The succinyl and acetyl modifications of succinoglycan influence susceptibility of succinoglycan to cleavage by the Rhizobium meliloti glycanases ExoK and ExsH

Journal of Bacteriology

Volumn 180, Issue 16, 1998, Pages 4184-4191

  York, Gregory M ^a   Walker, Graham C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; BACTERIAL POLYSACCHARIDE; GLUCAN SYNTHASE; SUCCINOGLYCAN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME METABOLISM; GENOTYPE; GLYCATION; MOLECULAR WEIGHT; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINORHIZOBIUM MELILOTI; STRUCTURE ANALYSIS;

EID: 0031858627     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.16.4184-4191.1998     Document Type: Article

References (46)

1. Aman, P., M. McNeil, L.-E. Franzen, A. G. Darvill, and P. Albersheim. 1981. Structural elucidation, using HPLC-MS and GLC-MS, of the acidic exopolysaccharide secreted by Rhizobium meliloti strain Rm1021. Carhohydr. Res. 95:263-282.
2. 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.
3. Becker, A., A. Kleickmann, W. Arnold, and A. Pühler. 1993. Analysis of the Rhizobium meliloti exoH, exoK, exoL fragment: ExoK shows homology to excreted endo-β 1,3-1,4 glucanases and ExoH resembles membrane proteins. Mol. Gen. Genet. 238:145-154.
4. Becker, A., A. Kleickmann, M. Keller, W. Arnold, and A. Pühler. 1993. Identification and analysis of the Rhizobium meliloti exoAMONP genes involved in exopolysaccharide biosynthesis and mapping of promoters located on the exoHKLAMONP fragment. Mol. Gen. Genet. 241:367-379.
5. Becker, A., A. Kleickmann, H. Küster, M. Keller, W. Arnold, and A. Pühler. 1993. Analysis of the Rhizobium meliloti genes exoU, exoV, exoW, exoT, and exoI involved in exopolysaccharide biosynthesis and nodule invasion: exoU and exoW probably encode glucosyltransferases. Mol. Plant-Microbe Interact. 6:735-744.
6. Becker, A., H. Küster, K. Niehaus, and A. Pühler. 1995. Extension of the Rhizobium meliloti succinoglycan biosynthesis gene cluster: identification of the exsA gene encoding an ABC transporter protein, and the exsβ gene which probably codes for a regulator of succinoglycan biosynthesis. Mol. Gen. Genet. 249:487-497.
7. Becker, A., K. Niehaus, and A. Pühler. 1995. Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated ExoP protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain. Mol. Microbiol. 16:191-203.
8. Becker, A., and A. Pühler. 1998. Specific amino acid substitutions in the proline-rich motif of the Rhizobium meliloti ExoP protein result in enhanced production of low-molecular-weight succinoglycan at the expense of high-molecular-weight succinoglycan. J. Bacteriol. 180:395-399.
9. Breedveld, M. W., L. P. T. M. Zevenhuizen, and A. J. B. Zehnder. 1990. Osmotically induced oligo-and polysaccharide synthesis by Rhizobium meliloti SU-47. J. Gen. Microbiol. 136:2511-2519.
10. Buendia, A. M., B. Enenkel, R. Köplin, K. Niehaus, W. Arnold, and A. Pühler. 1991. The Rhizobium meliloti exoZ/exoB fragment of megaplasmid 2: ExoB functions as a UDP-glucose-4-epimerase and ExoZ shows homology to NodX of Rhizobium leguminosarum biovar. viciae strain TOM. Mol. Microbiol. 5:1519-1530.
11. Burova, T. V., I. A. Golubeva, N. V. Grinberg, A. Y. Mashkevich, V. Y. Grinberg, A. I. Usov, L. Navarini, and A. Cesáro, 1996. Calorimetric study of the order-disorder conformational transition in succinoglycan. Biopolymers 39:517-529.
12. Doherty, D., J. A. Leigh, J. Glazebrook, and G. C. Walker. 1988. Rhizobium meliloti mutants that overproduce the R. meliloti acidic Calcofluor-binding exopolysaccharide. J. Bacteriol. 170:4249-4256.
13. Fidanza, M., M. Dentini, V. Crescenzi, and P. Del Vecchio. 1989. Influence of charged groups on the conformational stability of succinoglycan in dilute aqueous solution. Int. J. Biol. Macromol. 11:372-376.
14. 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.
15. 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.
16. Glucksmann, M. A., T. L. Reuber, and G. C. Walker. 1993. Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti. J. Bacteriol. 175:7033-7044.
17. 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.
18. 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.
19. González, J. E., C. E. Semino, L. E. Castellano-Torres, and G. C. Walker. Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbotically important exopolysaccharide of Rhizobium meliloti. Submitted for publication.
20. Gravanis, G., M. Milas, M. Rinaudo, and B. Tinland. 1987. Comparative behavior of the bacterial polysaccharides xanthan and succinoglycan. Carbohydr. Res. 160:259-265.
21. Greenwood, C. T., and E. A. Milne. 1968. Starch degrading and synthesizing enzymes: a discussion of their properties and action pattern. Adv. Carbohydr. Chem. 23:282-366.
22. Her, G.-R., J. Glazebrook, G. C. Walker, and V. N. Reinhold. 1990. Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm1021. Carbohydr. Res. 198:305-312.
23. Hollingsworth, R. I., M. Abe, J. E. Sherwood, and F. B. Dazzo. 1984. Bacteriophage-induced acidic heteropolysaccharide lyases that convert the acidic heteropolysaccharides of Rhizobium trifolii into oligosaccharide units. J. Bacteriol. 160:510-516.
24. Jansson, P.-E., L. Kenne, B. Lindberg, H. Ljunggren, U. Ruden, and S. Svensson. 1977. Demonstration of an octasaccharide repeating unit in the extracellular polysaccharide of R. meliloti by sequential degradation. J. Am. Chem. Soc. 99:3812-3815.
25. Keller, M., A. Roxlau, W. M. Weng, M. Schmidt, J. Quandt, N. Karsten, D. Jording, W. Arnold, and A. Pühler. 1995. Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan. Mol. Plant-Microbe Interact. 8:267-277.
26. Kennedy, L., K. McDowell, and I. W. Sutherland. 1992. Alginases from Azotobacter species. J. Gen. Microbiol. 138:2465-2471.
27. Leigh, J. A., and C. C. Lee. 1988. Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. J. Bacteriol. 170:3327-3332.
28. Leigh, J. A., J. W. Reed, J. F. Hanks, A. M. Hirsch, and G. C. Walker. 1987. Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion. Cell 51:579-587.
29. Leigh, J. A., E. R. Signer, and G. C. Walker. 1985. Exopolysaccharide-deficient mutants of R. meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:6231-6235.
30. Lever, M. 1972. A new reaction for colorimetric determination of carbohydrates. Anal. Biochem. 47:273-279.
31. Loewus, F. A. 1952. Improvement in the anthrone method for determination of carbohydrates. Anal. Chem. 24:219.
32. 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.
33. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
34. Müller, P., M. Hynes, D. Kapp, K. Niehaus, and A. Pühler. 1988. Two classes of Rhizobium meliloti infection mutants differ in exopolysaccharide production and in coinoculation properties with nodulation mutants. Mol. Gen. Genet. 211:17-26.
35. Palmer, R. J., Jr., and D. C. White. 1997. Developmental biology of biofilms: implications for treatment and control. Trends Microbiol. 5:435-440.
36. Reed, J. W., M. Capage, and G. C. Walker. 1991. Rhizobium meliloti exoG and exoJ mutations affect the ExoX-ExoY system for modulation of exopolysaccharide production. J. Bacteriol. 173:3776-3788.
37. Reinhold, B. B., S. Y. Chan, T. L. Reuber, A. Marra, G. C. Walker, and V. N. Reinhold. 1994. Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021. J. Bacteriol. 176: 1997-2002.
38. Reuber, T. L., and G. C. Walker. 1993. The acetyl substituent of succinoglycan is not necessary for alfalfa nodule invasion by Rhizobium meliloti Rm1021. J. Bacteriol. 175:3653-3655.
39. Reuber, T. L., and G. C. Walker. 1993. Biosynthesis of succinoglcean, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74: 269-280.
40. Reuhs, B. L., R. W. Carlson, and J. S. Kim. 1993. Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-D-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J. Bacteriol. 175:3570-3580.
41. - phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide. J. Bacteriol. 177:4289-4296.
42. Ridout, M. J., G. J. Brownsey, G. M. York, G. C. Walker, and V. J. Morris. 1997. Effect of o-acyl substituents on the functional behavior of Rhizobium meliloti succinoglycan. Int. J. Biol. Macromol. 20:1-7.
43. Sutherland, I. W., and L. Kennedy. 1996. Polysaccharide lyases from gellan-producing Sphingomonas spp. Microbiology 142:867-872.
44. York, G. M., and G. C. Walker. 1997. The Rhizobium meliloti exoK gene and prsD/prsE/exsH genes are components of independent degradative pathways which contribute to production of low-molecular-weight succinoglycan. Mol. Microbiol. 25:117-134.
45. York, G. M., and G. C. Walker. 1998. The Rhizobium meliloti ExoK and ExsH glycanases specifically depolymerize nascent succinoglyean chains. Proc. Natl. Acad. Sci. USA 95:4912-4917.
46. Zevenhuizen, L. P. T. M., and A. R. W. van Neerven. 1983. (1-2)-β-D-Glucan and acidic oligosaccharides produced by Rhizobium meliloti. Carbohydr. Res. 118:127-134.