Skip to main content
SpringerLink
Log in

Antibiofilm activity of Streptomyces sp. BFI 230 and Kribbella sp. BFI 1562 against Pseudomonas aeruginosa

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Members of the actinomycetes family are a rich source of bioactive compounds including diverse antibiotics. This study sought to identify novel and non-toxic biofilm inhibitors from the actinomycetes library for reducing the biofilm formation of Pseudomonas aeruginosa PAO1. After the screening of 4104 actinomycetes strains, we found that the culture spent medium (1 %, v/v) of Streptomyces sp. BFI 230 and Kribbella sp. BFI 1562 inhibited P. aeruginosa biofilm formation by 90 % without affecting the growth of planktonic P. aeruginosa cells, while the spent media enhanced the swarming motility of P. aeruginosa. Global transcriptome analyses revealed that the spent medium of Streptomyces sp. BFI 230 induced expression of phenazine, pyoverdine, pyochelin synthesis genes, and iron uptake genes in P. aeruginosa. The addition of exogenous iron restored the biofilm formation and swarming motility of P. aeruginosa in the presence of the spent medium of Streptomyces sp. BFI 230, which suggests that the Streptomyces sp. BFI 230 strain interfered iron acquisition in P. aeruginosa. Experiments on solvent extraction, heat treatment, and proteinase K treatment suggested that hydrophilic compound(s), possibly extracellular peptides or proteins from Streptomyces sp. BFI 230 cause the biofilm reduction of P. aeruginosa. Together, this study indicates that actinomycetes strains have an ability to control the biofilm of P. aeruginosa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Attila C, Ueda A, Cirillo SLG, Cirillo JD, Chen W, Wood TK (2008) Pseudomonas aeruginosa PAO1 virulence factors and poplar tree response in the rhizosphere. Microb Biotechnol 1:17–29

    CAS  Google Scholar 

  • Bakkiyaraj D, Pandian SK (2010) In vitro and in vivo antibiofilm activity of a coral associated actinomycete against drug resistant Staphylococcus aureus biofilms. Biofouling 26:711–717

    Article  CAS  Google Scholar 

  • Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102:11076–11081

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Challis GL, Ravel J (2000) Coelichelin, a new peptide siderophore encoded by the Streptomyces coelicolor genome: structure prediction from the sequence of its non-ribosomal peptide synthetase. FEMS Microbiol Lett 187:111–114

    Article  CAS  Google Scholar 

  • Chun J, Youn HD, Yim YI, Lee H, Kim MY, Hah YC, Kang SO (1997) Streptomyces seoulensis sp. nov. Int J Syst Bacteriol 47:492–498

    Article  CAS  Google Scholar 

  • Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    Article  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  CAS  Google Scholar 

  • Cox CD (1982) Effect of pyochelin on the virulence of Pseudomonas aeruginosa. Infect Immun 36:17–23

    CAS  Google Scholar 

  • Davies DG, Marques CN (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393–1403

    Article  CAS  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689

    Article  CAS  Google Scholar 

  • Essar DW, Eberly L, Hadero A, Crawford IP (1990) Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 172:884–900

    CAS  Google Scholar 

  • Everest GJ, Meyers PR (2008) Kribbella hippodromi sp. nov., isolated from soil from a racecourse in South Africa. Int J Syst Evol Microbiol 58:443–446

    Article  CAS  Google Scholar 

  • Garo E, Eldridge GR, Goering MG, DeLancey PE, Hamilton MA, Costerton JW, James GA (2007) Asiatic acid and corosolic acid enhance the susceptibility of Pseudomonas aeruginosa biofilms to tobramycin. Antimicrob Agents Chemother 51:1813–1817

    Article  CAS  Google Scholar 

  • Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Hoiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815

    Article  CAS  Google Scholar 

  • Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171–1175

    Article  CAS  Google Scholar 

  • Imperi F, Tiburzi F, Visca P (2009) Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 106:20440–20445

    Article  CAS  Google Scholar 

  • Kageyama A, Yazawa K, Nishimura K, Mikami Y (2004) Nocardia inohanensis sp. nov., Nocardia yamanashiensis sp. nov. and Nocardia niigatensis sp. nov., isolated from clinical specimens. Int J Syst Evol Microbiol 54:563–569

    Article  CAS  Google Scholar 

  • Köhler T, Curty LK, Barja F, van Delden C, Pechère JC (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990–5996

    Article  Google Scholar 

  • Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R (2010) d-amino acids trigger biofilm disassembly. Science 328:627–629

    Article  CAS  Google Scholar 

  • Labeda DP, Lechevalier MP, Testa RT (1997) Streptomyces stramineus sp. nov., a new species of the verticillate streptomycetes. Int J Syst Bacteriol 47:747–753

    Article  CAS  Google Scholar 

  • Lee J, Attila C, Cirillo SL, Cirillo JD, Wood TK (2009) Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2:75–90

    Article  CAS  Google Scholar 

  • Lee JH, Cho MH, Lee J (2011) 3-Indolylacetonitrile decreases Escherichia coli O157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ Microbiol 13:62–73

    Article  CAS  Google Scholar 

  • Lee JH, Kim YG, Kim CJ, Lee JC, Cho MH, Lee J (2012) Indole-3-acetaldehyde from Rhodococcus sp. BFI 332 inhibits Escherichia coli O157:H7 biofilm formation. Appl Microbiol Biotechnol. doi:10.1007/s00253-00012-03881-y

  • McNeil MM, Brown JM (1994) The medically important aerobic actinomycetes: epidemiology and microbiology. Clin Microbiol Rev 7:357–417

    CAS  Google Scholar 

  • Michel L, Gonzalez N, Jagdeep S, Nguyen-Ngoc T, Reimmann C (2005) PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol Microbiol 58:495–509

    Article  CAS  Google Scholar 

  • Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451

    Article  CAS  Google Scholar 

  • Musk DJ, Banko DA, Hergenrother PJ (2005) Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chem Biol 12:789–796

    Article  CAS  Google Scholar 

  • Overhage J, Lewenza S, Marr AK, Hancock RE (2007) Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 Mini-Tn5-lux mutant library. J Bacteriol 189:2164–2169

    Article  CAS  Google Scholar 

  • Overhage J, Bains M, Brazas MD, Hancock RE (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190:2671–2679

    Article  CAS  Google Scholar 

  • Park JH, Lee JH, Kim CJ, Lee JC, Cho MH, Lee J (2012) Extracellular protease in Actinomycetes culture supernatants inhibits and detaches Staphylococcus aureus biofilm formation. Biotechnol Lett 34:655–661

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pratt LA, Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30:285–293

    Article  CAS  Google Scholar 

  • Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524

    Article  CAS  Google Scholar 

  • Ren D, Zuo R, Wood TK (2005) Quorum-sensing antagonist (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone influences siderophore biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa. Appl Microbiol Biotechnol 66:689–695

    Article  CAS  Google Scholar 

  • Rong X, Huang Y (2012) Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA–DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 35:7–18

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326

    Article  CAS  Google Scholar 

  • Singh PK, Parsek MR, Greenberg EP, Welsh MJ (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417:552–555

    Article  CAS  Google Scholar 

  • Sperandio V, Torres AG, Kaper JB (2002) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809–821

    Article  CAS  Google Scholar 

  • Stintzi A, Evans K, Meyer JM, Poole K (1998) Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166:341–345

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tamaoka, Komagata (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128

    Article  CAS  Google Scholar 

  • Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30

    Article  CAS  Google Scholar 

  • Wilhelm S, Gdynia A, Tielen P, Rosenau F, Jaeger K-E (2007) The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J Bacteriol 189:6695–6703

    Article  CAS  Google Scholar 

  • Wu H, Lee B, Yang L, Wang H, Givskov M, Molin S, Hoiby N, Song Z (2011) Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunol Med Microbiol 62:49–56

    Article  CAS  Google Scholar 

  • Xu P, Li WJ, Wu WL, Wang D, Xu LH, Jiang CL (2004) Streptomyces hebeiensis sp. nov. Int J Syst Evol Microbiol 54:727–731

    Article  CAS  Google Scholar 

  • Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328

    Article  CAS  Google Scholar 

  • You J, Xue X, Cao L, Lu X, Wang J, Zhang L, Zhou S (2007) Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Appl Microbiol Biotechnol 76:1137–1144

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2010-0021871). We thank Prof. Sangwoo Joo of the World Class University Nano Research Center at Yeungnam University for providing a scanning confocal laser microscopy.

Author information

Authors and Affiliations

  1. School of Chemical Engineering, Yeungnam University, Gyeongsan, Republic of Korea

    Yong-Guy Kim, Jin-Hyung Lee, Moo Hwan Cho & Jintae Lee

  2. Biological Resource Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea

    Chang-Jin Kim, Jae-Chan Lee & Yoon Jung Ju

Authors
  1. Yong-Guy Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jin-Hyung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jae-Chan Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoon Jung Ju
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Moo Hwan Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jintae Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jintae Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 29 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, YG., Lee, JH., Kim, CJ. et al. Antibiofilm activity of Streptomyces sp. BFI 230 and Kribbella sp. BFI 1562 against Pseudomonas aeruginosa . Appl Microbiol Biotechnol 96, 1607–1617 (2012). https://doi.org/10.1007/s00253-012-4225-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4225-7

Keywords

Search

Navigation