Rhamnolipids mediate an interspecies biofilm dispersal signaling pathway

ACS Chemical Biology

Volumn 11, Issue 11, 2016, Pages 3068-3076

  Bhattacharjee, Arunima ^a   Nusca, Tyler D ^a   Hochbaum, Allon I ^a,b  

^a University of California at Irvine   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSURFACTANT; LIPOPOLYSACCHARIDE; N (3 OXODODECANOYL)HOMOSERINE LACTONE; N ACYLHOMOSERINE LACTONE; RHAMNOLIPID; GLYCOLIPID;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CULTURE; BIOFILM; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; TARGET CELL; DRUG EFFECTS; METABOLISM; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

BIOFILMS; ESCHERICHIA COLI; GLYCOLIPIDS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84996619200     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00750     Document Type: Article

References (39)

1. Kostakioti, M., Hadjifrangiskou, M., and Hultgren, S. J. (2013) Bacterial Biofilms: Development, Dispersal, and Therapeutic Strategies in the Dawn of the Postantibiotic Era Cold Spring Harbor Perspect. Med. 3, a010306 10.1101/cshperspect.a010306
2. Kaplan, J. B. (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses J. Dent. Res. 89, 205-218 10.1177/0022034509359403
3. Stewart, P. S. and Franklin, M. J. (2008) Physiological heterogeneity in biofilms Nat. Rev. Microbiol. 6, 199-210 10.1038/nrmicro1838
4. Oppenheimer-Shaanan, Y., Steinberg, N., and Kolodkin-Gal, I. (2013) Small molecules are natural triggers for the disassembly of biofilms Trends Microbiol. 21, 594-601 10.1016/j.tim.2013.08.005
5. Rowe, M. C., Withers, H. L., and Swift, S. (2010) Uropathogenic Escherichia coli forms biofilm aggregates under iron restriction that disperse upon the supply of iron FEMS Microbiol. Lett. 307, 102-109 10.1111/j.1574-6968.2010.01968.x
6. Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A. H., Davies, D. G., and Gilbert, P. (2004) Characterization of Nutrient-Induced Dispersion in Pseudomonas aeruginosa PAO1 Biofilm J. Bacteriol. 186, 7312-7326 10.1128/JB.186.21.7312-7326.2004
7. Karatan, E. and Watnick, P. (2009) Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms Microbiol. Mol. Biol. Rev. MMBR 73, 310-347 10.1128/MMBR.00041-08
8. Boles, B. R. and Horswill, A. R. (2008) agr-Mediated Dispersal of Staphylococcus aureus Biofilms PLoS Pathog. 4, e1000052 10.1371/journal.ppat.1000052
9. Davies, D. G. and Marques, C. N. H. (2009) A Fatty Acid Messenger Is Responsible for Inducing Dispersion in Microbial Biofilms J. Bacteriol. 191, 1393-1403 10.1128/JB.01214-08
10. Marques, C. N. H., Morozov, A., Planzos, P., and Zelaya, H. M. (2014) The Fatty Acid Signaling Molecule cis-2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State Appl. Environ. Microbiol. 80, 6976-6991 10.1128/AEM.01576-14
11. Solano, C., Echeverz, M., and Lasa, I. (2014) Biofilm dispersion and quorum sensing Curr. Opin. Microbiol. 18, 96-104 10.1016/j.mib.2014.02.008
12. Irie, Y., O'Toole, G. A., and Yuk, M. H. (2005) Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms FEMS Microbiol. Lett. 250, 237-243 10.1016/j.femsle.2005.07.012
13. Mireles, J. R., Toguchi, A., and Harshey, R. M. (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation J. Bacteriol. 183, 5848-5854 10.1128/JB.183.20.5848-5854.2001
14. Dean, S. N., Chung, M.-C., and van Hoek, M. L. (2015) Burkholderia Diffusible Signal Factor Signals to Francisella novicida To Disperse Biofilm and Increase Siderophore Production Appl. Environ. Microbiol. 81, 7057-7066 10.1128/AEM.02165-15
15. Boyd, A. and Chakrabarty, A. M. (1994) Role of alginate lyase in cell detachment of Pseudomonas aeruginosa Appl. Environ. Microbiol. 60, 2355-2359
16. Kaplan, J. B., Ragunath, C., Ramasubbu, N., and Fine, D. H. (2003) Detachment of Actinobacillus actinomycetemcomitans Biofilm Cells by an Endogenous β-Hexosaminidase Activity J. Bacteriol. 185, 4693-4698 10.1128/JB.185.16.4693-4698.2003
17. Purevdorj-Gage, B., Costerton, W. J., and Stoodley, P. (2005) Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms Microbiology 151, 1569-1576 10.1099/mic.0.27536-0
18. Dong, Y.-H., Zhang, X.-F., An, S.-W., Xu, J.-L., and Zhang, L.-H. (2008) A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa Commun. Integr. Biol. 1, 88-96 10.4161/cib.1.1.6717
19. Barraud, N., Hassett, D. J., Hwang, S.-H., Rice, S. A., Kjelleberg, S., and Webb, J. S. (2006) Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa J. Bacteriol. 188, 7344-7353 10.1128/JB.00779-06
20. Ma, Q., Zhang, G., and Wood, T. K. (2011) Escherichia coli BdcA controls biofilm dispersal in Pseudomonas aeruginosa and Rhizobium meliloti BMC Res. Notes 4, 447 10.1186/1756-0500-4-447
21. Medina, G., Juárez, K., Valderrama, B., and Soberón-Chávez, G. (2003) Mechanism of Pseudomonas aeruginosa RhlR Transcriptional Regulation of the rhlAB Promoter J. Bacteriol. 185, 5976-5983 10.1128/JB.185.20.5976-5983.2003
22. Lequette, Y. and Greenberg, E. P. (2005) Timing and Localization of Rhamnolipid Synthesis Gene Expression in Pseudomonas aeruginosa Biofilms J. Bacteriol. 187, 37-44 10.1128/JB.187.1.37-44.2005
23. Reis, R. S., Pereira, A. G., Neves, B. C., and Freire, D. M. G. (2011) Gene regulation of rhamnolipid production in Pseudomonas aeruginosa-A review Bioresour. Technol. 102, 6377-6384 10.1016/j.biortech.2011.03.074
24. Haba, E., Abalos, A., Jáuregui, O., Espuny, M. J., and Manresa, A. (2003) Use of liquid chromatography-mass spectroscopy for studying the composition and properties of rhamnolipids produced by different strains of Pseudomonas aeruginosa J. Surfactants Deterg. 6, 155-161 10.1007/s11743-003-0260-7
25. Caiazza, N. C., Shanks, R. M. Q., and O'Toole, G. A. (2005) Rhamnolipids Modulate Swarming Motility Patterns of Pseudomonas aeruginosa J. Bacteriol. 187, 7351-7361 10.1128/JB.187.21.7351-7361.2005
26. Davey, M. E., Caiazza, N. C., and O'Toole, G. A. (2003) Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1 J. Bacteriol. 185, 1027-1036 10.1128/JB.185.3.1027-1036.2003
27. Boles, B. R., Thoendel, M., and Singh, P. K. (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms Mol. Microbiol. 57, 1210-1223 10.1111/j.1365-2958.2005.04743.x
28. Abdel-Mawgoud, A. M., Lépine, F., and Déziel, E. (2010) Rhamnolipids: diversity of structures, microbial origins and roles Appl. Microbiol. Biotechnol. 86, 1323-1336 10.1007/s00253-010-2498-2
29. Lee, C. H. and Tsai, C. M. (1999) Quantification of bacterial lipopolysaccharides by the purpald assay: measuring formaldehyde generated from 2-keto-3-deoxyoctonate and heptose at the inner core by periodate oxidation Anal. Biochem. 267, 161-168 10.1006/abio.1998.2961
30. Al-Tahhan, R. A., Sandrin, T. R., Bodour, A. A., and Maier, R. M. (2000) Rhamnolipid-Induced Removal of Lipopolysaccharide from Pseudomonas aeruginosa: Effect on Cell Surface Properties and Interaction with Hydrophobic Substrates Appl. Environ. Microbiol. 66, 3262-3268 10.1128/AEM.66.8.3262-3268.2000
31. Kim, S.-K. and Lee, J.-H. (2016) Biofilm dispersion in Pseudomonas aeruginosa J. Microbiol. 54, 71-85 10.1007/s12275-016-5528-7
32. Lee, J., Jayaraman, A., and Wood, T. K. (2007) Indole is an inter-species biofilm signal mediated by SdiA BMC Microbiol. 7, 42 10.1186/1471-2180-7-42
33. Pearson, J. P., Pesci, E. C., and Iglewski, B. H. (1997) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes J. Bacteriol. 179, 5756-5767
34. Gao, X., Mukherjee, S., Matthews, P. M., Hammad, L. A., Kearns, D. B., and Dann, C. E. (2013) Functional Characterization of Core Components of the Bacillus subtilis Cyclic-Di-GMP Signaling Pathway J. Bacteriol. 195, 4782-4792 10.1128/JB.00373-13
35. Koestler, B. J. and Waters, C. M. (2013) Exploring Environmental Control of Cyclic di-GMP Signaling in Vibrio cholerae by Using the Ex Vivo Lysate Cyclic di-GMP Assay (TELCA) Appl. Environ. Microbiol. 79, 5233-5241 10.1128/AEM.01596-13
36. Römling, U., Galperin, M. Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger Microbiol. Mol. Biol. Rev. MMBR 77, 1-52 10.1128/MMBR.00043-12
37. Simm, R., Morr, M., Kader, A., Nimtz, M., and Römling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility Mol. Microbiol. 53, 1123-1134 10.1111/j.1365-2958.2004.04206.x
38. Hengge, R., Galperin, M. Y., Ghigo, J.-M., Gomelsky, M., Green, J., Hughes, K. T., Jenal, U., and Landini, P. (2016) Systematic nomenclature for GGDEF and EAL domain-containing c-di-GMP turnover proteins of Escherichia coli J. Bacteriol. 198, 7 10.1128/JB.00424-15
39. Kuchma, S. L., Ballok, A. E., Merritt, J. H., Hammond, J. H., Lu, W., Rabinowitz, J. D., and O'Toole, G. A. (2010) Cyclic-di-GMP-Mediated Repression of Swarming Motility by Pseudomonas aeruginosa: the pilY1 Gene and Its Impact on Surface-Associated Behaviors J. Bacteriol. 192, 2950-2964 10.1128/JB.01642-09