A complex LuxR-LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation

Molecular Microbiology

Volumn 85, Issue 5, 2012, Pages 916-933

  Zan, Jindong ^a,d   Cicirelli, Elisha M ^b,d,e   Mohamed, Naglaa M ^a   Sibhatu, Hiruy ^c,f   Kroll, Stephanie ^b,g   Choi, Ohkee ^b   Uhlson, Charis L ^c   Wysoczinski, Christina L ^c   Murphy, Robert C ^c   Churchill, Mair E A ^c   Hill, Russell T ^a   Fuqua, Clay ^b  

^a UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d Bio Amber Inc   (United States)

^e University of California San Diego   (United States)

^f Cayman Chemical Company   (United States)

^g Gyeongsang National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

3 OXO N ACYLHOMOSERINE LACTONE; BACTERIAL PROTEIN; LUXI PROTEIN; N ACYLHOMOSERINE LACTONE; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ACCLIMATIZATION; ANIMAL TISSUE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BIOFILM; BIOSENSOR; CELL MOTILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ANALYSIS; LUXI GENE; LUXR GENE; MARINE BACTERIUM; MYCALE LAXISSIMA; NONHUMAN; PRIORITY JOURNAL; RUEGERIA; SIGNAL TRANSDUCTION; SPONGE (PORIFERA); SSAI GENE; SSAR GENE; SSARI GENE; SSBL GENE; SSBR GENE; SSBRI GENE; SSCL GENE; SYMBIONT; WILD TYPE;

4-BUTYROLACTONE; ANIMALS; BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; PORIFERA; QUORUM SENSING; ROSEOBACTER; SIGNAL TRANSDUCTION;

MYCALE; ROSEOBACTER; RUEGERIA; SILICIBACTER;

EID: 84865555256     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08149.x     Document Type: Article

References (74)

1. Ahlgren, N.A., Harwood, C.S., Schaefer, A.L., Giraud, E., and Greenberg, E.P. (2011) Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci USA 108: 17183-17188.
2. Akakura, R., and Winans, S.C. (2002) Mutations in the occQ operator that decrease OccR-induced DNA bending do not cause constitutive promoter activity. J Biol Chem 277: 15883-15780.
3. Atkinson, S., Chang, C.Y., Patrick, H.L., Buckley, C.M.F., Wang, Y., Sockett, R.E., etal. (2008) Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA. Mol Microbiol 69: 137-151.
4. Beck von Bodman, S., and Farrand, S.K. (1995) Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J Bacteriol 177: 5000-5008.
5. Belas, R., Horikawa, E., Aizawa, S., and Suvanasuthi, R. (2009) Genetic determinants of Silicibacter sp. TM1040 motility. J Bacteriol 191: 4502-4512.
6. Bligh, E.G., and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
7. Buchan, A., Gonzalez, J.M., and Moran, M.A. (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71: 5665-5677.
8. Churchill, M.E.A., and Chen, L.L. (2011) Structural basis of acyl-homoserine lactone-dependent signaling. ACS Chem Rev 111: 68-85.
9. Cicirelli, E.M., Williamson, H., Tait, K., and Fuqua, C. (2008) Acylated homoserine lactone signaling in marine bacterial systems. In Chemical Communication Among Bacteria. Winans, S.C., and Bassler, B.L. (eds). Washington, DC: ASM Press, pp. 251-272.
10. Clay, K.L., and Murphy, R.C. (1979) New procedure for isolation of amino acids based on selective hydrolysis of trimethylsilyl derivatives. J Chromatogr 164: 417-426.
11. Daniels, R., Vanderleyden, J., and Michiels, J. (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28: 261-289.
12. Davey, M.E., Caiazza, N.C., and O'Toole, G.A. (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PA01. J Bacteriol 185: 1027-1036.
13. Davies, D.G., Parsek, M.R., Pearson, J.R., Iglewski, B.H., Costerton, J.W., and Greenberg, E.P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295-298.
14. Devine, J.H., Shadel, G.S., and Baldwin, T.O. (1989) Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. Proc Natl Acad Sci USA 86: 5688-5692.
15. Eberl, L., Winson, M.K., Sternberg, C., Stewart, G.S.A.B., Christiansen, G., Chhabra, S.R., etal. (1996) Involvement of N-acyl-L-homoserine lactone autoinducers in control of multicellular behavior of Serratia liquefaciens. Mol Microbiol 20: 127-136.
16. Egland, K.A., and Greenberg, E.P. (1999) Quorum sensing in Vibrio fischeri: elements of the luxI promoter. Mol Microbiol 31: 1197-1204.
17. Enticknap, J.J., Kelly, M., Peraud, O., and Hill, R.T. (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72: 3724-3732.
18. Fenchel, T. (2001) Eppur si muove: many water column bacteria are motile. Aquat Microbial Ecol 24: 197-201.
19. Fuqua, C. (2006) The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J Bacteriol 188: 3169-3171.
20. Fuqua, C., and Greenberg, E.P. (2002) Listening in on bacteria: acylhomoserine lactone signalling. Nat Rev Mol Cell Biol 3: 685-695.
21. Gould, T.A., Schweizer, H.P., and Churchill, M.E.A. (2004) Structure of the Pseudomonas aeruginosa acyl-homoserinelactone synthase LasI. Mol Microbiol 53: 1135-1146.
22. Gould, T.A., Herman, J., Krank, J., Murphy, R.C., and Churchill, M.E.A. (2006) Specificity of acyl-homoserine lactone synthases examined by mass spectrometry. J Bacteriol 188: 773-783.
23. Gram, L., Grossart, H.P., Schlingloff, A., and Kiorboe, T. (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68: 4111-4116.
24. Hammer, B.K., and Bassler, B.L. (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50: 101-114.
25. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
26. Hentschel, U., Usher, K.M., and Taylor, M.W. (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167-177.
27. Hibbing, M.E., and Fuqua, C. (2011) Antiparallel and interlinked control of cellular iron levels by the Irr and RirA regulators of Agrobacterium tumefaciens. J Bacteriol 193: 3461-3472.
28. Honag, H.H., Gurich, N., and González, J.E. (2008) Regulation of motility by the ExpR/Sin quorum - sensing system in Sinorhizobium meliloti. J Bacteriol 190: 861-871.
29. Kalogeraki, V.S., and Winans, S.C. (1997) Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188: 69-75.
30. Kim, J., Kang, Y., Choi, O., Jeong, Y., Jeong, J.E., Lim, J.Y., etal. (2007) Regulation of polar flagellum genes is mediated by quorum sensing and FlhDC in Burkholderia glumae. Mol Microbiol 64: 165-179.
31. Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, II, R.M., and Peterson, K.M. (1995) Four new derivatives of the broad host range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Genes Dev 166: 175-176.
32. Krasteva, P.V., Fong, J.C.N., Shikuma, N.J., Beyhan, S., Navarro, M.V.A.S., Yildiz, F.H., and Sondermann, H. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
33. Lequette, Y., Lee, J.H., Ledgham, F., Lazdunski, A., and Greenberg, E.P. (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum sensing circuit. J Bacteriol 183: 6454-6465.
34. Maclouf, J., Grassi, J., and Pradelles, P. (1987) Development of enzyme-immunoassay techniques for the measurement of eicosanoids. In Prostaglandin and Lipid Metabolism in Radiation Injury. Walden, T.L.J., and Hughes, H.N. (eds). Rockville, MD: Plenum Press, pp. 355-364.
35. Macnab, R.M. (1996) Flagella and motility. In Escherichia coli and Salmonella Typhimurium: Cellular and Moelcular Biology. Neidhart, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., etal. (eds). Washington, DC: ASM press, pp. 123-145.
36. Mayfield, C.I., and Inniss, W.E. (1977) Rapid, simple method for staining bacterial flagella. Can J Microbiol 23: 1311-1313.
37. Merritt, P.M., Danhorn, T., and Fuqua, C. (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189: 8005-8014.
38. Mersereau, M., Pazour, G.J., and Das, A. (1990) Efficient transformation of Agrobacterium tumefaciens by electroporation. Gene 90: 149-151.
39. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
40. Miller, T.R., and Belas, R. (2006) Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environ Microbiol 8: 1648-1659.
41. Minogue, T.D., Wehland-von Trebra, M., Bernhard, F., and Beck von Bodman, S. (2002) The autoregulatory role of EsaR, a quorum sensing regulator in Pantoea stewartii subsp. stewartii: evidence for a repressor function. Mol Microbiol 44: 1625-1635.
42. Mohamed, N.M., Rao, V., Hamann, M.T., Kelly, M., and Hill, R.T. (2008a) Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microbiol 74: 4133-4143.
43. Mohamed, N.M., Cicirelli, E.M., Kan, J., Chen, F., Fuqua, C., and Hill, R.T. (2008b) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10: 75-86.
44. Moran, M.A., Buchan, A., González, J.M., Heidelberg, J.F., Whitman, W.B., and Kiene, R.P. (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432: 910-913.
45. Muir, R.E., and Gober, J.W. (2004) Regulation of FlbD activity by flagellum assembly is accomplished through direct interaction with the trans-acting factor, FliX. Mol Microbiol 54: 715-730.
46. Ng, W.L., and Bassler, B.L. (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
47. O'Toole, G.A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
48. Pellock, B.J., Teplitski, M., Boinay, R.P., Bauer, W.D., and Walker, G.C. (2002) A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J Bacteriol 184: 5067-5076.
49. Pesci, E.C., Pearson, J.P., Seed, P.C., and Iglewski, B.H. (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179: 3127-3132.
50. Puskas, A., Greenberg, E.P., Kaplan, S., and Schaefer, A.L. (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J Bacteriol 179: 7530-7537.
51. 2. Nature 407: 364-367.
52. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., etal. (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
53. Sambrook, J., Fritsch, E., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
54. Schmitt, S., Angermeier, H., Schiller, R., Lindquist, N., and Hentschel, U. (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74: 7694-7708.
55. Schuster, M., Urbanowski, M.L., and Greenberg, E.P. (2004) Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc Natl Acad Sci USA 101: 15833-15877.
56. Sharp, K.H., Eam, B., Faulkner, D.J., and Haygood, M.G. (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73: 622-629.
57. Shrout, J.D., Chopp, D.L., Just, L.C., Hentzer, M., Givskov, M., and Parsek, M.R. (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62: 1264-1277.
58. Slightom, R.N., and Buchan, A. (2009) Surface colonization by marine Roseobacters: integrating genotypes and phenotypes. Appl Environ Microbiol 75: 6027-6037.
59. Soutourina, O.A., and Bertin, P.N. (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27: 505-523.
60. Taylor, M.W., Schupp, P.J., Baillie, H.J., Charlton, T.S., de Nys, R., Kjelleberg, S.K., and Steinberg, P.D. (2004) Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl Environ Microbiol 70: 4387-4389.
61. Tempé, J., Petit, A., Holsters, M., Van Montagu, M., and Schell, J. (1977) Thermosensitive step associated with transfer of the Ti plasmid during conjugation: possible relation to transformation in crown gall. Proc Natl Acad Sci USA 74: 2848-2849.
62. Tomlinson, A.D., Ramey-Hartung, B., Day, T.W., Merritt, P.M., and Fuqua, C. (2010) Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility. Microbiology 156: 2670-2681.
63. Vacelet, J. (1975) Etude en microscopie electronique de l'association entre bacteries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23: 271-288.
64. Vacelet, J., and Donadey, C. (1977) Electron microscope study of association between some sponges and bacteria. J Exp Mar Biol Ecol 30: 301-314.
65. Wagner-Dobler, I., Thiel, V., Eberl, L., Allgaier, M., Bodor, A., Meyer, S., etal. (2005) Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. Chembiochem 6: 2195-2206.
66. Waters, C.M., Lu, W., Rabinowitz, J.D., and Bassler, B.L. (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of VpsT. J Bacteriol 190: 2527-2536.
67. Watson, W.T., Minogue, T.D., Val, D.L., Beck von Bodman, S., and Churchill, M.E.A. (2002) Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum Sensing. Mol Cell 9: 685-694.
68. Webster, N.S., and Hill, R.T. (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-Proteobacterium. Mar Biol 138: 843-851.
69. Yates, E.A., Philipp, B., Buckey, C., Atkinso, S., Chhabra, S.R., Sockett, R.E., etal. (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.
70. Zan, J., Fuqua, C., and Hill, R.T. (2011a) Diversity and functional analysis of luxS genes in Vibrios from marine sponges Mycale laxissima and Ircinia strobilina. ISME J 5: 1505-1516.
71. Zan, J., Fricke, W.F., Fuqua, C., Ravel, J., and Hill, R. (2011b) Genome sequence of Ruegeria sp. KLH11, a N-acylhomoserine lactone-producing bacterium isolated from the marine sponge Mycale laxissima. J Bacteriol 193: 5011-5012.
72. Zhang, R.G., Pappas, J., Brace, J.L., Miller, P.C., Oulmassov, T., Molyneaux, J.M., etal. (2002) Structure of a bacterial quorum-sensing transcription factor complexed with autoinducer-type pheromone and DNA. Nature 417: 971-974.
73. Zhu, J., Beaber, J.W., More, M.I., Fuqua, C., Eberhard, A., and Winans, S.C. (1998) Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J Bacteriol 180: 5398-5405.
74. Zhu, J., Chai, Y., Zhong, Z., Li, S., and Winans, S.C. (2003) Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl Environ Microbiol 69: 6949-6953.