Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli

Biotechnology and Bioengineering

Volumn 88, Issue 5, 2004, Pages 630-642

  Ren, Dacheng ^a,c   Bedzyk, Laura A ^b   Ye, Rick W ^b   Thomas, Stuart M ^b   Wood, Thomas K ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b DUPONT COMPANY   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

AI 2; Furanone; Quorum sensing antagonist

Indexed keywords

ALGAE; BIOASSAY; BROMINE COMPOUNDS; CELLS; DNA; ESCHERICHIA COLI; ETHYLENE; KETONES; RNA;

DELISEA PULCHRA; FURANONE; GENE EXPRESSIONS; QUORUM SENSING DISRUPTOR;

GENES;

4 BROMO 5 (BROMOMETHYLENE) 3 BUTYL 2(5H) FURANONE; AUTOINDUCER 2; FURANONE DERIVATIVE; GENE PRODUCT; UNCLASSIFIED DRUG;

AER GENE; ALGA; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BROMINATION; CELL MOTILITY; CHEMOTAXIS; DELISEA PULCHRA; DNA MICROARRAY; ESCHERICHIA COLI; ESCHERICHIA COLI K 12; FLAGELLUM; GENE EXPRESSION; GENE FUNCTION; GENE INDUCTION; GENE REPRESSION; GENETIC TRANSCRIPTION; LUXS GENE; NONHUMAN; PFS GENE; REGULON; RNA HYBRIDIZATION; SIGNAL TRANSDUCTION; TSR GENE;

CHEMOTAXIS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FURANS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; LACTONES; SIGNAL TRANSDUCTION;

ALGAE; BACTERIA (MICROORGANISMS); DELISEA; DELISEA PULCHRA; ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 10644252538     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20259     Document Type: Article

References (53)

1. Bassler BL. 1999. How bacteria talk to each other: Regulation of gene expression by quorum, sensing. Curr Opin Microbiol 2:582-587.
2. Bassler BL, Wright M, Silverman MR. 1994. Multiple signaling systems controlling expression of luminescence in Vibrio harveyi: Sequence and function of genes encoding a second sensory, pathway. Molec Microbiol 13:273-286.
3. Beck von Bodman S, Majerczak DR, Coplin DL. 1998. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii, subsp. stewartii. Proc Natl Acad Sci USA 95:7687-7692.
4. Beechan CM, Sims JJ. 1979. The first synthesis of fimbrolides, a novel class of halogenated lactones naturally occuring in the red seaweed Delisea fimbriata (Bonnemaisoniaceae). Tetrahedron Lett 19:1649-1652.
5. Blattner FR, Plunkett G III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462.
6. Cao J-G, Meighen EA. 1989. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. T J Biol Chem 264:21670-21676.
7. Chen X, Schauder S, Potier N, Dorsselaer AV, Pelczer I, Bassler BL, Hughson FM. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549.
8. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
9. DeLisa MP, Valdes JJ, Bentley WE. 2001a. Quorum signaling via AI-2 communicates the "metabolic burden" associated with heterologous protein expression in Escherichia coli. Biotechnol Bioeng 75:439-450.
10. DeLisa MP, Wu C-F, Wang L, Valdes JJ, Bently WE. 2001b. DNA microarray-based identification of genes controlled by autoinducer 2-Stimulated quorum sensing in Escherichia coli. J Bacteriol 183:5239-5247.
11. Fawcett P, Eichenberger P, Losick R, Youngman P. 2000. The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 97:8063-8068.
12. Fong KP, Chung WO, Lamont RJ, Demuth DR. 2001. Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infection and Immunity 69:7625-7634.
13. Garrett RH, Grisham CM. 1999. Biochemistry. Orlando, FL: Harcourt Brace & Company.
14. Ghigo J-M. 2001. Natural conjugative plasmids induce bacterial biofilm, development. Nature 412:442-445.
15. Gram L, de Nys R, Maximilien R, Givskov M, Steinberg P, Kjelleberg S. 1996. Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Appl Environ Microbiol 62:4284-4287.
16. Greenberg EP, Hastings JW, Ulitzur S. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87-91.
17. Helmann JD, Wu MFW, Kobel PA, Gamo F-J, Wilson M, Morshedi MM, Navre M, Paddon C. 2001. Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183:7318-7328.
18. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, et al. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87-102.
19. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, et al. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. Eur Molec Biol Org J 22:3803-3815.
20. Ide N, Kutsukake K. 1997. Identification of a novel Escherichia coli gene whose expression is dependent on the flagellum-specific sigma factor, FliA, but dispensable for motility development. Gene 199:19-23.
21. Li Y-H, Lau PCY, Lee JH, Ellen RP, Cvitkovitch DG. 2001. Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897-908.
22. Lilley BN, Bassler BL. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma-54. Molec Microbiol 36:940-954.
23. Lithgow JK, Danino VE, Jones J, Downie JA. 2001. Analysis of N-acyl homoserine-lactone quorum-sensing molecules made by different strains and biovars of Rhizobium Leguminosarum containing different symbiotic plasmids. Plant Soil 232:3-12.
24. 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.
25. Manefield M, Harris L, Rice SA, de Nys R, Kjelleberg S. 2000. Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl Environ Microbiol 66:2079-2084.
26. Manefield M, Rasmussen TB, Hentzer M, Anderson JB, Steinberg P, Kjelleberg S, Givskov M. 2002. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148:1119-1127.
27. Manny AJ, Kjelleberg S, Kumar N, de Nys R, Read RW, Steinberg P. 1997. Reinvestigation of the sulfuric acid-catalysed cyclisation of brominated 2-alkyllevulinic acids to 3-alkyl-5-methylene-2(5H)-furanones. Tetrahedron 53:15813-15826.
28. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS, Lamont RJ. 2003. LuxS-based signalling in Streptococcus gordonii:: Autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185:274-284.
29. Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Molec Microbiol 30:285-293.
30. Rebbapragada A, Johnson MS, Harding GP, Zuccarelli AJ, Fletcher HM, Zhulin IB, Taylor BL. 1997. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Nat Acad Sci USA 94:10541-10546.
31. Reisner A, Haagensen JAJ, Schembri MA, Zechner EL, Molin S. 2003. Development and maturation of Escherichia coli K-12 biofilms. Molec Microbiol 48:933-946.
32. Ren D, Bedzyk L, Setlow P, Thomas S, Ye RW, Wood TK. 2004. Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance. Biotechnol Bioeng 86:344-364.
33. Ren D, Bedzyk L, Thomas S, Ye RW, Wood TK. 2004. Gene expression in Escherichia coli. Biofilms Appl Microbiol Biotechnol 64:515-524.
34. Ren D, Sims JJ, Wood TK. 2001. Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)- furanone. Environ Microbiol 3:731-736.
35. Ren D, Wood TK. 2004. (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)- furanone reduces corrosion from Desulfotomaculum orientis. Environ Microbiol 6:535-540.
36. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning, a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
37. Schauder S, Shokat K, Surette MG, Bassler BL. 2001. The LuxS-family of bacterial autoinducers: Biosynthesis of a novel quorum-sensing signal molecule. Molec Microbiol 41:463-476.
38. Schembri MA, Kjærgaard K, Klemm P. 2003. Global gene expression in Escherichia coli. Biofilms Molec Microbiol 48:253-267.
39. Shoemaker DD, Linsley PS. 2002. Recent developments in DNA microarray. Curr Opin Microbiol 5:334-337.
40. Sperandio V, Torres AG, Giron JA, Kaper JB. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 183:5187-5197.
41. Stanley NR, Britton RA, Grossman AD, Lazazzera BA. 2003. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951-1957.
42. Stintzi A, Evans K, Meyer J-M, Poole K. 1998. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/las1 mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166:341-345.
43. Surette MG, Bassler BL. 1998. Quorum sensing in Escherichia coli and Salmonella typhinurium. Proc Natl Acad Sci USA 95:7046-7050.
44. Surette MG, Miller MB, Bassler BL. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A new family of genes responsible for autoinducer production. Proc Natl Acad Sci USA 96:1639-1644.
45. Taga ME, Semmelhack JL, Bassler BL. 2001. The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Molec Microbiol 42:777-793.
46. Taylor BL, Zhulin IB, Johnson MS. 1999. Aerotaxis and other energy-sensing behavior in bacteria. Ann Rev Microbiol 53:103-128.
47. Wei Y, Lee J-M, Richmond C, Blattner FR, Rafalski JA, Larossa RA. 2001. High-density microarray-mediated gene expression profiling of Escherichia coli. J Bacteriol 183:545-556.
48. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teltzel GM, Lory S, Greenberg EP. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860-864.
49. Wilson M, DeRisi J, Kristensen H-H, Imboden P, Rane S, Brown PO, Schoolnik GK. 1999. Exploring drug-induced alterations in gene expression in Mycobacterium tuberculosis by microarray hybridization. Proc Natl Acad Sci USA 96:12833-12838.
50. Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MTG, Linforth R, Cornell KA, Taylor AJ, Hill PJ, Williams P. 2002. LuxS: Its role in central metabolism and the in vitro synthesis of 4-hydoxy-5-methyl-3(2H)-furanone. Microbiology 148:909-922.
51. Xavier KB, Bassler BL. 2003. LuxS quorum sensing: More than just a numbers game. Curr Opin Microbiol 6:191-197.
52. Ye RW, Tao W, Bedzyk L, Young T, Chen M, Li L. 2000. Global gene expression profiles of Bacillus subtilis grown under anaerobic conditions. J Bacteriol 182:4458-4465.
53. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562-4570.