Abstract
In this study, a total of 147 soil actinobacterial strains were screened for their ability to inhibit response of Chromobacterium violaceum CV026 to short chain N-acyl homoserine lactone (AHL) which is a quorum sensing molecule. Of these, three actinobacterial strains showed positive for violacein inhibition. We further tested these strains for the inhibition of Pseudomonas aeruginosa PAO1 quorum sensing-regulated phenotypes, namely, swarming and pyocyanin production. The three strains were found to inhibit at least one of the quorum sensing-regulated phenotypes of PAO1. Phylogenetic analysis of the 16S rRNA gene sequences indicated that these strains belong to the genera Micromonospora, Rhodococcus and Streptomyces. This is the first report presenting quorum quenching activity by a species of the genus Micromonospora. Our data suggest that Actinobacteria may be a rich source of active compounds that can act against bacterial quorum sensing system.
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References
Abed RMM, Dobretsov S, Al-Fori M, Gunasekera SP, Sudesh K, Paul VJ (2013) Quorum-sensing inhibitory compounds from extremophilic microorganisms isolated from a hypersaline cyanobacterial mat. J Ind Microbiol Biot 40:759–772. doi:10.1007/s10295-013-1276-4
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST†¯: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389
Babić F, Venturi V, Maravić-Vlahoviček G (2010) Tobramycin at subinhibitory concentration inhibits the RhlI/R quorum sensing system in a Pseudomonas aeruginosa environmental isolate. BMC Infect Dis 10:148. doi:10.1186/1471-2334-10-148
Bhardwaj AK, Vinothkumar K, Rajpara N (2013) Bacterial quorum sensing inhibitors: attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Patents Anti Infect Drug Discov 8:68–83. doi:10.2174/1574891X11308010012
Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, McCoy WF (2001) Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl Environ Microb 67:3174–3179. doi:10.1128/AEM.67.7.3174-3179.2001
Brint JM, Ohman DE (1995) Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR–RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR–LuxI family. J Bacteriol 177:7155–7163. doi:10.1128/jb.177.24.7155-7163.1995
Chan K-G, Yin W-F, Sam C-K, Koh C-L (2009) A novel medium for the isolation of N-acylhomoserine lactone-degrading bacteria. J Ind Microbiol Biot 36:247–251. doi:10.1007/s10295-008-0491-x
Chan K-G, Atkinson S, Mathee K, Sam CK, Chhabra SR, Cámara M, Koh CL, Williams P (2011) Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol 11:51–63. doi:10.1186/1471-2180-11-51
Chang CY, Krishnan T, Wang H, Chen, Y, Yin WF, Chong YM, Tan LY, Chong TM, Chan KG (2014) Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target. Sci Rep 4:7245. doi:10.1038/srep07245
Chankhamhaengdecha S, Hongvijit S, Srichaisupakit A, Charnchai P, Panbangred W (2013) Endophytic actinomycetes: a novel source of potential acyl homoserine lactone degrading enzymes. BioMed Res Int 2013:1–8. doi:10.1155/2013/782847
Chong YM, Yin WF, Ho CY, Mustafa MR, Hadi AHA, Awang K, Narrima P, Koh CL, Appleton DR, Chan KG (2011) Malabaricone C from Myristica cinnamomea exhibits anti-quorum sensing activity. J Nat Prod 74:2261–2264. doi:10.1021/np100872k
Cirou A, Mondy S, An S, Charrier A, Sarrazin A, Thoison O, DuBow M, Faure D (2012) Efficient biostimulation of native and introduced quorum-quenching Rhodococcus erythropolis populations is revealed by a combination of analytical chemistry, microbiology, and pyrosequencing. Appl Environ Microb 78:481–492. doi:10.1128/AEM.06159-11
Conti R, Cunha IGB, Siqueira VM, Souza-Motta CM, Amorim ELC, Janete M (2012) Endophytic microorganisms from leaves of Spermacoce verticillata (L.): diversity and antimicrobial activity. J Appl Pharm Sci 2:17–22. doi:10.7324/JAPS.2012.21204
Darabpour E, Ardakani MR, Motamedi H, Ronagh MT (2012) Isolation of a broad spectrum antibiotic producer bacterium, Pseudoalteromonas piscicida PG-02, from the Persian Gulf. Bangladesh J Pharmacol 6:74–83. doi:10.3329/bjp.v6i2.8592
De Kievit TR, Iglewski BH (2000) Bacterial quorum sensing in pathogenic relationships. Infect Immun 68:4839–4849. doi:10.1128/IAI.68.9.4839-4849.2000
Demain AL, Fang A (2000) The natural functions of secondary metabolites. In: Scheper T (ed) Advances in biochemical engineering/biotechnology. Springer, Berlin, pp 1–39
Dong Y-H, Gusti AR, Zhang Q, Xu J-L, Zhang L-H (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microb 68:1754–1759. doi:10.1128/AEM.68.4.1754-1759.2002
Fukumoto A, Murakami C, Anzai Y, Kato F (2016) Maniwamycins: new quorum-sensing inhibitors against Chromobacterium violaceum CV026 were isolated from Streptomyces sp. TOHO-M025. J Antibiot 69:395–399. doi:10.1038/ja.2015.126
Ghani N, Norizan S, Chan XY, Yin W-F, Chan K-G (2014) Labrenzia sp. BM1: a quorum quenching bacterium that degrades N-acyl homoserine lactones via lactonase activity. Sensors Basel 14:11760–11769. doi:10.3390/s140711760
Gray KM, Garey JR (2001) The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 147:2379–2387. doi:10.1099/00221287-147-8-2379
Hassan R, Shaaban MI, Bar FMA, El-Mahdy AM, Shokralla S (2016) Quorum sensing inhibiting activity of Streptomyces coelicoflavus isolated from soil. Front Microbiol 7:659. doi:10.3389/fmicb.2016.00659
Hong KW, Koh CL, Sam CK, Yin WF, Chan KG (2012) Quorum quenching revisited-from signal decays to signalling confusion. Sensors Basel 12:4661–4696. doi:10.3390/s120404661
Kalia VC, Raju SC, Purohit HJ (2011) Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and -lactonase. Open Microbiol J 5:1–13. doi:10.2174/1874285801105010001
Kang JE, Han JW, Jeon BJ, Kim BS (2016) Efficacies of quorum sensing inhibitors, piericidin A and glucopiericidin A, produced by Streptomyces xanthocidicus KPP01532 for the control of potato soft rot caused by Erwinia carotovora subsp. atroseptica. Microbiol Res 184:32–41. doi:10.1016/j.micres.2015.12.005
Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8:634–644. doi:10.1038/nrmicro2405
Köhler T, Curty LK, Barja F, van Delden C, Pechère J-C (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990–5996. doi:10.1128/JB.182.21.5990-5996.2000
Kumar S, Kaushik N, Proksch P (2013) Identification of antifungal principle in the solvent extract of an endophytic fungus Chaetomium globosum from Withania somnifera. SpringerPlus 2:37. doi:10.1186/2193-1801-2-37
Lade H, Paul D, Kweon JH (2014) N-Acyl homoserine lactone-mediated quorum sensing with special reference to use of quorum quenching bacteria in membrane biofouling control. BioMed Res Int 2014:162584. doi:10.1155/2014/162584
Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959
Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41. doi:10.1007/s13238-014-0100-x
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. doi:10.1038/srep16569
Lin Y-H, Xu J-L, Hu J, Wang L-H, Ong SL, Leadbetter JR, Zhang L-H (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47:849–860. doi:10.1046/j.1365-2958.2003.03351.x
Manefield M, De Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:283–291. doi:10.1099/13500872-145-2-283
McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GSAB, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703–3711. doi:10.1099/00221287-143-12-3703
Morkunas B, Galloway WRJD, Wright M, Ibbeson BM, Hodgkinson JT, O’Connell KMG, Bartolucci N, Valle MD, Welch M, Spring DR (2012) Inhibition of the production of the Pseudomonas aeruginosa virulence factor pyocyanin in wild-type cells by quorum sensing autoinducer-mimics. Org Biomol Chem 10:8452–8464. doi:10.1039/c2ob26501j
Morohoshi T, Fukamachi K, Kato M, Kato N, Ikeda T (2010) Regulation of the violacein biosynthetic gene cluster by acylhomoserine lactone-mediated quorum sensing in Chromobacterium violaceum ATCC 12472. Biosci Biotechnol Biochem 74:2116–2119. doi:10.1271/bbb.100385
Naik DN, Wahidullah S, Meena RM (2013) Attenuation of Pseudomonas aeruginosa virulence by marine invertebrate-derived Streptomyces sp. Lett Appl Microbiol 56:197–207. doi:10.1111/lam.12034
Norizan SNM, Yin WF, Chan KG (2013) Caffeine as a potential quorum sensing inhibitor. Sensors Basel 13:5117–5129. doi:10.3390/s130405117
O’May C, Tufenkji N (2011) The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials. Appl Environ Microb 77:3061–3067. doi:10.1128/AEM.02677-10
Ooka K, Fukumoto A, Yamanaka T, Shimada K (2013) Piericidins, novel quorum-sensing inhibitors against Chromobacterium violaceum CV026, from Streptomyces sp. TOHO-Y209 and TOHO-O348. Open J Med Chem 3:93–99. doi:10.4236/ojmc.2013.34012
Overhage J, Bains M, Brazas MD, Hancock REW (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190:2671–2679. doi:10.1128/JB.01659-07
Park S-Y, Kang H-O, Jang H-S, Lee J-K, Koo B-T (2005) Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microb 71:2632–2641. doi:10.1128/AEM.71.5.2632-2641.2005
Park S-Y, Hwang B-J, Shin M-H, Kim J-A, Kim H-K, Lee J-K (2006) N-Acylhomoserine lactonase producing Rhodococcus spp. with different AHL-degrading activities. FEMS Microbiol Lett 261:102–108. doi:10.1111/j.1574-6968.2006.00336.x
Pazhanimurugan R, Gopikrishnan V, Shanmuga-Sundaram T, Radhakrishnan M, Balagurunathan R (2012) Bioactive potential of actinobacteria against drug resistant pathogens. J Appl Pharm Sci 2:167–173. doi:10.7324/JAPS.2012.2542
Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132. doi:10.1128/jb.179.10.3127-3132.1997
Priya K, Yin WF, Chan KG (2013) Anti-quorum sensing activity of the traditional Chinese herb, Phyllanthus amarus. Sensors Basel 13:14558–14569. doi:10.3390/s131114558
Rasamiravaka T, Labtani Q, Duez P, Jaziri ME (2015) The formation of biofilms by Pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. BioMed Res Int 2015:1–17. doi:10.1155/2015/759348
Rasmussen TB, Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296:149–161. doi:10.1016/j.ijmm.2006.02.005
Reading NC, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11. doi:10.1111/j.1574-6968.2005.00001.x
Romero M, Martin-Cuadrado A-B, Roca-Rivada A, Cabello AM, Otero A (2011) Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol Ecol 75:205–217. doi:10.1111/j.1574-6941.2010.01011.x
Sharma D, Kaur T, Chadha B, Manhas R (2011) Antimicrobial activity of actinomycetes against multidrug resistant Staphylococcus aureus, E. coli and various other pathogens. Trop J Pharm Res 10:801–808. doi:10.4314/tjpr.v10i6.14
Supaphon P, Phongpaichit S, Rukachaisirikul V, Sakayaroj J (2013) Antimicrobial potential of endophytic fungi derived from three seagrass species: Cymodocea serrulata, Halophila ovalis and Thalassia hemprichii. PLoS One 8:e72520. doi:10.1371/journal.pone.0072520
Tan LY, Yin WF, Chan KG (2012) Silencing quorum sensing through extracts of Melicope lunu-ankenda. Sensors Basel 12:4339–4351. doi:10.3390/s120404339
Tan LY, Yin WF, Chan KG (2013) Piper nigrum, Piper betle and Gnetum gnemon-natural food sources with anti-quorum sensing properties. Sensors Basel 13:3975–3985. doi:10.3390/s130303975
Uroz S, Chhabra SR, Cámara M, Williams P, Oger P, Dessaux Y (2005) N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151:3313–3322. doi:10.1099/mic.0.27961-0
Uroz S, Oger PM, Chapelle E, Adeline M-T, Faure D, Dessaux Y (2008) A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl Environ Microb 74:1357–1366. doi:10.1128/AEM.02014-07
Valan AM, Asha K, Duraipandiyan V, Ignacimuthu S, Agastian P (2012) Characterization and phylogenetic analysis of novel polyene type antimicrobial metabolite producing actinomycetes from marine sediments: Bay of Bengal India. Asian Pacific J Trop Biomed 2:803–810. doi:10.1016/S2221-1691(12)60233-0
Vijayakumar R, Selvam KP, Muthukumar C, Thajuddin N, Panneerselvam A, Saravanamuthu R (2012) Antimicrobial potentiality of a halophilic strain of Streptomyces sp. VPTSA18 isolated from the saltpan environment of Vedaranyam, India. Ann Microbiol 62:1039–1047. doi:10.1007/s13213-011-0345-z
Visick KL, Fuqua C (2005) Decoding microbial chatter: cell–cell communication in bacteria. J Bacteriol 187:5507–5519. doi:10.1128/JB.187.16.5507-5519.2005
Wang WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T (2010) AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microb 76:2524–2530. doi:10.1128/AEM.02738-09
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. doi:10.1146/annurev.cellbio.21.012704.131001
Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Cámara M, Smith H, Williams P (2002) N-Acylhomoserine actones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70:5635–5646. doi:10.1128/IAI.70.10.5635-5646.2002
Zhang W, Li C (2016) Exploiting quorum sensing interfering strategies in Gram-negative bacteria for the enhancement of environmental applications. Front Microbiol 6:1535. doi:10.3389/fmicb.2015.01535
Acknowledgements
The authors gratefully acknowledge the Grants from University of Malaya (High Impact Research Grant: UM.C/625/1/HIR/MOHE/CHAN/01, Grant No. A-000001-50001 and UM-MOHE HIR Grant UM.C/625/1/HIR/MOHE/CHAN/14/1, No. H-50001-A000027 to KGC) and HIR-005.
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Communicated by Yusuf Akhter.
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Devaraj, K., Tan, G.Y.A. & Chan, KG. Quorum quenching properties of Actinobacteria isolated from Malaysian tropical soils. Arch Microbiol 199, 897–906 (2017). https://doi.org/10.1007/s00203-017-1371-4
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DOI: https://doi.org/10.1007/s00203-017-1371-4