LuxS influences Escherichia coli biofilm formation through autoinducer-2-dependent and autoinducer-2-independent modalities

FEMS Microbiology Ecology

Volumn 83, Issue 3, 2013, Pages 778-791

  Niu, Chen ^a   Robbins, Chandan M ^b   Pittman, Kelly J ^c   Osborn, joDi L ^b   Stubblefield, Bryan A ^b   Simmons, Robert B ^b   Gilbert, Eric S ^b  

^a FUDAN UNIVERSITY   (China)

^b GEORGIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Autoinducer 2; Biofilm; Microbial ecology; Quorum sensing

Indexed keywords

4,5 DIHYDROXY 2,3 PENTANEDIONE; 4,5-DIHYDROXY-2,3-PENTANEDIONE; BACTERIAL PROTEIN; CARBON; DRUG DERIVATIVE; HOMOSERINE; LACTONE; LUXS PROTEIN, BACTERIA; LYASE; N OCTANOYLHOMOSERINE LACTONE; N-OCTANOYLHOMOSERINE LACTONE; PENTANE; URONIC ACID;

ADAPTATION; BIOFILM; BIOMASS; COLONIZATION; FECAL COLIFORM; GENE EXPRESSION; INHIBITION; METHANE; MICROBIAL ECOLOGY; MUTATION; PLASMID;

ARTICLE; BIOFILM; ESCHERICHIA COLI; FIMBRIA; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE;

BACTERIAL PROTEINS; BIOFILMS; CARBON; CARBON-SULFUR LYASES; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; HOMOSERINE; LACTONES; PENTANES; PHENOTYPE; URONIC ACIDS;

ESCHERICHIA COLI;

EID: 84873118421     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12034     Document Type: Article

References (59)

1. Armbruster CE, Hong W, Pang B, Weimer KE, Juneau RA, Turner J & Swords WE (2010) Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. mBio 1: 102-110.
2. Bassler BL, Greenberg EP & Stevens AM (1997) Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol 179: 4043-4045.
3. Blumenkrantz N & Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54: 484-489.
4. Brandl MT, Miller WG et al. (2005) Production of autoinducer 2 in Salmonella enterica serovar Thompson contributes to its fitness in chickens but not on cilantro leaf surfaces. Appl Environ Microbiol 71: 2653-2662.
5. Camilli A & Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311: 1113-1116.
6. Casadesus J & Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70: 830-856.
7. Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M & Shear JB (2010) Probing prokaryotic social behaviors with bacterial "lobster traps". mBio 1: 202-210.
8. Cote JP & Mourez M (2011) Structure-function analysis of the TibA self-associating autotransporter reveals a modular organization. Infect Immun 79: 1826-1832.
9. Danese PN, Pratt LA & Kolter R (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182: 3593-3596.
10. DebRoy C & Maddox CW (2001) Identification of virulence attributes of gastrointestinal Escherichia coli isolates of veterinary significance. Anim Health Res Rev 2: 129-140.
11. DeLisa MP, Wu CF, Wang L, Valdes JJ & Bentley WE (2001) DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183: 5239-5247.
12. Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM & Dekker J (2010) Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1: 254-268.
13. Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling. Contrib Microbiol 16: 18-32.
14. Federle MJ & Bassler BL (2003) Interspecies communication in bacteria. J Clin Invest 112: 1291-1299.
15. Flint HJ, Duncan SH, Scott KP & Louis P (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9: 1101-1111.
16. Gonzalez Barrios AF, Zuo R, Hashimoto Y, Yang L, Bentley WE & Wood TK (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188: 305-316.
17. Greenberg EP, Hastings JW & Ulitzer S (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120: 87-91.
18. Guzman LM, Belin D, Carson MJ & Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
19. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK & Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146 (Pt 10): 2395-2407.
20. Holloway CT, Greene RC & Su CH (1970) Regulation of S-adenosylmethionine synthetase in Escherichia coli. J Bacteriol 104: 734-747.
21. Jones MB, Peterson SN, Benn R, Braisted JC, Jarrahi B, Shatzkes K, Ren D, Wood TK & Blaser MJ (2010) Role of luxS in Bacillus anthracis growth and virulence factor expression. Virulence 1: 72-83.
22. Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jorgensen A, Molin S & Tolker-Nielsen T (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48: 1511-1524.
23. Klemm P, Vejborg RM & Sherlock O (2006) Self-associating autotransporters, SAATs: functional and structural similarities. Int J Med Microbiol 296: 187-195.
24. Li J, Attila C, Wang L, Wood TK, Valdes JJ & Bentley WE (2007) Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189: 6011-6020.
25. Ling H, Kang A, Tan MH, Qi X & Chang MW (2010) The absence of the luxS gene increases swimming motility and flagella synthesis in Escherichia coli K12. Biochem Biophys Res Commun 401: 521-526.
26. Lukas F, Gorenc G & Kopecny J (2008) Detection of possible AI-2-mediated quorum sensing system in commensal intestinal bacteria. Folia Microbiol 53: 221-224.
27. Lyon WR, Madden JC, Levin JC, Stein JL & Caparon MG (2001) Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42: 145-157.
28. Macfarlane S (2008) Microbial biofilm communities in the gastrointestinal tract. J Clin Gastroenterol 42 (suppl 3 Pt 1): S142-S143.
29. Macfarlane S & Dillon JF (2007) Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102: 1187-1196.
30. Merritt J, Qi F, Goodman SD, Anderson MH & Shi W (2003) Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 71: 1972-1979.
31. Miller CH & Duerre JA (1968) S-ribosylhomocysteine cleavage enzyme from Escherichia coli. J Biol Chem 243: 92-97.
32. Mitri S, Xavier JB & Foster KR (2011) Social evolution in multispecies biofilms. P Natl Acad Sci USA 108 (suppl 2): 10839-10846.
33. Moreira CG, Carneiro SM, Nataro JP, Trabulsi LR & Elias WP (2003) Role of type I fimbriae in the aggregative adhesion pattern of enteroaggregative Escherichia coli. FEMS Microbiol Lett 226: 79-85.
34. Niu C & Gilbert ES (2004) Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl Environ Microbiol 70: 6951-6956.
35. O'Connell HA, Kottkamp GS, Eppelbaum JL, Stubblefield BA, Gilbert SE & Gilbert ES (2006) Influences of biofilm structure and antibiotic resistance mechanisms on indirect pathogenicity in a model polymicrobial biofilm. Appl Environ Microbiol 72: 5013-5019.
36. Ottoa K, Elwingb H & Hermansson M (1999) The role of type 1 fimbriae in adhesion of Escherichia coli to hydrophilic and hydrophobic surfaces. Colloids Surf B Biointerfaces 15: 99-111.
37. Pittman KJ, Robbins CM, Osborn JL, Stubblefield BA & Gilbert ES (2010) Agarose stabilization of fragile biofilms for quantitative structure analysis. J Microbiol Methods 81: 101-107.
38. 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.
39. Prouty AM, Schwesinger WH & Gunn JS (2002) Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 70: 2640-2649.
40. Qin J, Li R, Raes J et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
41. 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.
42. Rezzonico F & Duffy B (2008) Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8: 154.
43. Rezzonico F, Smits TH & Duffy B (2012) Detection of AI-2 receptors in genomes of Enterobacteriaceae suggests a role of type-2 quorum sensing in closed ecosystems. Sensors (Basel) 12: 6645-6665.
44. Robinson CJ, Bohannan BJ & Young VB (2010) From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74: 453-476.
45. Schauder S, Shokat K, Surette MG & Bassler BL (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41: 463-476.
46. Schembri MA, Christiansen G & Klemm P (2001) FimH-mediated autoaggregation of Escherichia coli. Mol Microbiol 41: 1419-1430.
47. Sperandio V, Torres AG, Jarvis B, Nataro JP & Kaper JB (2003) Bacteria-host communication: the language of hormones. P Natl Acad Sci USA 100: 8951-8956.
48. Srikhanta YN, Dowideit SJ, Edwards JL et al. (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog 5: e1000400.
49. Tenaillon O, Skurnik D, Picard B & Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8: 207-217.
50. van der Woude MW & Henderson IR (2008) Regulation and function of Ag43 (flu). Annu Rev Microbiol 62: 153-169.
51. Vendeville A, Winzer K, Heurlier K, Tang CM & Hardie KR (2005) Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3: 383-396.
52. Vidal JE, Ludewick HP, Kunkel RM, Zahner D & Klugman KP (2011) The LuxS-dependent quorum sensing system regulates early biofilm formation by Streptococcus pneumoniae strain D39. Infect Immun 79: 4050-4060.
53. Walters M, Sircili MP & Sperandio V (2006) AI-3 synthesis is not dependent on luxS in Escherichia coli. J Bacteriol 188: 5668-5681.
54. Wang L, Hashimoto Y, Tsao CY, Valdes JJ & Bentley WE (2005a) Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J Bacteriol 187: 2066-2076.
55. Wang L, Li J, March JC, Valdes JJ & Bentley WE (2005b) luxS-dependent gene regulation in Escherichia coli K-12 revealed by genomic expression profiling. J Bacteriol 187: 8350-8360.
56. Winzer K, Hardie KR, Burgess N et al. (2002) LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909-922.
57. Xavier KB & Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187: 238-248.
58. Xavier KB, Miller ST, Lu W, Kim JH, Rabinowitz J, Pelczer I, Semmelhack MF & Bassler BL (2007) Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria. ACS Chem Biol 2: 128-136.
59. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL & Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. P Natl Acad Sci USA 99: 3129-3134.