A bioinformatic survey of distribution, conservation, and probable functions of LuxR solo regulators in bacteria

Frontiers in Cellular and Infection Microbiology

Volumn 5, Issue FEB, 2015, Pages

  Subramoni, Sujatha ^a   Salcedo, Diana Vanessa Florez ^b   Suarez Moreno, Zulma R ^a  

^a UNIVERSIDAD DE LA SABANA   (Colombia)

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

LuxR solos or orphans; Orthologs; Phylogeny; QS domain LuxR proteins; Quorum sensing

Indexed keywords

N ACYLHOMOSERINE LACTONE; TRANSCRIPTION FACTOR LUXR;

ALPHAPROTEOBACTERIA; AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIA; BACTERIAL GENOME; BETAPROTEOBACTERIA; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; DATA BASE; GAMMAPROTEOBACTERIA; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENETIC CODE; HEALTH SURVEY; INTERPRO DATA BASE; NONHUMAN; ORTHOLOGY; PHYLOGENY; QUORUM SENSING; SEQUENCE ALIGNMENT; TAXONOMIC IDENTIFICATION;

EID: 84989306749     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2015.00016     Document Type: Article

References (72)

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. U.S.A. 108, 7183-7188. doi: 10.1073/pnas.1103821108
2. Ahmer, B. M. (2004). Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52, 933-945. doi: 10.1111/j.1365-2958.2004.04054.x
3. Ahmer, B. M., van Reeuwijk, J., Timmers, C. D., Valentine, P. J., and Heffron, F. (1998). Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J. Bacteriol. 180, 1185-1193.
4. Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., et al. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208. doi: 10.1093/nar/gkp335
5. Biswa, P., and Doble, M. (2013). Production of acylated homoserine lactone by gram-positive bacteria isolated from marine water. FEMS Microbiol. Lett. 343, 34-41. doi: 10.1111/1574-6968.12123
6. Brachmann, A. O., Brameyer, S., Kresovic, D., Hitkova, I., Kopp, Y., Manske, C., et al. (2013). Pyrones as bacterial signaling molecules. Nat. Chem. Biol. 9, 573-578. doi: 10.1038/nchembio.1295
7. Case, R. J., Labbate, M., and Kjelleberg, S. (2008). AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J. 2, 345-349. doi: 10.1038/ismej.2008.13
8. Chai, Y., Zhu, J., and Winans, S. C. (2001). TrlR, a defective TraR-like protein of Agrobacterium tumefaciens, blocks TraR function in vitro by forming inactive TrlR:TraR dimers. Mol. Microbiol. 40, 414-421. doi: 10.1046/j.1365-2958.2001.02385.x
9. Choi, S. H., and Greenberg, E. P. (1991). The C-terminal region of the Vibrio fischeri LuxR protein contains an inducer-independent lux gene activating domain. Proc. Natl. Acad. Sci. U.S.A. 88, 11115-11119. doi: 10.1073/pnas.88.24.11115
10. Chugani, S. A., Whiteley, M., Lee, K. M., D'argenio, D., Manoil, C., and Greenberg, E. P. (2001). QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 98, 2752-2757. doi: 10.1073/pnas.051624298
11. Cox, A. R., Thomson, N. R., Bycroft, B., Stewart, G. S., Williams, P., and Salmond, G. P. (1998). A pheromone-independent CarR protein controls carbapenem antibiotic synthesis in the opportunistic human pathogen Serratia marcescens. Microbiology 144(Pt 1), 201-209. doi: 10.1099/00221287-144-1-201
12. 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. doi: 10.1046/j.1365-2958.2003.03699.x
13. Delrue, R. M., Deschamps, C., Leonard, S., Nijskens, C., Danese, I., Schaus, J. M., et al. (2005). A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell. Microbiol. 7, 1151-1161. doi: 10.1111/j.1462-5822.2005.00543.x
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. U.S.A. 86, 5688-5692. doi: 10.1073/pnas.86.15.5688
15. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
16. Ferluga, S., Bigirimana, J., Hofte, M., and Venturi, V. (2007). A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol. Plant Pathol. 8, 529-538. doi: 10.1111/j.1364-3703.2007.00415.x
17. Ferluga, S., and Venturi, V. (2009). OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J. Bacteriol. 191, 890-897. doi: 10.1128/JB.01507-08
18. Fernandez-Pinar, R., Camara, M., Soriano, M. I., Dubern, J. F., Heeb, S., Ramos, J. L., et al. (2011). PpoR, an orphan LuxR-family protein of Pseudomonas putida KT2440, modulates competitive fitness and surface motility independently of N-acylhomoserine lactones. Environ. Microbiol. Rep. 3, 79-85. doi: 10.1111/j.1758-2229.2010.00190.x
19. Frickey, T., and Lupas, A. (2004). CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20, 3702-3704. doi: 10.1093/bioinformatics/bth444
20. Fuqua, C. (2006). The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J. Bacteriol. 188, 3169-3171. doi: 10.1128/JB.188.9.3169-3171.2006
21. Fuqua, C., and Greenberg, E. P. (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3, 685-695. doi: 10.1038/nrm907
22. Fuqua, C., Winans, S. C., and Greenberg, E. P. (1996). Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 50, 727-751. doi: 10.1146/annurev.micro.50.1.727
23. Fuqua, W. C., Winans, S. C., and Greenberg, E. P. (1994). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269-275.
24. Gao, M., Tang, M., Guerich, L., Salas-Gonzalez, I., and Teplitski, M. (2014). Modulation of Sinorhizobium meliloti quorum sensing by Hfq-mediated post-transcriptional regulation of ExpR. Environ. Microbiol. Rep. doi: 10.1111/1758-2229.12235. [Epub ahead of print].
25. Gonzalez, J. F., Myers, M. P., and Venturi, V. (2013). The inter-kingdom solo OryR regulator of Xanthomonas oryzae is important for motility. Mol. Plant Pathol. 14, 211-221. doi: 10.1111/j.1364-3703.2012.00843.x
26. Gonzalez, J. F., and Venturi, V. (2013). A novel widespread interkingdom signaling circuit. Trends Plant Sci. 18, 167-174. doi: 10.1016/j.tplants.2012.09.007
27. Hall, B. G. (2013). Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 30, 1229-1235. doi: 10.1093/molbev/mst012
28. Hao, G., Zhang, H., Zheng, D., and Burr, T. J. (2005). luxR homolog avhR in Agrobacterium vitis affects the development of a grape-specific necrosis and a tobacco hypersensitive response. J. Bacteriol. 187, 185-192. doi: 10.1128/JB.187.1.185-192.2005
29. Hanzelka, B. L., and Greenberg, E. P. (1995). Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain. J. Bacteriol. 177, 815-817.
30. Huang, Y., Niu, B., Gao, Y., Fu, L., and Li, W. (2010). CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680-682. doi: 10.1093/bioinformatics/btq003
31. Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T. K., Bateman, A., et al. (2012). InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res. 40, D306-D312. doi: 10.1093/nar/gks456
32. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
33. Kanamaru, K., Kanamaru, K., Tatsuno, I., Tobe, T., and Sasakawa, C. (2000). SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 38, 805-816.
34. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948. doi: 10.1093/bioinformatics/btm404
35. Ledgham, F., Ventre, I., Soscia, C., Foglino, M., Sturgis, J. N., and Lazdunski, A. (2003). Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol. Microbiol. 48, 199-210. doi: 10.1046/j.1365-2958.2003.03423.x
36. Lindemann, A., Pessi, G., Schaefer, A. L., Mattmann, M. E., Christensen, Q. H., Kessler, A., et al. (2011). Isovaleryl-homoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S.A. 108, 16765-16770. doi: 10.1073/pnas.1114125108
37. Luo, Z. Q., and Farrand, S. K. (1999). Signal-dependent DNA binding and functional domains of the quorum-sensing activator TraR as identified by repressor activity. Proc. Natl. Acad. Sci. U.S.A. 96, 9009-9014. doi: 10.1073/pnas.96.16.9009
38. Malott, R. J., O'grady, E. P., Toller, J., Inhulsen, S., Eberl, L., and Sokol, P. A. (2009). A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J. Bacteriol. 191, 2447-2460. doi: 10.1128/JB.01746-08
39. Mavrodi, D. V., Bonsall, R. F., Delaney, S. M., Soule, M. J., Phillips, G., and Thomashow, L. S. (2001). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J. Bacteriol. 183, 6454-6465. doi: 10.1128/JB.183.21.6454-6465.2001
40. McDowall, J., and Hunter, S. (2011). InterPro protein classification. Methods Mol. Biol. 694, 37-47. doi: 10.1007/978-1-60761-977-2_3
41. Michael, B., Smith, J. N., Swift, S., Heffron, F., and Ahmer, B. M. (2001). SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183, 5733-5742. doi: 10.1128/JB.183.19.5733-5742.2001
42. Molina-Henares, A. J., Krell, T., Eugenia Guazzaroni, M., Segura, A., and Ramos, J. L. (2006). Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol. Rev. 30, 157-186. doi: 10.1111/j.1574-6976.2005.00008.x
43. Oberto, J. (2013). SyntTax: a web server linking synteny to prokaryotic taxonomy. BMC Bioinformatics 14:4. doi: 10.1186/1471-2105-14-4
44. Oinuma, K., and Greenberg, E. P. (2011). Acyl-homoserine lactone binding to and stability of the orphan Pseudomonas aeruginosa quorum-sensing signal receptor QscR. J. Bacteriol. 193, 421-428. doi: 10.1128/JB.01041-10
45. Patankar, A. V., and Gonzalez, J. E. (2009a). An orphan LuxR homolog of Sinorhizobium meliloti affects stress adaptation and competition for nodulation. Appl. Environ. Microbiol. 75, 946-955. doi: 10.1128/AEM.01692-08
46. Patankar, A. V., and Gonzalez, J. E. (2009b). Orphan LuxR regulators of quorum sensing. FEMS Microbiol. Rev. 33, 739-756. doi: 10.1111/j.1574-6976.2009.00163.x
47. 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. doi: 10.1128/JB.184.18.5067-5076.2002
48. Poulter, S., Carlton, T. M., Spring, D. R., and Salmond, G. P. (2011). The Serratia LuxR family regulator CarR 39006 activates transcription independently of cognate quorum sensing signals. Mol. Microbiol. 80, 1120-1131. doi: 10.1111/j.1365-2958.2011.07634.x
49. Qiu, X., Kulasekara, B. R., and Lory, S. (2009). Role of horizontal gene transfer in the evolution of Pseudomonas aeruginosa virulence. Genome Dyn. 6, 126-139. doi: 10.1159/000235767
50. Rambow-Larsen, A. A., Rajashekara, G., Petersen, E., and Splitter, G. (2008). Putative quorum-sensing regulator BlxR of Brucella melitensis regulates virulence factors including the type IV secretion system and flagella. J. Bacteriol. 190, 3274-3282. doi: 10.1128/JB.01915-07
51. Ryan, G. T., Wei, Y., and Winans, S. C. (2013). A LuxR-type repressor of Burkholderia cenocepacia inhibits transcription via antiactivation and is inactivated by its cognate acylhomoserine lactone. Mol. Microbiol. 87, 94-111. doi: 10.1111/mmi.12085
52. Sabag-Daigle, A., and Ahmer, B. M. (2012). ExpI and PhzI are descendants of the long lost cognate signal synthase for SdiA. PLoS ONE 7:e47720. doi: 10.1371/journal.pone.0047720
53. 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. doi: 10.1038/nature07088
54. Soares, J. A., and Ahmer, B. M. (2011). Detection of acyl-homoserine lactones by Escherichia and Salmonella. Curr. Opin. Microbiol. 14, 188-193. doi: 10.1016/j.mib.2011.01.006
55. Solovyev, V., and Salamov, A. (2011). "Automatic annotation of microbial genomes and metagenomic sequences," in Metagenomics and its Applications in Agriculture, Biomedicine and Environmental Studies, ed R. W. Li (Hauppauge, NY: Nova Science Publishers), 61-78.
56. Subramoni, S., Gonzalez, J. F., Johnson, A., Pechy-Tarr, M., Rochat, L., Paulsen, I., et al. (2011). Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 77, 4579-4588. doi: 10.1128/AEM.00183-11
57. Subramoni, S., and Venturi, V. (2009a). LuxR-family 'solos': bachelor sensors/regulators of signalling molecules. Microbiology 155, 1377-1385. doi: 10.1099/mic.0.026849-0
58. Subramoni, S., and Venturi, V. (2009b). PpoR is a conserved unpaired LuxR solo of Pseudomonas putida which binds N-acyl homoserine lactones. BMC Microbiol. 9:125. doi: 10.1186/1471-2180-9-125
59. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
60. Thomas-Chollier, M., Defrance, M., Medina-Rivera, A., Sand, O., Herrmann, C., Thieffry, D., et al. (2011). RSAT 2011: regulatory sequence analysis tools. Nucleic Acids Res. 39, W86-W91. doi: 10.1093/nar/gkr377
61. Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2002). Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics Chap. 2: Unit 2.3. doi: 10.1002/0471250953.bi0203s00
62. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. doi: 10.1093/nar/22.22.4673
63. Tyson, G. W., Chapman, J., Hugenholtz, P., Allen, E. E., Ram, R. J., Richardson, P. M., et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37-43. doi: 10.1038/nature02340
64. Uzureau, S., Lemaire, J., Delaive, E., Dieu, M., Gaigneaux, A., Raes, M., et al. (2010). Global analysis of quorum sensing targets in the intracellular pathogen Brucella melitensis 16 M. J. Proteome Res. 9, 3200-3217. doi: 10.1021/pr100068p
65. Venturi, V., and Fuqua, C. (2013). Chemical signaling between plants and plant-pathogenic bacteria. Annu. Rev. Phytopathol. 51, 17-37. doi: 10.1146/annurev-phyto-082712-102239
66. Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J., and Salmond, G. P. (2001). Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25, 365-404. doi: 10.1111/j.1574-6976.2001.tb00583.x
67. Whiteley, M., and Greenberg, E. P. (2001). Promoter specificity elements in Pseudomonas aeruginosa quorum-sensing-controlled genes. J. Bacteriol. 183, 5529-5534. doi: 10.1128/JB.183.19.5529-5534.2001
68. Wilkinson, A., Danino, V., Wisniewski-Dye, F., Lithgow, J. K., and Downie, J. A. (2002). N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. 184, 4510-4519. doi: 10.1128/JB.184.16.4510-4519.2002
69. Zhang, L., Jia, Y., Wang, L., and Fang, R. (2007). A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol. Microbiol. 65, 121-136. doi: 10.1111/j.1365-2958.2007.05775.x
70. Zhang, R. G., Pappas, K. M., Brace, J. L., Miller, P. C., Oulmassov, T., Molyneaux, J. M., et al. (2002). Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417, 971-974. doi: 10.1038/nature00833
71. Zheng, D., Zhang, H., Carle, S., Hao, G., Holden, M. R., and Burr, T. J. (2003). A luxR homolog, aviR, in Agrobacterium vitis is associated with induction of necrosis on grape and a hypersensitive response on tobacco. Mol. Plant Microbe. Interact. 16, 650-658. doi: 10.1094/MPMI.2003.16.7.650
72. Zhu, J., and Winans, S. C. (2001). The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc. Natl. Acad. Sci. U.S.A. 98, 1507-1512. doi: 10.1073/pnas.98.4.1507