulence activities of metabolites from Plectosphaerella cucumerina against Pseudomonas aeruginosa. Front Microbiol. 8:769. doi:10.3389/fmicb.2017.00769
   PubMed Web of Science ®Google Scholar
• Zhou JW, Hou B, Liu GY, Jiang H, Sun B, Wang ZN, Shi RF, Xu Y, Wang R, Jia AQ. 2018. Attenuation of Pseudomonas aeruginosa biofilm by hordenine: a combinatorial study with aminoglycoside antibiotics. Appl Microbiol Biotechnol. 102:9745–9758. doi:10.1007/s00253-018-9315-8
   PubMed Web of Science ®Google Scholar
• Zhou W, Li J, Chen J, Liu X, Xiang T, Zhang L, Wan Y. 2016. The red pigment prodigiosin is not an essential virulence factor in entomopathogenic Serratia marcescens. J Invertebr Pathol. 136:92–94. doi:10.1016/j.jip.2016.03.011
   PubMed Web of Science ®Google Scholar
• Zhou JW, Ruan LY, Chen HJ, Luo HZ, Jiang H, Wang JS, Jia AQ. 2019. Inhibition of quorum sensing and virulence in Serratia marcescens by hordenine. J Agric Food Chem. 67:784–795. doi:10.1021/acs.jafc.8b05922
   PubMed Web of Science ®Google Scholar