Production of cell-cell signalling molecules by bacteria isolated from human chronic wounds

Journal of Applied Microbiology

Volumn 108, Issue 5, 2010, Pages 1509-1522

  Rickard, A H ^a   Colacino, K R ^a   Manton, K M ^a   Morton, R I ^a   Pulcini, E ^b   Pfeil, J ^a   Rhoads, D ^c   Wolcott, R D ^c   James, G ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c Wound Care Center   (United States)

Author keywords

Acyl homoserine lactone; Autoinducer 1; Autoinducer 2; Biofilm; Chronic wound; Signal molecules

Indexed keywords

AMINO ACIDS; BATCH CELL CULTURE; CELL SIGNALING; CELLS; ESTERS; MOLECULAR BIOLOGY; RNA;

ACYL-HOMOSERINE-LACTONE; AUTOINDUCER-1; AUTOINDUCER-2; AUTOINDUCERS; CELL-CELL SIGNALING; CHRONIC WOUNDS; DEBRIDEMENT; HOMOSERINE LACTONES; SIGNAL MOLECULES; SIGNALING MOLECULES;

BACTERIA;

N ACYLHOMOSERINE LACTONE; RNA 16S; S RIBOSYLHOMOCYSTEINASE;

BACTERIUM; BIOASSAY; BIOFILM; GENETIC ANALYSIS; IDENTIFICATION METHOD; MICROBIOLOGY; MOLECULAR ANALYSIS; WOUNDING;

ACINETOBACTER; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BIOLUMINESCENCE; DEBRIDEMENT; DISEASE SEVERITY; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PHYLOGENY; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION; WOUND;

ACINETOBACTER; BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SERRATIA MARCESCENS;

EID: 77950657489     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04554.x     Document Type: Article

References (77)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389 3402.
2. Berlau, J., Aucken, H., Malnick, H. Pitt, T. (1999) Distribution of Acinetobacter species on skin of healthy humans. Eur J Clin Microbiol Infect Dis 18, 179 183.
3. Bernier, S.P., Beeston, A.L. Sokol, P.A. (2008) Detection of N-acyl homoserine lactones using a traI-luxCDABE-based biosensor as a high-throughput screening tool. BMC Biotechnol 8, 59.
4. Bielecki, P., Glik, J., Kawecki, M. Martins dos Santos, V.A. (2008) Towards understanding Pseudomonas aeruginosa burn wound infections by profiling gene expression. Biotechnol Lett 30, 777 790.
5. Blehert, D.S., Palmer, R.J. Jr., Xavier, J.B., Almeida, J.S. Kolenbrander, P.E. (2003) Autoinducer 2 production by Streptococcus gordonii DL1 and the biofilm phenotype of a luxS mutant are influenced by nutritional conditions. J Bacteriol 185, 4851 4860.
6. Bowler, P.G. Davies, B.J. (1999) The microbiology of acute and chronic wounds. Wounds 11, 72 78.
7. Brelles-Marino, G. Bedmar, E.J. (2001) Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria. J Biotechnol 91, 197 209.
8. Chambers, C.E., Visser, M.B., Schwab, U. Sokol, P.A. (2005) Identification of N-acylhomoserine lactones in mucopurulent respiratory secretions from cystic fibrosis patients. FEMS Microbiol Lett 244, 297 304.
9. Davies, C.E., Hill, K.E., Wilson, M.J., Stephens, P., Hill, C.M., Harding, K.G. Thomas, D.W. (2004) Use of 16S ribosomal DNA PCR and denaturing gradient gel electrophoresis for analysis of the microfloras of healing and nonhealing chronic venous leg ulcers. J Clin Microbiol 42, 3549 3557.
10. DeKeersmaecker, S.C. Vanderleyden, J. (2003) Constraints on detection of autoinducer-2 (AI-2) signalling molecules using Vibrio harveyi as a reporter. Microbiology 149, 1953 1956.
11. Dekio, I., Hayashi, H., Sakamoto, M., Kitahara, M., Nishikawa, T., Suematsu, M. Benno, Y. (2005) Detection of potentially novel bacterial components of the human skin microbiota using culture-independent molecular profiling. J Med Microbiol 54, 1231 1238.
12. Donlan, R.M. Costerton, J.W. (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15, 167 193.
13. Dow, G., Browne, A. Sibbald, R.G. (1999) Infection in chronic wounds: controversies in diagnosis and treatment. Ostomy Wound Manage 45, 23 27, 29-40; quiz 41-22.
14. Dowd, S.E., Sun, Y., Secor, P.R., Rhoads, D.D., Wolcott, B.M., James, G.A. Wolcott, R.D. (2008a) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8, 43.
15. Dowd, S.E., Wolcott, R.D., Sun, Y., McKeehan, T., Smith, E. Rhoads, D. (2008b) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS ONE 3, e3326.
16. Erickson, D.L., Nsereko, V.L., Morgavi, D.P., Selinger, L.B., Rode, L.M. Beauchemin, K.A. (2002) Evidence of quorum sensing in the rumen ecosystem: detection of N-acyl homoserine lactone autoinducers in ruminal contents. Can J Microbiol 48, 374 378.
17. Frias, J., Olle, E. Alsina, M. (2001) Periodontal pathogens produce quorum sensing signal molecules. Infect Immun 69, 3431 3434.
18. Fux, C.A., Costerton, J.W., Stewart, P.S. Stoodley, P. (2005) Survival strategies of infectious biofilms. Trends Microbiol 13, 34 40.
19. Gao, Z., Tseng, C.H., Pei, Z. Blaser, M.J. (2007) Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci U S A 104, 2927 2932.
20. Gilbert, P., Maira-Litran, T., McBain, A.J., Rickard, A.H. Whyte, F.W. (2002) The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol 46, 202 256.
21. Gjodsbol, K., Christensen, J.J., Karlsmark, T., Jorgensen, B., Klein, B.M. Krogfelt, K.A. (2006) Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 3, 225 231.
22. Gonzalez Barrios, A.F., Zuo, R., Hashimoto, Y., Yang, L., Bentley, W.E. Wood, T.K. (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188, 305 316.
23. Gootz, T.D. Marra, A. (2008) Acinetobacter baumannii: an emerging multidrug-resistant threat. Expert Rev Anti Infect Ther 6, 309 325.
24. Greenberg, E.P., Hasting, J.W. Ulitzur, S. (1979) Induction of luciferase synthesis in Benechkea harveyi by other marine bacteria. Arch Microbiol 120, 87 91.
25. Grice, E.A., Kong, H.H., Renaud, G., Young, A.C., Bouffard, G.G., Blakesley, R.W., Wolfsberg, T.G., Turner, M.L. et al. (2008) A diversity profile of the human skin microbiota. Genome Res 18, 1043 1050.
26. Hardie, K.R. Heurlier, K. (2008) Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development. Nat Rev Microbiol 6, 635 643.
27. Harding, K.G., Morris, H.L. Patel, G.K. (2002) Science, medicine and the future: healing chronic wounds. BMJ 324, 160 163.
28. Hernandez, R. (2006) The use of systemic antibiotics in the treatment of chronic wounds. Dermatol Ther 19, 326 337.
29. Hill, K.E., Davies, C.E., Wilson, M.J., Stephens, P., Harding, K.G. Thomas, D.W. (2003) Molecular analysis of the microflora in chronic venous leg ulceration. J Med Microbiol 52, 365 369.
30. Howell-Jones, R.S., Wilson, M.J., Hill, K.E., Howard, A.J., Price, P.E. Thomas, D.W. (2005) A review of the microbiology, antibiotic usage and resistance in chronic skin wounds. J Antimicrob Chemother 55, 143 149.
31. Irie, Y. Parsek, M.R. (2008) Quorum sensing and microbial biofilms. Curr Top Microbiol Immunol 322, 67 84.
32. James, T.J., Hughes, M.A., Cherry, G.W. Taylor, R.P. (2000) Simple biochemical markers to assess chronic wounds. Wound Repair Regen 8, 264 269.
33. James, G.A., Swogger, E., Wolcott, R., Pulcini, E., Secor, P., Sestrich, J., Costerton, J.W. Stewart, P.S. (2008) Biofilms in chronic wounds. Wound Repair Regen 16, 37 44.
34. Jones, K.R., Fennie, K. Lenihan, A. (2007) Chronic wounds: factors influencing healing within 3 months and nonhealing after 5-6 months of care. Wounds 19, 51 63.
35. Juhas, M., Eberl, L. Tummler, B. (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7, 459 471.
36. Jukes, T.H. Cantor, C.P. (1969) Evolution of protein molecules. In Mammalian Protein Metabolism ed. Munro, H.N. pp. 21 132.
37. Kirketerp-Møller, K., Jensen, P.Ø., Fazli, M., Madsen, K.G., Pedersen, J., Moses, C., Tolker-Nielsen, T., Høiby, N. et al 2008) Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 46, 2717 2722.
38. Lowbury, E.J. (1969) Gram-negative bacilli on the skin. Br J Dermatol 81, 55 61.
39. McClean, K.H., Winson, M.K., Fish, L. et al. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143 (Pt 12 3703 3711.
40. Medina-Martinez, M.S., Uyttendaele, M., Meireman, S. Debevere, J. (2007) Relevance of N-acyl-l-homoserine lactone production by Yersinia enterocolitica in fresh foods. J Appl Microbiol 102, 1150 1158.
41. Middleton, B., Rodgers, H.C., Camara, M., Knox, A.J., Williams, P. Hardman, A. (2002) Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol Lett 207, 1 7. (Pubitemid 34214797)
42. Miller, M.B. Bassler, B.L. (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55, 165 199.
43. Morohoshi, T., Shiono, T., Takidouchi, K., Kato, M., Kato, N., Kato, J. Ikeda, T. (2007) Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone. Appl Environ Microbiol 73, 6339 6344. (Pubitemid 47628680)
44. Mustoe, T.A., O'Shaughnessy, K. Kloeters, O. (2006) Chronic wound pathogenesis and current treatment strategies: a unifying hypothesis. Plast Reconstr Surg 117, 35S 41S. (Pubitemid 44317770)
45. Nakagami, G., Sanada, H., Sugama, J., Morohoshi, T., Ikeda, T. Ohta, Y. (2008) Detection of Pseudomonas aeruginosa quorum sensing signals in an infected ischemic wound: an experimental study in rats. Wound Repair Regen 16, 30 36.
46. Navon-Venezia, S., Ben-Ami, R. Carmeli, Y. (2005) Update on Pseudomonas aeruginosa and Acinetobacter baumannii infections in the healthcare setting. Curr Opin Infect Dis 18, 306 313. (Pubitemid 41017634)
47. Niu, C., Clemmer, K.M., Bonomo, R.A. Rather, P.N. (2008) Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. J Bacteriol 190, 3386 3392. (Pubitemid 351581435)
48. Peleg, A.Y., Seifert, H. Paterson, D.L. (2008) Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 21, 538 582.
49. Pollack, M. (1984) The virulence of Pseudomonas aeruginosa. Rev Infect Dis 6 (Suppl 3 S617 S626.
50. Price, P.B. (1938) The bacteriology of normal skin; a new quantitative test applied to a study of the bacterial flora and the disinfectant action of mechanical cleansing. J Infect Dis 63, 601.
51. Rickard, A.H., Leach, S.A., Hall, L.S., Buswell, C.M., High, N.J. Handley, P.S. (2002) Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Appl Environ Microbiol 68, 3644 3650.
52. Rickard, A.H., Palmer, R.J. Jr., Blehert, D.S., Campagna, S.R., Semmelhack, M.F., Egland, P.G., Bassler, B.L. Kolenbrander, P.E. (2006) Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60, 1446 1456.
53. Roth, R.R. James, W.D. (1988) Microbial ecology of the skin. Annu Rev Microbiol 42, 441 464.
54. Rumbaugh, K.P., Griswold, J.A., Iglewski, B.H. Hamood, A.N. (1999) Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 67, 5854 5862.
55. Ruocco, E., Donnarumma, G., Baroni, A. Tufano, M.A. (2007) Bacterial and viral skin diseases. Dermatol Clin 25, 663 676, xi. (Pubitemid 47446081)
56. Semmelhack, M.F., Campagna, S.R., Federle, M.J. Bassler, B.L. (2005) An expeditious synthesis of DPD and boron binding studies. Org Lett 7, 569 572. (Pubitemid 40353443)
57. Shao, H., James, D., Lamont, R.J. Demuth, D.R. (2007) Differential interaction of Aggregatibacter (Actinobacillus) actinomycetemcomitans LsrB and RbsB proteins with autoinducer 2. J Bacteriol 189, 5559 5565. (Pubitemid 47206401)
58. Sio, C.F., Otten, L.G., Cool, R.H. et al. (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74, 1673 1682.
59. Spormann, A.M. (2008) Physiology of microbes in biofilms. Curr Top Microbiol Immunol 322, 17 36.
60. Stackebrandt, E. Goebel, B.M. (1994) A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846 849. (Pubitemid 24315169)
61. Stickler, D.J., Morris, N.S., McLean, R.J. Fuqua, C. (1998) Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro. Appl Environ Microbiol 64, 3486 3490. (Pubitemid 28411477)
62. Sun, J., Daniel, R., Wagner-Dobler, I. Zeng, A.P. (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4, 36. (Pubitemid 39526776)
63. Surette, M.G. Bassler, B.L. (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 95, 7046 7050.
64. Surette, M.G., Miller, M.B. Bassler, B.L. (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 96, 1639 1644.
65. Taga, M.E. (2007) Bacterial signal destruction. ACS Chem Biol 2, 89 92.
66. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876 4882. (Pubitemid 28022245)
67. Trengove, N.J., Langton, S.R. Stacey, M.C. (1996) Biochemical analysis of wound fluid from nonhealing and healing chronic leg ulcers. Wound Repair Regen 4, 234 239.
68. Van de Peer, Y. De Wachter, R. (1993) TREECON: a software package for the construction and drawing of evolutionary trees. Comput Appl Biosci 9, 177 182. (Pubitemid 23127140)
69. Van Houdt, R., Givskov, M. Michiels, C.W. (2007) Quorum sensing in Serratia. FEMS Microbiol Rev 31, 407 424. (Pubitemid 46920249)
70. Weisburg, W.G., Barns, S.M., Pelletier, D.A. Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697 703.
71. Williams, P. (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153, 3923 3938.
72. Wilson, K.H., Blitchington, R.B. Greene, R.C. (1990) Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction. J Clin Microbiol 28, 1942 1946.
73. Wolcott, R.D., Rhoads, D.D. Dowd, S.E. (2008) Biofilms and chronic wound inflammation. J Wound Care 17, 333 341.
74. Xavier, K.B. Bassler, B.L. (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187, 238 248.
75. Yang, F., Wang, L.H., Wang, J., Dong, Y.H., Hu, J.Y. Zhang, L.H. (2005) Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett 579, 3713 3717.
76. Yates, E.A., Philipp, B., Buckley, C. et al. (2002) N-acylhomoserine lactones 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.
77. Yoshida, A., Ansai, T., Takehara, T. Kuramitsu, H.K. (2005) LuxS-based signaling affects Streptococcus mutans biofilm formation. Appl Environ Microbiol 71, 2372 2380.