A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator

Molecular Microbiology

Volumn 87, Issue 1, 2013, Pages 1-13

  Ramsay, Joshua P ^a   Major, Anthony S ^a   Komarovsky, Victor M ^a   Sullivan, John T ^a   Dy, Ron L ^a   Hynes, Michael F ^b   Salmond, George P C ^c   Ronson, Clive W ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; N ACYLHOMOSERINE LACTONE; PROTEIN QSEC; PROTEIN QSEM; PROTEIN TRAR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; GENE CASSETTE; GENE EXPRESSION; GENE MUTATION; GENE TRANSFER; GENETIC TRANSCRIPTION; GENOMIC ISLAND; MESORHIZOBIUM; MESORHIZOBIUM LOTI; NONHUMAN; OPERATOR GENE; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QSEC GENE; QSEM GENE; QUORUM SENSING; SYMBIOSIS; TRAR GENE;

4-BUTYROLACTONE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CONJUGATION, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; HOMOSERINE; LOTUS; MESORHIZOBIUM; NITROGEN FIXATION; PLASMIDS; PROMOTER REGIONS, GENETIC; QUORUM SENSING; RNA, MESSENGER; SYMBIOSIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS); MESORHIZOBIUM LOTI;

EID: 84871409152     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12079     Document Type: Article

References (50)

1. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., etal. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
2. Ball, N.J., McGeehan, J.E., Streeter, S.D., Thresh, S.J., and Kneale, G.G. (2012) The structural basis of differential DNA sequence recognition by restriction-modification controller proteins. Nucleic Acids Res. doi: 10.1093/nar/gks718.
3. Bogdanova, E., Djordjevic, M., Papapanagiotou, I., Heyduk, T., Kneale, G., and Severinov, K. (2008) Transcription regulation of the type II restriction-modification system AhdI. Nucleic Acids Res 36: 1429-1442.
4. Burrus, V., Pavlovic, G., Decaris, B., and Guedon, G. (2002) Conjugative transposons: the tip of the iceberg. Mol Microbiol 46: 601-610.
5. Coulthurst, S.J., Williamson, N.R., Harris, A.K., Spring, D.R., and Salmond, G.P. (2006) Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology 152: 1899-1911.
6. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
7. Danino, V.E., Wilkinson, A., Edwards, A., and Downie, J.A. (2003) Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Microbiol 50: 511-525.
8. Demarre, G., Guerout, A.M., Matsumoto-Mashimo, C., Rowe-Magnus, D.A., Marliere, P., and Mazel, D. (2005) A new family of mobilizable suicide plasmids based on broad host range R388 plasmid (IncW) and RP4 plasmid (IncPalpha) conjugative machineries and their cognate Escherichia coli host strains. Res Microbiol 156: 245-255.
9. Dobrindt, U., Chowdary, M.G., Krumbholz, G., and Hacker, J. (2010) Genome dynamics and its impact on evolution of Escherichia coli. Med Microbiol Immunol 199: 145-154.
10. Erler, I., Hirnet, D., Wissenbach, U., Flockerzi, V., and Niemeyer, B.A. (2004) Ca2+-selective transient receptor potential V channel architecture and function require a specific ankyrin repeat. J Biol Chem 279: 34456-34463.
11. Fuqua, C., Burbea, M., and Winans, S.C. (1995) Activity of the Agrobacterium Ti plasmid conjugal transfer regulator TraR is inhibited by the product of the traM gene. J Bacteriol 177: 1367-1373.
12. Goldenfeld, N., and Woese, C. (2007) Biology's next revolution. Nature 445: 369.
13. Goryachev, A.B. (2011) Understanding bacterial cell-cell communication with computational modeling. Chem Rev 111: 238-250.
14. Goryachev, A.B., Toh, D.J., Wee, K.B., Lee, T., Zhang, H.B., and Zhang, L.H. (2005) Transition to quorum sensing in an Agrobacterium population: a stochastic model. PLoS Comput Biol 1: e37.
15. Grohmann, E. (2010) Autonomous plasmid-like replication of Bacillus ICEBs1: a general feature of integrative conjugative elements? Mol Microbiol 75: 261-263.
16. Guglielmini, J., Quintais, L., Garcillan-Barcia, M.P., Cruz, F., and Rocha, E.P. (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222.
17. Huson, D.H., Richter, D.C., Rausch, C., Dezulian, T., Franz, M., and Rupp, R. (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460.
18. Hwang, I., Cook, D.M., and Farrand, S.K. (1995) A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. J Bacteriol 177: 449-458.
19. Hwang, I., Smyth, A.J., Luo, Z.Q., and Farrand, S.K. (1999) Modulating quorum sensing by antiactivation: TraM interacts with TraR to inhibit activation of Ti plasmid conjugal transfer genes. Mol Microbiol 34: 282-294.
20. Juhas, M., van der Meer, J.R., Gaillard, M., Harding, R.M., Hood, D.W., and Crook, D.W. (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33: 376-393.
21. Khan, S.R., Gaines, J., Roop, R.M., 2nd, and Farrand, S.K. (2008) Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl Environ Microbiol 74: 5053-5062.
22. Knowle, D., Lintner, R.E., Touma, Y.M., and Blumenthal, R.M. (2005) Nature of the promoter activated by C.PvuII, an unusual regulatory protein conserved among restriction-modification systems. J Bacteriol 187: 488-497.
23. Lerat, E., and Moran, N.A. (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21: 903-913.
24. Luo, Z.Q., Qin, Y., and Farrand, S.K. (2000) The antiactivator TraM interferes with the autoinducer-dependent binding of TraR to DNA by interacting with the C-terminal region of the quorum-sensing activator. J Biol Chem 275: 7713-7722.
25. McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Camara, M., etal. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143: 3703-3711.
26. McGeehan, J.E., Papapanagiotou, I., Streeter, S.D., and Kneale, G.G. (2006) Cooperative binding of the C.AhdI controller protein to the C/R promoter and its role in endonuclease gene expression. J Mol Biol 358: 523-531.
27. McGeehan, J.E., Streeter, S.D., Thresh, S.J., Ball, N., Ravelli, R.B., and Kneale, G.G. (2008) Structural analysis of the genetic switch that regulates the expression of restriction-modification genes. Nucleic Acids Res 36: 4778-4787.
28. McGeehan, J.E., Ball, N.J., Streeter, S.D., Thresh, S.J., and Kneale, G.G. (2012) Recognition of dual symmetry by the controller protein C.Esp1396I based on the structure of the transcriptional activation complex. Nucleic Acids Res 40: 4158-4167.
29. MacLellan, S.R., MacLean, A.M., and Finan, T.M. (2006) Promoter prediction in the rhizobia. Microbiology 152: 1751-1763.
30. Malott, R.J., Baldwin, A., Mahenthiralingam, E., and Sokol, P.A. (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73: 4982-4992.
31. Mruk, I., Rajesh, P., and Blumenthal, R.M. (2007) Regulatory circuit based on autogenous activation-repression: roles of C-boxes and spacer sequences in control of the PvuII restriction-modification system. Nucleic Acids Res 35: 6935-6952.
32. Nakayama, Y., and Kobayashi, I. (1998) Restriction-modification gene complexes as selfish gene entities: roles of a regulatory system in their establishment, maintenance, and apoptotic mutual exclusion. Proc Natl Acad Sci USA 95: 6442-6447.
33. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
34. Qin, Y., Su, S., and Farrand, S.K. (2007) Molecular basis of transcriptional antiactivation. TraM disrupts the TraR-DNA complex through stepwise interactions. J Biol Chem 282: 19979-19991.
35. Ramsay, J.P., Sullivan, J.T., Stuart, G.S., Lamont, I.L., and Ronson, C.W. (2006) Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62: 723-734.
36. Ramsay, J.P., Sullivan, J.T., Jambari, N., Ortori, C.A., Heeb, S., Williams, P., etal. (2009) A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73: 1141-1155.
37. Ramsay, J.P., Williamson, N.R., Spring, D.R., and Salmond, G.P. (2011) A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium. Proc Natl Acad Sci USA 108: 14932-14937.
38. Ronson, C.W., Nixon, B.T., Albright, L.M., and Ausubel, F.M. (1987) Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions. J Bacteriol 169: 2424-2431.
39. Scornavacca, C., Zickmann, F., and Huson, D.H. (2011) Tanglegrams for rooted phylogenetic trees and networks. Bioinformatics 27: i248-i256.
40. Seet, Q., and Zhang, L.H. (2011) Anti-activator QslA defines the quorum sensing threshold and response in Pseudomonas aeruginosa. Mol Microbiol 80: 951-965.
41. Siehnel, R., Traxler, B., An, D.D., Parsek, M.R., Schaefer, A.L., and Singh, P.K. (2010) A unique regulator controls the activation threshold of quorum-regulated genes in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 107: 7916-7921.
42. Simon, R., Priefer, U., and Puhler, A. (1983) A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1: 784-790.
43. Sorokin, V., Severinov, K., and Gelfand, M.S. (2009) Systematic prediction of control proteins and their DNA binding sites. Nucleic Acids Res 37: 441-451.
44. Sullivan, J.T., and Ronson, C.W. (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95: 5145-5149.
45. Sullivan, J.T., Patrick, H.N., Lowther, W.L., Scott, D.B., and Ronson, C.W. (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92: 8985-8989.
46. Sullivan, J.T., Trzebiatowski, J.R., Cruickshank, R.W., Gouzy, J., Brown, S.D., Elliot, R.M., etal. (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184: 3086-3095.
47. Toussaint, A., Merlin, C., Monchy, S., Benotmane, M.A., Leplae, R., Mergeay, M., and Springael, D. (2003) The biphenyl- and 4-chlorobiphenyl-catabolic transposon Tn4371, a member of a new family of genomic islands related to IncP and Ti plasmids. Appl Environ Microbiol 69: 4837-4845.
48. Venturi, V., Rampioni, G., Pongor, S., and Leoni, L. (2011) The virtue of temperance: built-in negative regulators of quorum sensing in Pseudomonas. Mol Microbiol 82: 1060-1070.
49. Wozniak, R.A., and Waldor, M.K. (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8: 552-563.
50. Xia, X., and Xie, Z. (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92: 371-373.