The novel genes emmABC are associated with exopolysaccharide production, motility, stress adaptation, and symbiosis in Sinorhizobium meliloti

Journal of Bacteriology

Volumn 191, Issue 19, 2009, Pages 5890-5900

  Morris, Jennifer ^a   González, Juan E ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EXOPOLYSACCHARIDE; MUTANT PROTEIN; PROTEIN EMMA; PROTEIN EMMB; PROTEIN EMMC; SUCCINOGLYCAN; UNCLASSIFIED DRUG;

ALFALFA; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL MOTILITY; CONTROLLED STUDY; ENVIRONMENTAL STRESS; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; GENETIC ASSOCIATION; MUTAGENESIS; NONHUMAN; OSMOSIS; PRIORITY JOURNAL; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

BACTERIA (MICROORGANISMS); FABACEAE; MEDICAGO SATIVA; SINORHIZOBIUM MELILOTI;

EID: 70349125074     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00760-09     Document Type: Article

References (63)

1. Alami, Y., W. Achouak, C. Marol, and T. Heulin. 2000. Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide- producing Rhizobium sp. strain isolated from sunflower roots. Appl. Environ. Microbiol. 66:3393-3398.
2. Ali, A., J. A. Johnson, A. A. Franco, D. J. Metzger, T. D. Connell, J. G. Morris, Jr., and S. Sozhamannan. 2000. Mutations in the extracellular protein secretion pathway genes (eps) interfere with rugose polysaccharide production in and motility of Vibrio cholerae. Infect. Immun. 68:1967-1974.
3. Battisti, L., J. C. Lara, and J. A. Leigh. 1992. Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proc. Natl. Acad. Sci. USA 89:5625-5629.
4. Becker, A., S. Rüberg, B. Baumgarth, P. A. Bertram-Drogatz, I. Quester, and A. Pühler. 2002. Regulation of succinoglycan and galactoglucan biosynthesis in Sinorhizobium meliloti. J. Mol. Microbiol. Biotechnol. 4:187-190.
5. Brencic, A., and S. C. Winans. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:155-194.
6. Brumbley, S. M., and T. P. Denny. 1990. Cloning of wild-type Pseudomonas solanacearum phcA, a gene that when mutated alters expression of multiple traits that contribute to virulence. J. Bacteriol. 172:5677-5685.
7. Campbell, G. R., B. L. Reuhs, and G. C. Walker. 2002. Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc. Natl. Acad. Sci. USA 99:3938-3943.
8. Campbell, G. R., L. A. Sharypova, H. Scheidle, K. M. Jones, K. Niehaus, A. Becker, and G. C. Walker. 2003. Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J. Bacteriol. 185: 3853-3862.
9. Cano, D. A., G. Dominguez-Bernal, A. Tierrez, F. Garcia-Del Portillo, and J. Casadesus. 2002. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162:1513-1523.
10. Charles, T. C., and E. W. Nester. 1993. A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 175:6614-6625.
11. Chen, E. J., E. A. Sabio, and S. R. Long. 2008. The periplasmic regulator ExoR inhibits ExoS/ChvI two-component signalling in Sinorhizobium meliloti. Mol. Microbiol. 69:1290-1303.
12. Cheng, H. P., and G. C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:5183-5191.
13. Cheng, H. P., and G. C. Walker. 1998. Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J. Bacteriol. 180:20-26.
14. Cytryn, E. J., D. P. Sangurdekar, J. G. Streeter, W. L. Franck, W. S. Chang, G. Stacey, D. W. Emerich, T. Joshi, D. Xu, and M. J. Sadowsky. 2007. Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J. Bacteriol. 189:6751-6762.
15. Das, S., J. C. Noe, S. Paik, and T. Kitten. 2005. An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites. J. Microbiol. Methods 63:89-94.
16. Davies, B. W., and G. C. Walker. 2007. Disruption of sitA compromises Sinorhizobium meliloti for manganese uptake required for protection against oxidative stress. J. Bacteriol. 189:2101-2109.
17. Dominguez-Ferreras, A., R. Perez-Arnedo, A. Becker, J. Olivares, M. J. Soto, and J. Sanjuan. 2006. Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J. Bacteriol. 188:7617-7625.
18. Finan, T. M., A. M. Hirsch, J. A. Leigh, E. Johansen, G. A. Kuldau, S. Deegan, G. C. Walker, and E. R. Signer. 1985. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40:869-877.
19. Fraysse, N., F. Couderc, and V. Poinsot. 2003. Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur. J. Biochem. 270:1365-1380.
20. Galibert, F., T. M. Finan, S. R. Long, A. Pühler, P. Abola, F. Ampe, F. Barloy-Hubler, M. J. Barnett, A. Becker, P. Boistard, G. Bothe, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R. W. Davis, S. Dreano, N. A. Federspiel, R. F. Fisher, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R. W. Hyman, T. Jones, D. Kahn, M. L. Kahn, S. Kalman, D. H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M. C. Peck, T. M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vandenbol, F. J. Vorholter, S. Weidner, D. H. Wells, K. Wong, K. C. Yeh, and J. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
21. Gibson, K. E., M. J. Barnett, C. J. Toman, S. R. Long, and G. C. Walker. 2007. The symbiosis regulator CbrA modulates a complex regulatory network affecting the flagellar apparatus and cell envelope proteins. J. Bacteriol. 189:3591-3602.
22. Gibson, K. E., G. R. Campbell, J. Lloret, and G. C. Walker. 2006. CbrA is a stationary-phase regulator of cell surface physiology and legume symbiosis in Sinorhizobium meliloti. J. Bacteriol. 188:4508-4521.
23. Glazebrook, J., and G. C. Walker. 1991. Genetic techniques in Rhizobium meliloti. Methods Enzymol. 204:398-418.
24. Glazebrook, J., and G. C. Walker. 1989. A novel exopolysaccharide can function in place of the Calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 56:661-672.
25. Glenn, S. A., N. Gurich, M. A. Feeney, and J. E. González. 2007. The ExpR/Sin quorum-sensing system controls succinoglycan production in Sinorhizobium meliloti. J. Bacteriol. 189:7077-7088.
26. Glucksmann, M. A., T. L. Reuber, and G. C. Walker. 1993. Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J. Bacteriol. 175:7045-7055.
27. González, J. E., and M. M. Marketon. 2003. Quorum sensing in nitrogen-fixing rhizobia. Microbiol. Mol. Biol. Rev. 67:574-592.
28. González, J. E., B. L. Reuhs, and G. C. Walker. 1996. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:8636-8641.
29. González, J. E., G. M. York, and G. C. Walker. 1996. Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179:141-146.
30. Gurich, N., and J. E. González. 2009. The role of quorum sensing in the Sinorhizobium meliloti-alfalfa symbiosis. J. Bacteriol. 191:4372-4382.
31. Hoang, H. H., A. Becker, and J. E. González. 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.
32. Hoang, H. H., N. Gurich, and J. E. González. 2008. Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J. Bacteriol. 190:861-871.
33. Jones, K. M., H. Kobayashi, B. W. Davies, M. E. Taga, and G. C. Walker. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-633.
34. Krol, E., and A. Becker. 2004. Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol. Genet. Genomics 272:1-17.
35. Laus, M. C., T. J. Logman, A. A. Van Brussel, R. W. Carlson, P. Azadi, M. Y. Gao, and J. W. Kijne. 2004. Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J. Bacteriol. 186:6617-6625.
36. Leigh, J. A., E. R. Signer, and G. C. Walker. 1985. Exopolysaccharide- deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:6231-6235.
37. Long, S., J. W. Reed, J. Himawan, and G. C. Walker. 1988. Genetic analysis of a cluster of genes required for synthesis of the Calcofluor-binding exopolysaccharide of Rhizobium meliloti. J. Bacteriol. 170:4239-4248.
38. Marketon, M. M., S. A. Glenn, A. Eberhard, and J. E. González. 2003. Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J. Bacteriol. 185:325-331.
39. Meade, H. M., S. R. Long, G. B. Ruvkun, S. E. Brown, and F. M. Ausubel. 1982. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J. Bacteriol. 149:114-122.
40. Morris, D. 1948. Quantitative determination of carbohydrates with Drerywood's anthrone reagent. Science 108:254-255.
41. Navarini, L., A. Cesaro, and S. B. Ross-Murphy. 1992. Exopolysaccharides from Rhizobium meliloti YE-2 grown under different osmolarity conditions: viscoelastic properties. Carbohydr Res. 223:227-234.
42. Newman, J. R., and C. Fuqua. 1999. Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227:197-203.
43. Ophir, T., and D. L. Gutnick. 1994. A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl. Environ. Microbiol. 60:740-745.
44. Paulsen, I. T., R. Seshadri, K. E. Nelson, J. A. Eisen, J. F. Heidelberg, T. D. Read, R. J. Dodson, L. Umayam, L. M. Brinkac, M. J. Beanan, S. C. Daugherty, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, W. C. Nelson, B. Ayodeji, M. Kraul, J. Shetty, J. Malek, S. E. Van Aken, S. Riedmuller, H. Tettelin, S. R. Gill, O. White, S. L. Salzberg, D. L. Hoover, L. E. Lindler, S. M. Halling, S. M. Boyle, and C. M. Fraser. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99:13148-13153.
45. Pellock, B. J., H. P. Cheng, and G. C. Walker. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:4310-4318.
46. Pellock, B. J., M. Teplitski, R. P. Boinay, W. D. Bauer, and G. C. Walker. 2002. A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 184:5067-5076.
47. Pobigaylo, N., D. Wetter, S. Szymczak, U. Schiller, S. Kurtz, F. Meyer, T. W. Nattkemper, and A. Becker. 2006. Construction of a large signature-tagged mini-Tn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti. Appl. Environ. Microbiol. 72:4329-4337.
48. Reed, J., J. Glazebrook, and G. C. Walker. 1991. The exoR gene of Rhizobium meliloti affects RNA levels of other exo genes but lacks homology to known transcriptional regulators. J. Bacteriol. 173:3789-3794.
49. Reuber, T. L., and G. C. Walker. 1993. Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74: 269-280.
50. Rinaudi, L., N. A. Fujishige, A. M. Hirsch, E. Banchio, A. Zorreguieta, and W. Giordano. 2006. Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res. Microbiol. 157:867-875.
51. Rotter, C., S. Muhlbacher, D. Salamon, R. Schmitt, and B. Scharf. 2006. Rem, a new transcriptional activator of motility and chemotaxis in Sinorhizobium meliloti. J. Bacteriol. 188:6932-6942.
52. Santaella, C., M. Schue, O. Berge, T. Heulin, and W. Achouak. 2008. The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ. Microbiol. 10:2150-2163.
53. Santos, R., D. Herouart, S. Sigaud, D. Touati, and A. Puppo. 2001. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant-Microbe Interact. 14:86-89.
54. Skorupska, A., M. Janczarek, M. Marczak, A. Mazur, and J. Król. 2006. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5:7.
55. Sola-Landa, A., J. Pizarro-Cerda, M. J. Grillo, E. Moreno, I. Moriyon, J. M. Blasco, J. P. Gorvel, and I. Lopez-Goni. 1998. A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Mol. Microbiol. 29:125-138.
56. Sourjik, V., P. Muschler, B. Scharf, and R. Schmitt. 2000. VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J. Bacteriol. 182:782-788.
57. Staehelin, C., L. S. Forsberg, W. D'Haeze, M. Y. Gao, R. W. Carlson, Z. P. Xie, B. J. Pellock, K. M. Jones, G. C. Walker, W. R. Streit, and W. J. Broughton. 2006. Exo-oligosaccharides of Rhizobium sp. strain NGR234 are required for symbiosis with various legumes. J. Bacteriol. 188:6168-6178.
58. Urzainqui, A., and G. C. Walker. 1992. Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants. J. Bacteriol. 174:3403-3406.
59. Vriezen, J. A., F. J. de Bruijn, and K. Nüsslein. 2007. Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl. Environ. Microbiol. 73:3451-3459.
60. Wang, L. X., Y. Wang, B. Pellock, and G. C. Walker. 1999. Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181:6788-6796.
61. Wells, D. H., E. J. Chen, R. F. Fisher, and S. R. Long. 2007. ExoR is genetically coupled to the ExoS-ChvI two-component system and located in the periplasm of Sinorhizobium meliloti. Mol. Microbiol. 64:647-664.
62. Yao, S. Y., L. Luo, K. J. Har, A. Becker, S. Ruberg, G. Q. Yu, J. B. Zhu, and H. P. Cheng. 2004. Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J. Bacteriol. 186:6042-6049.
63. Zhan, H. J., and J. A. Leigh. 1990. Two genes that regulate exopolysaccharide production in Rhizobium meliloti. J. Bacteriol. 172:5254-5259.