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

Molecular Microbiology

Volumn 73, Issue 6, 2009, Pages 1141-1155

  Ramsay, Joshua P ^a,c   Sullivan, John T ^a   Jambari, Nuzul ^a   Ortori, Catharine A ^b   Heeb, Stephan ^b   Williams, Paul ^b   Barrett, David A ^b   Lamont, Lain L ^a   Ronson, Clive W ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LUXR; TRANSCRIPTION FACTOR TRAL1; TRANSCRIPTION FACTOR TRAL2; UNCLASSIFIED DRUG;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL STRAIN; GENE EXPRESSION; GENE TRANSFER; MESORHIZOBIUM; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS;

4-BUTYROLACTONE; ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; BASE SEQUENCE; CONJUGATION, GENETIC; DNA, BACTERIAL; GENE EXPRESSION REGULATION; GENE ORDER; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; LOTUS; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC;

MESORHIZOBIUM LOTI; PROTEOBACTERIA;

EID: 70350170511     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06843.x     Document Type: Article

References (54)

1. Altschul, S.F., Madden, T.L., Schlatter, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, DJ. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
2. Antoine, R., Alonso, S., Raze, D., Coutte, L., Lesjean, S., Willery, E., et al. (2000) New virulence-activated and virulence-repressed genes identified by systematic gene inactivation and generation of transcriptional fusions in Bordetella pertussis. J Bacteriol 182: 5902-5905. (Pubitemid 30746541)
3. Bailey, T.L., and Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14: 48-54.
4. Bailey, T.L., Williams, N., Misleh, C., and Li, W.W. (2006) MEME: discovering and analysing DNA and protein sequence motifs. Nucleic Adds Res 34: W369-W373. (Pubitemid 44529795)
5. Binnewies, T.T., Motro, Y., Hallin, P.F., Lund, O., Dunn, D., La, T., et al. (2006) Ten years of bacterial genome sequencing: comparative-genomics-based discoveries. Fund lntegr Genomics 6: 165-185. (Pubitemid 43885067)
6. Burrus, V., and Waldor, M.K. (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Mierobid 155: 376-386. (Pubitemid 38781181)
7. Burrus, V., Pavlovic, G., Decaris, B., and Guédon, G. (2002) Conjugative transposons: the tip of the iceberg. Mol Microbiol 46: 601-610.
8. Chen, G., Jeffrey, P.D., Fuqua, C., Shi, Y., and Chen, L. (2007) Structural basis for antiactivation in bacterial quorum sensing. Proc Natl Acad Sci USA 104: 16474-16479. (Pubitemid 350211043)
9. Cheng, J., Sibley, C.D., Zaheer, R., and Finan, T.M. (2007) A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology 153: 375-387. (Pubitemid 46306485)
10. Chhabra, S.R., Stead, P., Bainton, N.J., Salmond, G.P., Stewart, G.S., Williams, P., and Bycroft, B.W. (1993) Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl) -L-homoserine lactone. J Antibiot (Tokyo) 46: 441-454. (Pubitemid 23127304)
11. Chhabra, S.R., Harty, C., Hooi, D.S., Daykin, M., Williams, P., Telford, G., et al. (2003) Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-Lhomoserine lactone as immune modulators. J Med Chem 46: 97-104. (Pubitemid 36043789)
12. Danino, V.E., Wilkinson, A., Edwards, A., and Downie, J.A. (2003) Recipient-induced transfer of the symbiotic plasmid pR1jI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Mierobiol 50: 511-525. (Pubitemid 37297131)
13. Dobrindt, U., Hochhut, B., Hentschel, U., and Hacker, J. (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Mierobiol 2: 414-424. (Pubitemid 39490120)
14. Dombrecht, B., Vanderleyden, J., and Michiels, J. (2001) Stable RK2-derived cloning vectors for the analysis of gene expression and gene function in gram-negative bacteria. MoI Plant Microbe Interact 14: 426-430. (Pubitemid 32176739)
15. Frost, L.S., Leplae, R., Summers, A.O., and Toussaint, A.(2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3: 722-732. (Pubitemid 41195088)
16. Fuqua, C., and Winans, S.C. (1996) Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J Bacteriol 178: 435-440. (Pubitemid 26030596)
17. 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.
18. Fuqua, W.C., and Winans, S.C. (1994) A LuxR-Luxl type regulatory system activates AgrobaderiumTi plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol 176: 2796-2806.
19. Gould, T.A., Herman, J., Krank, J., Murphy, R.C., and Churchill, M.E. (2006) Specificity of acyl-homoserine lactone synthases examined by mass spectrometry. J Bacteriol 188: 773-783. (Pubitemid 43100563)
20. Grant, G.S.N., Jessee, F.R., Bloom, F.R., and Hanahan, D. (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 87: 4645-4649. (Pubitemid 20204159)
21. Guy, L. (2006) Identification and characterization of pathogenicity and other genomic islands using base composition analyses. Future Microbiol 1: 309-316.
22. Hwang, I., Li, P.L., Zhang, L., Piper, K.R., Cook, D.M., Tate, M.E., and Farrand, S.K. (1994) Tral, a Luxl homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc Natl Acad Sci USA 91: 4639-4643. (Pubitemid 24177704)
23. Hwang, I., Cook, D.M., and Farrand, S.K. (1995) A new regulatory element modulates homoserine lactonemediated autoinduction of Ti plasmid conjugal transfer. J Bacteriol 177: 449-458.
24. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., et al. (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7: 331-338.
25. Khan, S.R., Gaines, J., Roop, R.M., 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 Mierobid 74: 5053-5062.
26. Krick, A., Kehraus, S., Eberi, L., Riedel, K., Anke, H., Kaesler, I., et al. (2007) A marine Mesorhizobium sp. produces structurally novel long-chain N-acyl-L-homoserine lactones. Appl Environ Microbiol 73: 3587-3594. (Pubitemid 46871448)
27. de Lorenzo, V., Eltis, L., Kessler, B., and Timmis, K.N. (1993) Analysis of Pseudomonas gene products using lacf/Ptrp- lac plasmids and transposons that confer conditional phenotypes. Gene 123: 17-24. (Pubitemid 23035786)
28. McAnulla, C., Edwards, A., Sanchez-Contreras, M., Sawers, R.G., and Downie, J.A. (2007) Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar Vidae. Microbiology 153: 2074-2082.
29. McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Cámara, M., et al. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143: 3703-3711. (Pubitemid 28004603)
30. Mantri, Y., and Williams, K.P. (2004) Islander: a database of integrative islands in prokaryotic genomes, the associated integrases and their DNA site specificities. Nucleic Adds Res 32: D55-D58. (Pubitemid 38081604)
31. Marchler-Bauer, A., Anderson, J.B., Derbyshire, M.K., DeWeese-Scott, C, Gonzales, N.R., Gwadz, M., et al. (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35: D237-D240.
32. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
33. Miller, W.G., Leveau, J.H., and Lindow, S.E. (2000) Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 13: 1243-1250.
34. Ochman, H., Lawrence, J.G., and Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304. (Pubitemid 30337055)
35. Ortori, C.A., Atkinson, S., Chhabra, S.R., Cámara, M., Williams, P., and Barrett, D.A. (2007) Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal Bioanal Chem 387: 497-511. (Pubitemid 46067465)
36. Ou, H.Y., Chen, L.L., Lonnen, J., Chaudhuri, R.R., Thani, A.B., Smith, R., et al. (2006) A novel strategy for the identification of genomic islands by comparative analysis of the contents and contexts of tRNA sites in closely related bacteria. Nucleic Acids Res 34: e3. (Pubitemid 43160066)
37. Pappas, K.M., and Winans, S.C. (2003) A LuxR-type regulator from Agrobacterium tumefadens elevates Ti plasmid copy number by activating transcription of plasmid replication genes. MoI Microbiol 48: 1059-1073.
38. Piper, K.R., Beck von Bodman, S., and Farrand, S.K. (1993) Conjugation factor of Agrobacterium tumefadens regulates Ti plasmid transfer by autoinduction. Nature 362:448-450. (Pubitemid 23107367)
39. Piper, K.R., Beck Von Bodman, S., Hwang, I., and Farrand, S.K. (1999) Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol Microbiol 32: 1077-1089. (Pubitemid 29255773)
40. Qin, Y.P., Su, S.C., and Farrand, S.K. (2007) Molecular basis of transcriptional antiactivation -TraM disrupts the TraRDNA complex through stepwise interactions. J Biol Chem 282: 19979-19991.
41. Quandt, J., and Hynes, M.F. (1993) Versatile suicide vectors which allow direct selection for gene replacement in gramnegative bacteria. Gene 127: 15-21. (Pubitemid 23140440)
42. 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 RIxS. Mol Mierobiol 62: 723-734.
43. Sanchez-Contreras, M., Bauer, W.D., Gao, M., Robinson, J.B., and Downie, J.A. (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond B 362: 1149-1163. (Pubitemid 47075147)
44. Schaefer, A.L., Greenberg, E.P., Oliver, C.M., Oda, Y., Huang, J.J., Bittan-Banin, G., et al. (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454: 595-599.
45. Su, S.C., Khan, S.R., and Farrand, S.K. (2008) Induction and loss of Ti plasmid conjugative competence in response to the acyl-homoserine lactone quorum-sensing signal. J Bacteriol 190: 4398-4407.
46. 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.
47. 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.
48. Sullivan, J.T., Trzebiatowski, J.R., Cruickshank, R.W., Gouzy, J., Brown, S.D., Elliot, R.M., et al. (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184: 3086-3095.
49. 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. (Pubitemid 36992948)
50. Waters, C.M., and Bassler, B.L. (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346. (Pubitemid 41740638)
51. White, C.E., and Winans, S.C. (2007) Cell-cell communication in the plant pathogen Agrobacterium tumefadens. Philos Trans R Soc Lond B 362: 1135-1148.
52. Williams, P., Winzer, K., Chan, W.C., and Cámara, M. (2007) Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362: 1119-1134. (Pubitemid 47075145)
53. Yang, M., Sun, K., Zhou, L., Yang, R., Zhong, Z., and Zhu, J. (2009) Functional analysis of three AHL autoinducer synthase genes in Mesorhizobium loti reveals the important role of quorum sensing in symbiotic nodulation. Can J Microbiol 55: 210-214.
54. Yoon, S.H., Hur, C.G., Kang, H.Y., Kim, Y.H., Oh, T.K., and Kim, J.F. (2005) A computational approach for identifying pathogenicity islands in prokaryotic genomes. BMC Bioinformatics 6: 184.