Abstract
Chronic infections caused by Pseudomonas aeruginosa have been a major concern as their spread and mortality continue to be on the rise. These infections are majorly attributed to biofilm formation via sequential steps where motility plays an essential role in initial attachment of bacterial cells onto biotic and abiotic surfaces, thereby contributing to multi-drug resistance among pathogens. Therefore, attenuating motility properties can be considered as highly potential for controlling P. aeruginosa biofilm formation. This strategy has employed the use of various natural and chemically synthesized compounds. The present review article explained the importance and regulation of different types of motilities properties. Furthermore, it also covered several important alternative approaches using anti-motility agents which could be helpful for controlling P. aeruginosa biofilm-associated infections. Further studies are required for in-depth understandings about the mechanisms of motilities controlling of these molecules at molecular levels.
Similar content being viewed by others
References
Abinaya M, Gayathri M (2019) Inhibition of biofilm formation, quorum sensing activity and molecular docking study of isolated 3, 5, 7-trihydroxyflavone from Alstonia scholaris leaf against P. aeruginosa. Bioorg Chem 87:291–301. https://doi.org/10.1016/j.bioorg.2019.03.050
Alavi M, Karimi N (2018) Antiplanktonic, antibiofilm, antiswarming motility and antiquorum sensing activities of green synthesized Ag-TiO2, TiO2-Ag, Ag-Cu and Cu-Ag nanocomposites against multi-drug-resistant bacteria. Artif Cells Nanomed Biotechnol 46:S399–S413. https://doi.org/10.1080/21691401.2018.1496923
Alhajlan M, Alhariri M, Omri A (2013) Efficacy and safety of liposomal clarithromycin and its effect on Pseudomonas aeruginosa virulence factors. Antimicrob Agents Chemother 57:2694–2704. https://doi.org/10.1128/AAC.00235-13
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 beta-carboline with quorum sensing regulated virulence functions and biofilm in foodborne pathogenic bacteria: a first report. Saudi J Biol Sci 26:308–316. https://doi.org/10.1016/j.sjbs.2018.04.013
Bahari S, Zeighami H, Mirshahabi H, Roudashti S, Haghi F (2017) Inhibition of Pseudomonas aeruginosa quorum sensing by subinhibitory concentrations of curcumin with gentamicin and azithromycin. J Glob Antimicrob Resist 10:21–28. https://doi.org/10.1016/j.jgar.2017.03.006
Bala A, Kumar R, Harjai K (2011) Inhibition of quorum sensing in Pseudomonas aeruginosa by azithromycin and its effectiveness in urinary tract infections. J Med Microbiol 60:300–306. https://doi.org/10.1099/jmm.0.025387-0
Bandara MB, Zhu H, Sankaridurg PR, Willcox MD (2006) Salicylic acid reduces the production of several potential virulence factors of Pseudomonas aeruginosa associated with microbial keratitis. Invest Ophthalmol Vis Sci 47:4453–4460. https://doi.org/10.1167/iovs.06-0288
Beatson SA, Whitchurch CB, Semmler AB, Mattick JS (2002) Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184:3598–3604
Blus-Kadosh I, Zilka A, Yerushalmi G, Banin E (2013) The effect of pstS and phoB on quorum sensing and swarming motility in Pseudomonas aeruginosa. PLoS One 8:e74444. https://doi.org/10.1371/journal.pone.0074444
Bonez PC, Rossi GG, Bandeira JR, Ramos AP, Mizdal CR, Agertt VA, Dalla Nora ESS, de Souza ME, Dos Santos Alves CF, Dos Santos FS, Gündel A, de Almeida VR, Santos RCV, de Campos MMA (2017) Anti-biofilm activity of A22 ((S-3,4-dichlorobenzyl) isothiourea hydrochloride) against Pseudomonas aeruginosa: influence on biofilm formation, motility and bioadhesion. Microb Pathog 111:6–13. https://doi.org/10.1016/j.micpath.2017.08.008
Boucher JC, Schurr MJ, Deretic V (2000) Dual regulation of mucoidy in Pseudomonas aeruginosa and sigma factor antagonism. Mol Microbiol 36:341–351
Burrows LL (2012) Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 66:493–520. https://doi.org/10.1146/annurev-micro-092611-150055
Caiazza NC, Shanks RM, O’Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187:7351–7361. https://doi.org/10.1128/JB.187.21.7351-7361.2005
Caiazza NC, Merritt JH, Brothers KM, O’Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:3603–3612. https://doi.org/10.1128/JB.01685-06
Casciaro B, Lin Q, Afonin S, Loffredo MR, de Turris V, Middel V, Ulrich AS, Di YP, Mangoni ML (2019) Inhibition of Pseudomonas aeruginosa biofilm formation and expression of virulence genes by selective epimerization in the peptide Esculentin-1a(1-21)NH2. FEBS J. https://doi.org/10.1111/febs.14940
Cevik K, Ulusoy S (2015) Inhibition of Pseudomonas aeruginosa biofilm formation by 2,2'-bipyridyl, lipoic, kojic and picolinic acids. Iran J Basic Med Sci 18:758–763
Chang CY (2017) Surface sensing for biofilm formation in Pseudomonas aeruginosa. Front Microbiol 8:2671. https://doi.org/10.3389/fmicb.2017.02671
Chatterjee M, D'Morris S, Paul V, Warrier S, Vasudevan AK, Vanuopadath M, Nair SS, Paul-Prasanth B, Mohan CG, Biswas R (2017) Mechanistic understanding of phenyllactic acid mediated inhibition of quorum sensing and biofilm development in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 101:8223–8236. https://doi.org/10.1007/s00253-017-8546-4
Chung IY, Jang HJ, Bae HW, Cho YH (2014) A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. Proc Natl Acad Sci U S A 111:11503–11508. https://doi.org/10.1073/pnas.1403537111
Conrad JC, Gibiansky ML, ** F, Gordon VD, Motto DA, Mathewson MA, Stopka WG, Zelasko DC, Shrout JD, Wong GC (2011) Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys J 100:1608–1616. https://doi.org/10.1016/j.bpj.2011.02.020
D'Argenio DA, Miller SI (2004) Cyclic di-GMP as a bacterial second messenger. Microbiology 150:2497–2502. https://doi.org/10.1099/mic.0.27099-0
Das MC, Sandhu P, Gupta P, Rudrapaul P, De UC, Tribedi P, Akhter Y, Bhattacharjee S (2016a) Attenuation of Pseudomonas aeruginosa biofilm formation by vitexin: a combinatorial study with azithromycin and gentamicin. Sci Rep 6:23347. https://doi.org/10.1038/srep23347
Das MC, Paul S, Gupta P, Tribedi P, Sarkar S, Manna D, Bhattacharjee S (2016b) 3-Amino-4-aminoximidofurazan derivatives: small molecules possessing antimicrobial and antibiofilm activity against Staphylococcus aureus and Pseudomonas aeruginosa. J Appl Microbiol 120:842–859. https://doi.org/10.1111/jam.13063
de la Fuente-Núñez C, Korolik V, Bains M, Nguyen U, Breidenstein EB, Horsman S, Lewenza S, Burrows L, Hancock RE (2012) Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide. Antimicrob Agents Chemother 56:2696–2704. https://doi.org/10.1128/AAC.00064-12
de la Fuente-Núñez C, Reffuveille F, Haney EF, Straus SK, Hancock RE (2014) Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog 10:e1004152-e1004152. https://doi.org/10.1371/journal.ppat.1004152
Deziel E, Lepine F, Milot S, Villemur R (2003) rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149:2005–2013. https://doi.org/10.1099/mic.0.26154-0
Dos Santos Ramos MA, Da Silva PB, Spósito L, De Toledo LG, Bonifácio BV, Rodero CF, Dos Santos KC, Chorilli M, Bauab TM (2018) Nanotechnology-based drug delivery systems for control of microbial biofilms: a review. Int J Nanomedicine 13:1179–1213. https://doi.org/10.2147/IJN.S146195
El-Shaer S, Shaaban M, Barwa R, Hassan R (2016) Control of quorum sensing and virulence factors of Pseudomonas aeruginosa using phenylalanine arginyl beta-naphthylamide. J Med Microbiol 65:1194–1204. https://doi.org/10.1099/jmm.0.000327
Ferrer-Espada R, Shahrour H, Pitts B, Stewart PS, Sanchez-Gomez S, Martinez-de-Tejada G (2019) A permeability-increasing drug synergizes with bacterial efflux pump inhibitors and restores susceptibility to antibiotics in multi-drug resistant Pseudomonas aeruginosa strains. Sci Rep 9:3452. https://doi.org/10.1038/s41598-019-39659-4
Fong J, Mortensen KT, Nørskov A, Qvortrup K, Yang L, Tan CH, Nielsen TE, Givskov M (2018) Itaconimides as novel quorum sensing inhibitors of Pseudomonas aeruginosa. Front Cell Infect Microbiol 8:443. https://doi.org/10.3389/fcimb.2018.00443
Francis VI, Stevenson EC, Porter SL (2017) Two-component systems required for virulence in Pseudomonas aeruginosa. FEMS Microbiol Lett:364. https://doi.org/10.1093/femsle/fnx104
Fulcher NB, Holliday PM, Klem E, Cann MJ, Wolfgang MC (2010) The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Mol Microbiol 76:889–904. https://doi.org/10.1111/j.1365-2958.2010.07135.x
Furukawa S, Kuchma SL, O'Toole GA (2006) Kee** their options open: acute versus persistent infections. J Bacteriol 188:1211–1217. https://doi.org/10.1128/JB.188.4.1211-1217.2006
Gellatly SL, Hancock RE (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67:159–173. https://doi.org/10.1111/2049-632X.12033
Gibiansky ML, Conrad JC, ** F, Gordon VD, Motto DA, Mathewson MA, Stopka WG, Zelasko DC, Shrout JD, Wong GC (2010) Bacteria use type IV Pili to walk upright and detach from surfaces. Science 330:197–197. https://doi.org/10.1126/science.1194238
Glessner A, Smith RS, Iglewski BH, Robinson JB (1999) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J Bacteriol 181:1623–1629
Gupta P, Sarkar A, Sandhu P, Daware A, Das MC, Akhter Y, Bhattacharjee S (2017) Potentiation of antibiotic against Pseudomonas aeruginosa biofilm: a study with plumbagin and gentamicin. J Appl Microbiol 123:246–261. https://doi.org/10.1111/jam.13476
Gutierrez-Barranquero JA, Reen FJ, Parages ML, McCarthy R, Dobson ADW, O'Gara F (2019) Disruption of N-acyl-homoserine lactone-specific signalling and virulence in clinical pathogens by marine sponge bacteria. Microb Biotechnol 12:1049–1063. https://doi.org/10.1111/1751-7915.12867
Ha DG, O'Toole GA (2015) c-di-GMP and its effects on biofilm formation and dispersion: a Pseudomonas aeruginosa. Review Microbiol Spectr 3:MB-0003-2014. https://doi.org/10.1128/microbiolspec.MB-0003-2014
Heidari A, Noshiranzadeh N, Haghi F, Bikas R (2017) Inhibition of quorum sensing related virulence factors of Pseudomonas aeruginosa by pyridoxal lactohydrazone. Microb Pathog 112:103–110. https://doi.org/10.1016/j.micpath.2017.09.043
Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69:376–389. https://doi.org/10.1111/j.1365-2958.2008.06281.x
Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332. https://doi.org/10.1016/j.ijantimicag.2009.12.011
Hossain MA, Lee SJ, Park NH, Mechesso AF, Birhanu BT, Kang J, Reza MA, Suh JW, Park SC (2017) Impact of phenolic compounds in the acyl homoserine lactone-mediated quorum sensing regulatory pathways. Sci Rep 7:10618. https://doi.org/10.1038/s41598-017-10997-5
Husain FM, Ahmad I (2013) Doxycycline interferes with quorum sensing-mediated virulence factors and biofilm formation in gram-negative bacteria World. J Microbiol Biotechnol 29:949–957. https://doi.org/10.1007/s11274-013-1252-1
Inoue T, Shingaki R, Fukui K (2008) Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett 281:81–86. https://doi.org/10.1111/j.1574-6968.2008.01089.x
Jansari VH, Potharla VY, Riddell GT, Bardy SL (2016) Twitching motility and cAMP levels: signal transduction through a single methyl-accepting chemotaxis protein. FEMS Microbiol Lett:363. https://doi.org/10.1093/femsle/fnw119
Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8:634–644. https://doi.org/10.1038/nrmicro2405
Khan F, Manivasagan P, Lee JW, Pham DTN, Oh J, Kim YM (2019a) Fucoidan-stabilized gold nanoparticle-mediated biofilm inhibition, attenuation of virulence and motility properties in Pseudomonas aeruginosa PAO1. Mar Drugs 17. https://doi.org/10.3390/md17040208
Khan F, Javaid A, Kim YM (2019b) Functional diversity of quorum sensing receptors in pathogenic bacteria: interspecies, intraspecies and interkingdom level. Curr Drug Targets 20:655–667. https://doi.org/10.2174/1389450120666181123123333
Khan F, Manivasagan P, Pham DTN, Oh J, Kim SK, Kim YM (2019c) Antibiofilm and antivirulence properties of chitosan-polypyrrole nanocomposites to Pseudomonas aeruginosa. Microb Pathog 128:363–373. https://doi.org/10.1016/j.micpath.2019.01.033
Khan F, Lee JW, Manivasagan P, Pham DTN, Oh J, Kim YM (2019d) Synthesis and characterization of chitosan oligosaccharide-capped gold nanoparticles as an effective antibiofilm drug against the Pseudomonas aeruginosa PAO1. Microb Pathog 135:103623. https://doi.org/10.1016/j.micpath.2019.103623
Kim B, Park JS, Choi HY, Yoon SS, Kim WG (2018) Terrein is an inhibitor of quorum sensing and c-di-GMP in Pseudomonas aeruginosa: a connection between quorum sensing and c-di-GMP. Sci Rep 8:8617. https://doi.org/10.1038/s41598-018-26974-5
Kiymaci ME, Altanlar N, Gumustas M, Ozkan SA, Akin A (2018) Quorum sensing signals and related virulence inhibition of Pseudomonas aeruginosa by a potential probiotic strain's organic acid. Microb Pathog 121:190–197. https://doi.org/10.1016/j.micpath.2018.05.042
Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302. https://doi.org/10.1038/441300a
Kostakioti M, Hadjifrangiskou M, Hultgren SJ (2013) Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med 3:a010306. https://doi.org/10.1101/cshperspect.a010306
Kumar L, Chhibber S, Harjai K (2013) Zingerone inhibit biofilm formation and improve antibiofilm efficacy of ciprofloxacin against Pseudomonas aeruginosa PAO1. Fitoterapia 90:73–78. https://doi.org/10.1016/j.fitote.2013.06.017
Lee J, Attila C, Cirillo SL, Cirillo JD, Wood TK (2009) Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2:75–90. https://doi.org/10.1111/j.1751-7915.2008.00061.x
Lee JH, Kim YG, Cho MH, Kim JA, Lee J (2012) 7-Fluoroindole as an antivirulence compound against Pseudomonas aeruginosa. FEMS Microbiol Lett 329:36–44. https://doi.org/10.1111/j.1574-6968.2012.02500.x
Leighton TL, Buensuceso RN, Howell PL, Burrows LL (2015) Biogenesis of Pseudomonas aeruginosa type IV pili and regulation of their function. Environ Microbiol 17:4148–4163. https://doi.org/10.1111/1462-2920.12849
Li J, Metruccio MME, Evans DJ, Fleiszig SMJ (2017) Mucosal fluid glycoprotein DMBT1 suppresses twitching motility and virulence of the opportunistic pathogen Pseudomonas aeruginosa. PLoS Pathog 13:e1006392. https://doi.org/10.1371/journal.ppat.1006392
Li WR, Ma YK, Shi QS, **e XB, Sun TL, Peng H, Huang XM (2018) Diallyl disulfide from garlic oil inhibits Pseudomonas aeruginosa virulence factors by inactivating key quorum sensing genes. Appl Microbiol Biotechnol 102:7555–7564. https://doi.org/10.1007/s00253-018-9175-2
Lidor O, Al-Quntar A, Pesci EC, Steinberg D (2015) Mechanistic analysis of a synthetic inhibitor of the Pseudomonas aeruginosa LasI quorum-sensing signal synthase. Sci Rep 5:16569. https://doi.org/10.1038/srep16569
Lin Chua S, Liu Y, Li Y, Jun Ting H, Kohli GS, Cai Z, Suwanchaikasem P, Kau Kit Goh K, Pin Ng S, Tolker-Nielsen T, Yang L, Givskov M (2017) Reduced intracellular c-di-GMP content increases expression of quorum sensing-regulated genes in Pseudomonas aeruginosa. Front Cell Infect Microbiol 7:451. https://doi.org/10.3389/fcimb.2017.00451
Liu H, Gong Q, Luo C, Liang Y, Kong X, Wu C, Feng P, Wang Q, Zhang H, Wireko MA (2019) Synthesis and biological evaluation of novel L-homoserine lactone analogs as quorum sensing inhibitors of Pseudomonas aeruginosa. Chem Pharm Bull (Tokyo) 67:1088–1098. https://doi.org/10.1248/cpb.c19-00359
Lou Z, Letsididi KS, Yu F, Pei Z, Wang H, Letsididi R (2019) Inhibitive effect of eugenol and its nanoemulsion on quorum sensing-mediated virulence factors and biofilm formation by Pseudomonas aeruginosa. J Food Prot 82:379–389. https://doi.org/10.4315/0362-028X.JFP-18-196
Luo Y, Zhao K, Baker AE, Kuchma SL, Coggan KA, Wolfgang MC, Wong GC, O'Toole GA (2015) A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. MBio:6. https://doi.org/10.1128/mBio.02456-14
Luo J, Dong B, Wang K, Cai S, Liu T, Cheng X, Lei D, Chen Y, Li Y, Kong J, Chen Y (2017) Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS One 12:e0176883. https://doi.org/10.1371/journal.pone.0176883
Mah TF, O'Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39
Maier B, Wong GCL (2015) How bacteria use type IV pili machinery on surfaces. Trends Microbiol 23:775–788. https://doi.org/10.1016/j.tim.2015.09.002
Majik MS, Naik D, Bhat C, Tilve S, Tilvi S, D'Souza L (2013) Synthesis of (R)-norbgugaine and its potential as quorum sensing inhibitor against Pseudomonas aeruginosa. Bioorg Med Chem Lett 23:2353–2356. https://doi.org/10.1016/j.bmcl.2013.02.051
Manner S, Fallarero A (2018) Screening of natural product derivatives identifies two structurally related flavonoids as potent quorum sensing inhibitors against Gram-negative bacteria. Int J Mol Sci:19. https://doi.org/10.3390/ijms19051346
Marko VA, Kilmury SLN, MacNeil LT, Burrows LL (2018) Pseudomonas aeruginosa type IV minor pilins and PilY1 regulate virulence by modulating FimS-AlgR activity. PLoS Pathog 14:e1007074. https://doi.org/10.1371/journal.ppat.1007074
Masak J, Cejkova A, Schreiberova O, Rezanka T (2014) Pseudomonas biofilms: possibilities of their control. FEMS Microbiol Ecol 89:1–14. https://doi.org/10.1111/1574-6941.12344
Maurice NM, Bedi B, Sadikot RT (2018) Pseudomonas aeruginosa biofilms: host response and clinical implications in lung infections. Am J Respir Cell Mol Biol 58:428–439. https://doi.org/10.1165/rcmb.2017-0321TR
Mulcahy LR, Isabella VM, Lewis K (2014) Pseudomonas aeruginosa biofilms in disease. Microb Ecol 68:1–12. https://doi.org/10.1007/s00248-013-0297-x
Musthafa KS, Balamurugan K, Pandian SK, Ravi AV (2012) 2,5-Piperazinedione inhibits quorum sensing-dependent factor production in Pseudomonas aeruginosa PAO1. J Basic Microbiol 52:679–686. https://doi.org/10.1002/jobm.201100292
Nirody JA, Sun Y-R, Lo C-J (2017) The biophysicist’s guide to the bacterial flagellar motor. Advances in Physics: X 2:324–343. https://doi.org/10.1080/23746149.2017.1289120
Nolan LM, Cavaliere R, Turnbull L, Whitchurch CB (2015) Extracellular ATP inhibits twitching motility-mediated biofilm expansion by Pseudomonas aeruginosa. BMC Microbiol 15:55. https://doi.org/10.1186/s12866-015-0392-x
Norizan SN, Yin WF, Chan KG (2013) Caffeine as a potential quorum sensing inhibitor. Sensors (Basel) 13:5117–5129. https://doi.org/10.3390/s130405117
Oloketuyi SF, Khan F (2017) Strategies for biofilm inhibition and virulence attenuation of foodborne pathogen-Escherichia coli O157:H7. Curr Microbiol 74:1477–1489. https://doi.org/10.1007/s00284-017-1314-y
O'May C, Ciobanu A, Lam H, Tufenkji N (2012) Tannin derived materials can block swarming motility and enhance biofilm formation in Pseudomonas aeruginosa. Biofouling 28:1063–1076. https://doi.org/10.1080/08927014.2012.725130
Oura H, Tashiro Y, Toyofuku M, Ueda K, Kiyokawa T, Ito S, Takahashi Y, Lee S, Nojiri H, Nakajima-Kambe T, Uchiyama H, Futamata H, Nomura N (2015) Inhibition of Pseudomonas aeruginosa swarming motility by 1-naphthol and other bicyclic compounds bearing hydroxyl groups. Appl Environ Microbiol 81:2808–2818. https://doi.org/10.1128/AEM.04220-14
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. https://doi.org/10.1016/j.foodchem.2012.08.002
Parai D, Banerjee M, Dey P, Chakraborty A, Islam E, Mukherjee SK (2018) Effect of reserpine on Pseudomonas aeruginosa quorum sensing mediated virulence factors and biofilm formation. Biofouling 34:320–334. https://doi.org/10.1080/08927014.2018.1437910
Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP, Poole K (2008) Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 190:662–671. https://doi.org/10.1128/JB.01473-07
Pattnaik SS, Ranganathan S, Ampasala DR, Syed A, Ameen F, Busi S (2018) Attenuation of quorum sensing regulated virulence and biofilm development in Pseudomonas aeruginosa PAO1 by Diaporthe phaseolorum SSP12. Microb Pathog 118:177–189. https://doi.org/10.1016/j.micpath.2018.03.031
Pe** B, Ciric A, Markovic JD, Glamoclija J, Nikolic M, Stanimirovic B, Sokovic M (2015) Quercetin potently reduces biofilm formation of the strain Pseudomonas aeruginosa PAO1 in vitro. Curr Pharm Biotechnol 16:733–737
Petrov A, Lombardo S, Audette GF (2013) Fibril-mediated oligomerization of pilin-derived protein nanotubes. J Nanobiotechnology 11:24. https://doi.org/10.1186/1477-3155-11-24
Qu L, She P, Wang Y, Liu F, Zhang D, Chen L, Luo Z, Xu H, Qi Y, Wu Y (2016) Effects of norspermidine on Pseudomonas aeruginosa biofilm formation and eradication. Microbiologyopen 5:402–412. https://doi.org/10.1002/mbo3.338
Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52. https://doi.org/10.1128/MMBR.00043-12
Roudashti S, Zeighami H, Mirshahabi H, Bahari S, Soltani A, Haghi F (2017) Synergistic activity of sub-inhibitory concentrations of curcumin with ceftazidime and ciprofloxacin against Pseudomonas aeruginosa quorum sensing related genes and virulence traits. World J Microbiol Biotechnol 33:50. https://doi.org/10.1007/s11274-016-2195-0
Roy R, Tiwari M, Donelli G, Tiwari V (2018) Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence 9:522–554. https://doi.org/10.1080/21505594.2017.1313372
Scoffone VC, Trespidi G, Chiarelli LR, Barbieri G, Buroni S (2019) Quorum sensing as antivirulence target in cystic fibrosis pathogens. Int J Mol Sci:20. https://doi.org/10.3390/ijms20081838
Sheng JY, Chen TT, Tan XJ, Chen T, Jia AQ (2015) The quorum-sensing inhibiting effects of stilbenoids and their potential structure-activity relationship. Bioorg Med Chem Lett 25:5217–5220. https://doi.org/10.1016/j.bmcl.2015.09.064
Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, Parsek MR (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62:1264–1277. https://doi.org/10.1111/j.1365-2958.2006.05421.x
Singh VK, Mishra A, Jha B (2019) 3-Benzyl-Hexahydro-pyrrolo[1,2-a]pyrazine-1,4-dione extracted from exiguobacterium indicum showed anti-biofilm activity against Pseudomonas aeruginosa by attenuating quorum sensing. Front Microbiol 10:1269. https://doi.org/10.3389/fmicb.2019.01269
Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964. https://doi.org/10.1038/35023079
Tapia-Rodriguez MR, Bernal-Mercado AT, Gutierrez-Pacheco MM, Vazquez-Armenta FJ, Hernandez-Mendoza A, Gonzalez-Aguilar GA, Martinez-Tellez MA, Nazzaro F, Ayala-Zavala JF (2019) Virulence of Pseudomonas aeruginosa exposed to carvacrol: alterations of the quorum sensing at enzymatic and gene levels. J Cell Commun Signal:1–7. https://doi.org/10.1007/s12079-019-00516-8
Topa SH, Subramoni S, Palombo EA, Kingshott P, Rice SA, Blackall LL (2018) Cinnamaldehyde disrupts biofilm formation and swarming motility of Pseudomonas aeruginosa. Microbiology 164:1087–1097. https://doi.org/10.1099/mic.0.000692
Tremblay J, Deziel E (2010) Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 11:587. https://doi.org/10.1186/1471-2164-11-587
Turkina MV, Vikstrom E (2019) Bacteria-host crosstalk: sensing of the quorum in the context of Pseudomonas aeruginosa infections. J Innate Immun 11:263–279. https://doi.org/10.1159/000494069
Turner KH, Everett J, Trivedi U, Rumbaugh KP, Whiteley M (2014) Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLoS Genet 10:e1004518. https://doi.org/10.1371/journal.pgen.1004518
Tyers M, Wright GD (2019) Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nat Rev Microbiol 17:141–155. https://doi.org/10.1038/s41579-018-0141-x
Ugurlu A, Karahasan Yagci A, Ulusoy S, Aksu B, Bosgelmez-Tinaz G (2016) Phenolic compounds affect production of pyocyanin, swarming motility and biofilm formation of Pseudomonas aeruginosa. Asian Pacific Journal of Tropical Biomedicine 6:698–701. https://doi.org/10.1016/j.apjtb.2016.06.008
Ulrey RK, Barksdale SM, Zhou W, van Hoek ML (2014) Cranberry proanthocyanidins have anti-biofilm properties against Pseudomonas aeruginosa. BMC Complement Altern Med 14:499. https://doi.org/10.1186/1472-6882-14-499
Usjak D, Ivkovic B, Bozic DD, Boskovic L, Milenkovic M (2019) Antimicrobial activity of novel chalcones and modulation of virulence factors in hospital strains of Acinetobacter baumannii and Pseudomonas aeruginosa. Microb Pathog 131:186–196. https://doi.org/10.1016/j.micpath.2019.04.015
Uusitalo P, Hagglund U, Rhoos E, Scherman Norberg H, Elofsson M, Sundin C (2017) The salicylidene acylhydrazide INP0341 attenuates Pseudomonas aeruginosa virulence in vitro and in vivo. J Antibiot (Tokyo) 70:937–943. https://doi.org/10.1038/ja.2017.64
Vadekeetil A, Saini H, Chhibber S, Harjai K (2016) Exploiting the antivirulence efficacy of an ajoene-ciprofloxacin combination against Pseudomonas aeruginosa biofilm associated murine acute pyelonephritis. Biofouling 32:371–382. https://doi.org/10.1080/08927014.2015.1137289
Valentini M, Filloux A (2016) Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem 291:12547–12555. https://doi.org/10.1074/jbc.R115.711507
Valentini M, Gonzalez D, Mavridou DA, Filloux A (2018) Lifestyle transitions and adaptive pathogenesis of Pseudomonas aeruginosa. Curr Opin Microbiol 41:15–20. https://doi.org/10.1016/j.mib.2017.11.006
Valentini M, Laventie B-J, Moscoso J, Jenal U, Filloux A (2016) The diguanylate cyclase HsbD intersects with the hptb regulatory cascade to control Pseudomonas aeruginosa biofilm and motility. PLoS Genet 12:e1006354–e1006354. https://doi.org/10.1371/journal.pgen.1006354
Vasavi HS, Sudeep HV, Lingaraju HB, Shyam Prasad K (2017) Bioavailability-enhanced Resveramax modulates quorum sensing and inhibits biofilm formation in Pseudomonas aeruginosa PAO1. Microb Pathog 104:64–71. https://doi.org/10.1016/j.micpath.2017.01.015
Wang H, Chu W, Ye C, Gaeta B, Tao H, Wang M, Qiu Z (2019a) Chlorogenic acid attenuates virulence factors and pathogenicity of Pseudomonas aeruginosa by regulating quorum sensing. Appl Microbiol Biotechnol 103:903–915. https://doi.org/10.1007/s00253-018-9482-7
Wang TN, Guan QT, Pain A, Kaksonen AH, Hong PY (2019b) Discovering, characterizing, and applying acyl homoserine lactone-quenching enzymes to mitigate microbe-associated problems under saline conditions. Front Microbiol 10:823. https://doi.org/10.3389/fmicb.2019.00823
Wilhelm S, Gdynia A, Tielen P, Rosenau F, Jaeger KE (2007) The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J Bacteriol 189:6695–6703. https://doi.org/10.1128/JB.00023-07
Wolfe AJ, Visick KL (2008) Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190:463–475. https://doi.org/10.1128/JB.01418-07
Wu H, Lee B, Yang L, Wang H, Givskov M, Molin S, Høiby N, Song Z (2011) Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunol Med Microbiol 62:49–56. https://doi.org/10.1111/j.1574-695X.2011.00787.x
Wu H, Moser C, Wang HZ, Hoiby N, Song ZJ (2015a) Strategies for combating bacterial biofilm infections. Int J Oral Sci 7:1–7. https://doi.org/10.1038/ijos.2014.65
Wu DQ, Huang WF, Duan QJ, Cheng HJ, Wang CZ (2015b) Sodium houttuyfonate inhibits virulence related motility of Pseudomonas aeruginosa. Zhongguo Zhong Yao Za Zhi 40:1585–1588
Yang R, Guan Y, Zhou J, Sun B, Wang Z, Chen H, He Z, Jia A (2017) Phytochemicals from camellia nitidissima chi flowers reduce the pyocyanin production and motility of Pseudomonas aeruginosa PAO1. Front Microbiol 8:2640. https://doi.org/10.3389/fmicb.2017.02640
Yeung AT, Torfs EC, Jamshidi F, Bains M, Wiegand I, Hancock RE, Overhage J (2009) Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including. MetR J Bacteriol 191:5592–5602. https://doi.org/10.1128/JB.00157-09
Yin H, Deng Y, Wang H, Liu W, Zhuang X, Chu W (2015) Tea polyphenols as an antivirulence compound disrupt quorum-sensing regulated pathogenicity of Pseudomonas aeruginosa. Sci Rep 5:16158. https://doi.org/10.1038/srep16158
Zhang M, Wang M, Zhu X, Yu W, Gong Q (2018) Equisetin as potential quorum sensing inhibitor of Pseudomonas aeruginosa. Biotechnol Lett 40:865–870. https://doi.org/10.1007/s10529-018-2527-2
Zhao K, Tseng BS, Beckerman B, ** F, Gibiansky ML, Harrison JJ, Luijten E, Parsek MR, Wong GCL (2013) Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497:388–391. https://doi.org/10.1038/nature12155
Zhao J, Jiang H, Cheng W, Wu J, Zhao J, Wang J, Dong L (2015) The role of quorum sensing system in antimicrobial induced ampC expression in Pseudomonas aeruginosa biofilm. J Basic Microbiol 55:671–678. https://doi.org/10.1002/jobm.201300987
Zhao J, Li X, Hou X, Quan C, Chen M (2019) Widespread existence of quorum sensing inhibitors in marine bacteria: potential drugs to combat pathogens with novel strategies. Mar Drugs:17. https://doi.org/10.3390/md17050275
Zhou JW, Luo HZ, Jiang H, Jian TK, Chen ZQ, Jia AQ (2018) Hordenine: a novel quorum sensing inhibitor and antibiofilm agent against Pseudomonas aeruginosa. J Agric Food Chem 66:1620–1628. https://doi.org/10.1021/acs.jafc.7b05035
Zhou G, Peng H, Wang YS, Huang XM, **e XB, Shi QS (2019) Enhanced synergistic effects of xylitol and isothiazolones for inhibition of initial biofilm formation by Pseudomonas aeruginosa ATCC 9027 and Staphylococcus aureus ATCC 6538. J Oral Sci 61:255–263. https://doi.org/10.2334/josnusd.18-0102
Funding
This work was supported by Marine Biotechnology Program (Grant no. 20150220) funded by the Ministry of Oceans and Fisheries, Republic of Korea. This research was also supported by Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF-2019R1A2C1087156).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This review paper does not contain any studies with human participants or animals.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Khan, F., Pham, D.T.N., Oloketuyi, S.F. et al. Regulation and controlling the motility properties of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 104, 33–49 (2020). https://doi.org/10.1007/s00253-019-10201-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-10201-w