Effects of AiiA-mediated quorum quenching in Sinorhizobium meliloti on quorum-sensing signals, proteome patterns, and symbiotic interactions

Molecular Plant-Microbe Interactions

Volumn 20, Issue 7, 2007, Pages 843-856

  Gao, Mengsheng ^a   Chen, Hancai ^b   Eberhard, Anatol ^c   Gronquist, Matthew R ^d   Robinson, Jayne B ^e   Connolly, Mary ^e   Teplitski, Max ^a   Rolfe, Barry G ^b   Bauer, Wolfgang D ^f  

^a UNIVERSITY OF FLORIDA   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c Department of Obstetrics Gynecology   (United States)

^d STATE UNIVERSITY OF NEW YORK AT FREDONIA   (United States)

^e UNIVERSITY OF DAYTON   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacteroids; ESI MS MS; ExpR; SinI

Indexed keywords

BACTERIAL PROTEIN; CARBOXYLESTERASE; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; N ACYL HOMOSERINE LACTONASE; N-ACYL HOMOSERINE LACTONASE; PROTEOME; UNCLASSIFIED DRUG;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MEDICAGO; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; QUORUM SENSING; SINORHIZOBIUM MELILOTI; SYMBIOSIS; THIN LAYER CHROMATOGRAPHY;

4-BUTYROLACTONE; BACTERIAL PROTEINS; CARBOXYLIC ESTER HYDROLASES; CHROMATOGRAPHY, THIN LAYER; GENE EXPRESSION REGULATION, BACTERIAL; MEDICAGO; PROTEOME; QUORUM SENSING; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); EUKARYOTA; MEDICAGO TRUNCATULA; SINORHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 34250633557     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-20-7-0843     Document Type: Article

References (83)

1. Agafonov, D. E., Kolb, V. A., Nazimov, I. V., and Spirin, A. S. 1999. A protein residing at the subunit interface of the bacterial ribosome. Proc. Natl. Acad. Sci. U.S.A. 96:12345-12349.
2. Alfano, J. R., and Kahn, M. L. 1993. Isolation and characterization of a gene coding for a novel aspartate aminotransferase from Rhizobium meliloti. J. Bacteriol. 175:4186-4196.
3. Arevalo-Ferro, C., Hentzer, M., Reil, G., Gorg, A., Kjelleberg, S., Givskov, M., Riedel, K., and Eberl, L. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:1350-1369.
4. Bae, Y. M., and Crawford, I. P. 1990. The Rhizobium meliloti trpE(G) gene is regulated by attenuation, and its product, anthranilate synthase, is regulated by feedback inhibition. J. Bacteriol. 172:3318-3327.
5. Barsomian, G. D., Urzainqui, A., Lohman, K., and Walker, G. C. 1992. Rhizobium meliloti mutants unable to synthesize anthranilate display a novel symbiotic phenotype. J. Bacteriol. 174:4416-4426.
6. Bassler, B. L., and Losick, R. 2006. Bacterially speaking. Cell 125:237-46.
7. Bhuvaneswari, T. V., Bhagwat, A., and Bauer, W. D. 1981. Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol. 68:1144-1149.
8. Bittner, A. N., and Oke, V. 2006. Multiple groESL operons are not key targets of RpoH1 and RpoH2 in Sinorhizobium meliloti. J. Bacteriol. 188:3507-3515.
9. Brencic, A., and Winans, S. C. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:155-194.
10. Cantero, L., Palacios, J. M., Ruiz-Argueso, T., and Imperial, J. 2006. Proteomic analysis of quorum sensing in Rhizobium leguminosarum biovar viciae UPM791. Proteomics 6 (Suppl. 1):S97-S106.
11. Cha, C., Gao, P., Chen, Y. C., Shaw, P. D., and Farrand, S. K. 1998. Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11:1119-1129.
12. Chen, H., Higgins, J., Kondorosi, E., Kondorosi, A., Djordjevic, M. A., Weinman, J. J., and Rolfe, B. G. 2000. Identification of nolR-regulated proteins in Sinorhizobium meliloti using proteome analysis. Electrophoresis 21:3823-3832.
13. Chen, H., Teplitski, M., Gao, M., Robinson, J. B., Rolfe, B. G., and Bauer, W. D. 2003. Proteomic analysis of wildtype Sinorhizobium meliloti responses to N-acyl homoserine lactone quorum sensing signals. J. Bacteriol. 185:5029-5036.
14. Daniels, R., De Vos, D. E., Desair, J., Raedschelders, G., Luyten, E., Rosemeyer, V., Verreth, C., Schoeters, E., Vanderleyden, J., and Michiels, J. 2002. The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J. Biol. Chem. 277:462-468.
15. Daniels, R., Vanderleyden, J., and Michiels, J. 2004. Quorum sensing and swarming migration in bacteria. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 28:261-289.
16. Degrassi, G., Devescovi, G., Solis, R., Steindler, L., and Venturi, V. 2007. Oryza sativa rice plants contain molecules that activate different quorum-sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 269:213-220.
17. Dong, Y. H., and Zhang, L. H. 2005. Quorum sensing and quorum-quenching enzymes. J. Microbiol. (Spec. No.) 43:101-109.
18. Dong, Y. H., Xu, J. L., Li, X. Z., and Zhang, L. H. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. U.S.A. 97:3526-3531.
19. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and Zhang, L. H. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813-817.
20. Dong, Y. H., Gusti, A. R., Zhang, Q., Xu, J. L., and Zhang, L. H. 2002. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68:1754-1759.
21. Dong, Y. H.. Zhang. X. F., Xu, J. L., and Zhang, L. H. 2004. Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl. Environ. Microbiol. 70:954-960.
22. Dudler, R., and Eberl, L. 2006. Interactions between bacteria and eukaryotes via small molecules. Curr. Opin. Biotechnol. 17:268-273.
23. Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, G. L., Nealson, K. H., and Oppenheimer, N. J. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-2449.
24. Galibert, F., Finan, T. M., Long, S. R., Puhle, R. A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R. W., Dreano, S., Federspiel, N. A., Fisher, R. F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., Hernandez-Lucas, I., Hong, A., Huizar, L., Hyman, R. W., Jones, T., Kahn, D., Kahn, M. L. Kalman, S., Keating, D. H., Kiss, E., Komp, C., Lelaure, V., Masuy, D., Palm, C., Peck, M. C., Pohl, T. M., Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F. J., Weidne, R. S., Wells, D. H., Wong, K., Yeh, K. C., and Batut, J. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
25. Gao, M., Teplitski, M., Robinson, J. B., and Bauer, W. D. 2003. Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol. Plant-Microbe Interact. 16:827-834.
26. Gao, M., Chen, H., Eberhard, A., Gronquist, M. R., Robinson, J. B., Rolfe, B. G., and Bauer, W. D. 2005. sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J. Bacteriol. 187:7931-7944.
27. Givskov, M., Nys, R. D., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D., and Kjelleberg, S. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178:6618-6622.
28. Glazebrook, J., and Walker, G. C. 1991. Genetic techniques in Rhizobium meliloti. Methods Enzymol. 204:398-418.
29. Gonzalez, J. E., and Marketon, M. M. 2003. Quorum sensing in nitrogen-fixing rhizobia. Microbiol. Mol. Biol. Rev. 67:574-592.
30. Gray, K. M., Pearson, J. P., Downie, J. A., Boboye, B. E., and Greenberg, E. P. 1996. Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: Autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178:372-376.
31. Grundy, F. J., and Henkin, T. M. 2004. Kinetic analysis of tRNA-directed transcription antitermination of the Bacillus subtilis glyQS gene in vitro. J. Bacteriol. 186:5392-5399.
32. Haynes, J. G., Czymmek, K. J., Carlson, C. A., Veereshlingam, H., Dickstein, R., and Sherrier, D. J. 2004. Rapid analysis of legume root nodule development using confocal microscopy New Phytol. 163:661-668.
33. Hentzer, M., Wu, H., Andersen, J. B., Riedel, K., Rasmussen, T. B., Bagge, N., Kumar, N., Schembri, M. A., Song, Z., Kristoffersen, P., Manefield, M., Costerton, J. W., Molin, S., Eberl, L., Steinberg, P., Kjelleberg, S., Hoiby, N., and Givskov, M. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO (Eur. Mol. Biol. Organ.) J. 22:3803-3815.
34. Hoang, H. H., Becker, A., and Gonzalez, J. E. 2004. The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J. Bacteriol. 186:5460-5472.
35. Kabir, M.S., Sagara, T., Oshima, T., Kawagoe, Y., Mori, H., Tsunedomi, R., and Yamada, M. 2004. Effects of mutations in the rpoS gene on cell viability and global gene expression under nitrogen starvation in Escherichia coli. Microbiology 150:2543-2553.
36. Kainou, T., Okada, K., Suzuki, K., Nakagawa, T., Matsuda, H., and Kawamukai, M. 2001. Dimer formation of octaprenyl-diphosphate synthase (lspB) is essential for chain length determination of ubiquinone. J. Biol. Chem. 276:7876-7883.
37. Keller, L., and Surette, M. G. 2006. Communication in bacteria: An ecological and evolutionary perspective. Nat. Rev. Microbiol. 4:249-258.
38. Li, K., Hein, S., Zou, W., and Klug, G. 2004. The glutathione- glutaredoxin system in Rhodobacter capsulatus: Part of a complex regulatory network controlling defense against oxidative stress. J. Bacteriol. 186:6800-6808.
39. Loh, J., Pierson, E. A., Pierson, L. S., 3rd, Stacey, G., and Chatterjee, A. 2002. Quorum sensing in plant-associated bacteria. Curr. Opin. Plant Biol. 5:285-290.
40. Long, S., McCune, S., and Walker, G. C. 1988. Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis. J. Bacteriol. 170:4257-4265.
41. Lupp, C., and Ruby, E. G. 2005. Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J. Bacteriol. 187:3620-3629.
42. Lupp, C., Urbanowski, M., Greenberg, E. P., and Ruby, E. G. 2003. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol. Microbiol. 50:319-331.
43. Maki, Y., Yoshida, H., and Wada, A. 2000. Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells 5:965-974.
44. Margolin, W. 2003. Bacterial division: The fellowship of the ring. Curr. Biol. 13:R16-18.
45. Margolin, W., and Long, S. R. 1994. Rhizobium meliloti contains a novel second homolog of the cell division gene ftsZ. J. Bacteriol. 176:2033-2043.
46. Margolin, W., Corbo, J. C., and Long, S. R. 1991. Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J. Bacteriol. 173:5822-5830.
47. Marketon, M. M., and Gonzalez, J. E. 2002. Identification of two quorum-sensing systems in Sinorhizobium meliloti. J. Bacteriol. 184:3466-3475.
48. Marketon, M. M., Gronquist, M. R., Eberhard, A., and Gonzalez, J. E. 2002. Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J. Bacteriol. 184:5686-5695.
49. McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S., Bycroft, B. W., Stewart, G. S., and Williams, P. 1997. Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703-3711.
50. Meade, H. M., and Signer, E. R. 1977. Genetic mapping of Rhizobium meliloti. Proc. Natl. Acad. Sci. U.S.A. 74:2076-2078.
51. Mitsui, H., Sato, T., Sato, Y., Ito, N., and Minamisawa, K. 2004. Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa. Mol. Genet. Genomics. 271:416-425.
52. Molina, L., Rezzonico, F., Defago, G., and Duffy, B. 2005. Autoinduction in Erwinia amylovora: Evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J. Bacteriol. 187:3206-3213.
53. Morita, T., Maki, K., and Aiba, H. 2005. RNase E-based ribonucleoprotein complexes: Mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 19:2176-2186.
54. Natera, S. H. A., Guerreiro, N., and Djordjevic, M. A. 2000. Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Mol. Plant-Microbe Interact. 13:995-1009.
55. Neuhoff, V., Arold, N., Taube, D., and Ehrhardt, W. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255-262.
56. Pearson, J. P., Van Delden, C., and Iglewski, B. H. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181:1203-1210.
57. 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.
58. Richardson, L. V., and Richardson, J. P. 2005. Identification of a structural element that is essential for two functions of transcription factor NusG. Biochim. Biophys. Acta 1729:135-140.
59. Sanchez-Contreras, M., Bauer, W. D., Gao, M., Robinson, J. B., and Downie, A. J. 2007. Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Phil. Trans. R. Soc.doi:10.1098/rstb.2007. 2041. Published online.
60. Schuster, M., Lostroh, C. P., Ogi, T., and Greenberg, E. P. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: A transcriptome analysis. J. Bacteriol. 185:2066-2079.
61. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E., Jr., Rinehart, K. L., and Farrand, S. K. 1997. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. U.S.A. 94:6036-6041.
62. Smadja, B., Latour, X., Faure, D., Chevalier, S., Dessaux, Y., and Orange, N. 2004. Involvement of N-acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Mol. Plant-Microbe Interact. 17:1269-1278.
63. Staskawicz, B., Dahlbeck, D., Keen, N., and Napoli, C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
64. Steidle, A., Sigl, K., Schuhegger, R., Ihring, A., Schmid, M., Gantner, S., Stoffels, M., Riedel, K., Givskov, M., Hartmann, A., Langebartels, C., and Eberl, L. 2001. Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67:5761-5770.
65. Swanson, J. A., Mulligan, J. T., and Long, S. R. 1993. Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics 134:435-444.
66. Teplitski, M., Robinson, J. B., and Bauer, W. D. 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact. 13:637-648.
67. Teplitski, M., Eberhard, A., Gronquist, M., Gao, M., Robinson, J. B., and Bauer, W. D. 2003. Chemical identification of N-acyl homoserine lactone quorum sensing signals produced by Sinorhizobium meliloti strains in defined medium. Arch. Microbiol. 180:494-497.
68. Teplitski, M., Chen, H., Rajamani, S., Gao, M., Merighi, M., Sayre, R. T., Robinson, J. B., Rolfe, B. G., and Bauer, W. D. 2004. Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol. 134:137-146.
69. Thorne, S. H., and Williams, H. D. 1999. Cell density-dependent starvation survival of Rhizobium leguminosarum bv. phaseoli: Identification of the role of an N-acyl homoserine lactone in adaptation to stationary-phase survival. J. Bacteriol. 181:981-990.
70. Vasil, M. L. 2003. DNA microarrays in analysis of quorum sensing: Strengths and limitations. J. Bacteriol. 185:2061-2065.
71. von Bodman, S. B., Bauer, W. D., and Coplin, D. L. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Plant Pathol. 41:455-482.
72. Wagner, V. E., Bushnell, D., Passador, L., Brooks, A. I., and Iglewski, B. H. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: Effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
73. Weiller, G. F., Djordjevic, M. J., Caraux, G., Chen, H., and Weinman, J. J. 2001. A specialised proteolytic database for comparing matrix-assisted laser desorption/ionization-time of flight mass spectrometry data of tryptic peptides with corresponding sequence database segments. Proteomics 1:1489-1494.
74. Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J., and Salmond, G. P. 2001. Quorum-sensing in gram-negative bacteria. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 25:365-404.
75. Whiteley, M., Lee, K. M., and Greenberg, E. P. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 96:13904-13909.
76. 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.
77. Winans, S. C. 2002. Bacterial esperanto. Nat. Struct. Biol. 9:83-84.
78. Winson, M. K., Swift, S., Fish, L., Throup, J. P., Jorgensen, F., Chhabra, S. R., Bycroft, B. W., Williams, P., and Stewart, G. S. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 163.185-192.
79. Wisniewski-Dye, F., and Downie, J. A. 2002. Quorum-sensing in Rhizobium. Antonie Leeuwenhoek 81:397-407.
80. Wopperer, J., Cardona, S. T., Huber, B., Jacobi, C. A., Valvano, M. A., and Eberl, L. 2006. A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl. Environ. Microbiol. 72:1579-1587.
81. Zheng, H., Zhong, Z., Lai, X., Chen, W. X., Li, S., and Zhu, J. 2006. A LuxR/LuxI-type quorum-sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation. J. Bacteriol. 188:1943-1949.
82. Zhu, J., and Winans, S. C. 1999. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc. Natl. Acad. Sci. U.S.A. 96:4832-4837.
83. 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.