Abstract
Pathogenic biofilms have been associated with persistent infections due to their high resistance to antimicrobial agents. To identify nontoxic biofilm inhibitors for enterohemorrhagic Escherichia coli O157:H7, the spent media of a 4,104 Actinomycetes library was screened. The culture spent medium (1%, v/v) of plant pathogen Rhodococcus sp. BFI 332 markedly inhibited E. coli O157:H7 biofilm formation without affecting the growth of planktonic E. coli O157:H7 cells. Rhodococcus sp. BFI 332 produced significant amounts of indole-3-acetaldehyde and indole-3-acetic acid, and the former of which reduced E. coli O157:H7 biofilm formation. Global transcriptome analyses showed that indole-3-acetaldehyde most repressed two curli operons, csgBAC and csgDEFG, and induced tryptophanase (tnaAB) in E. coli O157:H7 biofilm cells. Electron microscopy showed that spent medium of Rhodococcus sp. BFI 332 and indole-3-acetaldehyde reduced curli production in E. coli O157:H7. The spent medium of Rhodococcus sp. BFI 332 also significantly reduced the biofilm formation of Staphylococcus aureus and Staphylococcus epidermidis. Overall, this study suggests that indole derivatives are present in the Actinomycetes strains and they can be used as biofilm inhibitors against pathogenic bacteria.
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References
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
Bansal T, Englert D, Lee J, Hegde M, Wood TK, Jayaraman A (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75:4597–4607
Bokranz W, Wang X, Tschäpe H, Römling U (2005) Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 54:1171–1182
Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855
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
Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
Crespi M, Messens E, Caplan AB, van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11:795–804
Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689.
Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171–1175
Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379:324–329
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
Lee J-H, Lee J (2010) Indole as an intercellular signal in microbial community. FEMS Microbiol Rev 34:426–444
Lee J, Bansal T, Jayaraman A, Bentley WE, Wood TK (2007) Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 73:4100–4109
Lee J-H, Cho MH, Lee J (2011) 3-Indolylacetonitrile decreases Escherichia coli O157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ Microbiol 13:62–73
McNeil MM, Brown JM (1994) The medically important aerobic actinomycetes: epidemiology and microbiology. Clin Microbiol Rev 7:357–417
Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11:142–201
Patel J, Sharma M, Ravishakar S (2011) Effect of curli expression and hydrophobicity of Escherichia coli O157:H7 on attachment to fresh produce surfaces. J Appl Microbiol 110:737–745
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
Rivas L, Dykes GA, Fegan N (2007) A comparative study of biofilm formation by Shiga toxigenic Escherichia coli using epifluorescence microscopy on stainless steel and a microtitre plate method. J Microbiol Methods 69:44–51
Römling U, Bian Z, Hammar M, Sierralta WD, Normark S (1998) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731
Ryu JH, Beuchat LR (2005) Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl Environ Microbiol 71:247–254
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
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
Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128
Tarr PI, Gordon CA, Chandler WL (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073–1086
Uhlich GA, Cooke PH, Solomon EB (2006) Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl Environ Microbiol 72:2564–2572
Vandeputte O, Oden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl Environ Microbiol 71:1169–1177
Vikram A, Jesudhasan PR, Jayaprakasha GK, Pillai BS, Patil BS (2010a) Grapefruit bioactive limonoids modulate E. coli O157:H7 TTSS and biofilm. Int J Food Microbiol 140:109–116
Vikram A, Jayaprakasha GK, Jesudhasan PR, Pillai SD, Patil BS (2010b) Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J Appl Microbiol 109:515–527
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
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
Acknowledgments
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology (2011-0026639) and was also supported by a grant from KRIBB Research Initiative Program.
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Lee, JH., Kim, YG., Kim, CJ. et al. Indole-3-acetaldehyde from Rhodococcus sp. BFI 332 inhibits Escherichia coli O157:H7 biofilm formation. Appl Microbiol Biotechnol 96, 1071–1078 (2012). https://doi.org/10.1007/s00253-012-3881-y
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DOI: https://doi.org/10.1007/s00253-012-3881-y