Three Genes Encoding for Putative Methyl- and Acetyltransferases Map Adjacent to the wzm and wzt Genes and Are Essential for O-Antigen Biosynthesis in Rhizobium etli CE3

Molecular Plant-Microbe Interactions

Volumn 16, Issue 12, 2003, Pages 1085-1093

  Lerouge, I ^a   Verreth, C ^a   Michiels, J ^a   Carlson, R W ^b   Datta, A ^b   Gao, M Y ^b   Vanderleyden, J ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Lipopolysaccharide (LPS)

Indexed keywords

AGROBACTERIUM; BACTERIA (MICROORGANISMS); PROKARYOTA; RHIZOBIUM; RHIZOBIUM ETLI;

EID: 0345581727     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2003.16.12.1085     Document Type: Article

References (49)

1. Allignet, J., and el Solh, N. 1995. Diversity among the gram-positive acetyltransferases inactivating streptogramin A and structurally related compounds and characterization of a new staphylococcal determinant, vatB. Antimicrob. Agents Chemother. 39:2027-2036.
2. Altschul, S. F., Gish, W., Milles, W., Yersand, E. W., and Ipman, D. J. 1990. Basic local alignment tool. J. Mol. Biol. 215:403-410.
3. Anderson, M. S., and Raetz, C. R. H. 1987. Biosynthesis of lipid A precursors in Escherichia coli. A cytoplasmic acyltransferase that converts UDP-N-acetylglucosamine to UDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine. J. Biol. Chem. 262:5159-5169.
4. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. 1987. Current Protocols in Molecular Biology. John Wiley and Sons, New York.
5. Baev, N., and Kondorosi, A. 1992. Nucleotide sequence of the Rhizobium meliloti nodL gene located in locus n5 of the nod regulon. Plant Mol. Biol. 18:843-846.
6. Berck, S., Perret, X., Quesada-Vincens, D., Prome, J., Broughton, W. J., and Jabbouri, S. 1999. NolL of Rhizobium sp. strain NGR234 is required for O-acetyltransferase activity. J. Bacteriol. 181:957-964.
7. Beringer, J. E. 1974. R-factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 120:421-429.
8. Bhat U. R., and Carlson, R. W. 1992. Chemical characterization of pH-dependent structural epitopes of lipopolysaccharides from Rhizobium leguminosarum biovar phaseoli. J. Bacteriol. 174:2230-2235.
9. Carlson, R. W., Reuhs, B., Chen, T. B., Bhat, U. R., and Noel, K. D. 1995. Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen. J. Biol. Chem. 270:11783-11788.
10. Cava, J. R., Elias, P. M., Turowski, D. A., and Noel, K. D. 1989. Rhizobium leguminosarum CFN42 genetic regions encoding lipopolysaccharide structures essential for complete nodule development on bean plants. J. Bacteriol. 171:8-15.
11. Cava, J. R., Tao, H., and Noel, K. D. 1990. Mapping of complementation groups within a Rhizobium leguminosarum CFN42 chromosomal region required for lipopolysaccharide synthesis. Mol. Gen. Genet. 221:125-128.
12. 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. Mol. Plant-Microbe Interact. 14:426-430.
13. Duelli, D. M., and Noel, K. D. 1997. Compounds exuded by Phaseolus vulgaris that induce a modification of Rhizobium etli lipopolysaccharide. Mol. Plant-Microbe Interact. 10:903-910.
14. Duelli, D. M., Tobin, A., Box, J. M., Kolli, V. S., Carlson, R. W., and Noel, K. D. 2001. Genetic locus required for antigenic maturation of Rhizobium etli CE3 lipopolysaccharide. J. Bacteriol. 183:6054-6064.
15. Forsberg, L. S., Bhat U. R., and Carlson, R. W. 2000. Structural characterization of the O-antigenic polysaccharide of the lipopolysaccharide from Rhizobium etli strain CE3. A unique O-acetylated glycan of discrete size, containing 3-O-methyl-6-deoxy-L-talose and 2,3,4-tri-O-methyl-1 fucose. J. Biol. Chem. 275:18851-18863.
16. Forsberg, L. S., and Carlson, R. W. 1998. The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359: The complete structure of the core region of R. etli lipopolysaccharides. J. Biol. Chem. 273:2747-2757.
17. Geelen, D., Mergaert, P., Geremia, R. A., Goormachtig, S., Van Montagu, M., and Holsters, M. 1993. Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: evidence that nodS encodes a methyltransferase involved in Nod factor modification. Mol. Microbiol. 9:145-154.
18. Herrero, M., L., V, and Timmis, K. N. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
19. Kagan, R. M., and Clarke, S. 1994. Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch. Biochem. Biophys. 310:417-427.
20. Kannenberg, E. L., and Carlson, R. W. 2000. Rhizobium Bacteroids Express Hydrophobic Lipopolysaccharides. Page 245 in: Nitrogen Fixation: From Molecules to Crop-Productivity. F. O. Pedrosa, M. Hungria, G. Yates, and W. E. Newton, eds. Foz do Iguacu, Parana, Brazil; Kluwer Academic Publisher, Dordrecht The Netherlands.
21. Kannenberg, E. L., and Carlson, R. W. 2001. Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become Hydrophobic during bacteroid development. Mol. Microbiol. 39:379-392.
22. Kannenberg, E. L., Reuhs, B. L., Forsberg, L. S., and Carlson, R. W. 1998. Lipopolysaccharides and K-antigens: Their structures, biosynthesis and functions. Pages 119-154 in: The Rhizobiaceae. H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Lerouge, I., Laeremans, T., Verreth, C., Vanderleyden, J., Van Soom, C., Tobin, A., and Carlson, R. W. 2001. Identification of an ATP-binding cassette transporter for export of the O-antigen across the inner membrane in Rhizobium etli based on the genetic, functional, and structural analysis of an lps mutant deficient in O-antigen. J. Biol. Chem. 276:17190-17198.
25. Lerouge, I., and Vanderleyden, J. 2002. O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 26:17-47.
26. Michiels, J., Moris, M., Dombrecht, B., Verreth, C., and Vanderleyden, J. 1998. Differential regulation of Rhizobium etli rpoN, gene expression during symbiosis and free-living growth. J. Bacteriol. 180:3620-3628.
27. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Press, Cold Spring Harbor, NY, U.S.A.
28. Nicholas, K. B., Nicholas, H. B., Jr., and Deerfield, D. W. 1997. GeneDoc: Analysis and visualization of genetic variation. EMBNEW News 4:14.
29. Noel, K. D., and Duelli, D. M. 2000. Rhizobium lipopolysaccharide and its role in symbiosis. Pages 415-431 in: Prokaryotic Nitrogen Fixation: A Model System for Analysis of a Biological Process. E. W. Triplett, ed. Horizon Scientific Press, Wymondham, U.K.
30. Noel, K. D., Forsberg, L. S., and Carlson, R. W. 2000. Varying the abundance of O antigen in Rhizobium etli and its effect on symbiosis with Phaseolus vulgaris. J. Bacteriol. 182:5317-5324.
31. Noel, K. D., Sanchez, A., Fernandez, L., Leemans, J., and Cevallos, M. A. 1984. Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J. Bacteriol. 182:5317-5324.
32. Paton, A. W., and Paton, J. C. 1999. Molecular characterization of the locus encoding biosynthesis of the lipopolysaccharide O antigen of Escherichia coli serotype O113. Infect. Immun. 67:5930-5937.
33. Payie, K. G., and Clarke, A. J. 1997. Characterization of gentamicin 2′-N-acetyltransferase from Providencia stuartii: its use of peptidoglycan metabolites for acetylation of both aminoglycosides and peptidoglycan. J. Bacteriol. 179:4106-4114.
34. Quandt, J., and Hynes, M. F. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
35. Raetz, C. R. H., and Roderick, S. L. 1995. A left-handed parallel β helix in the structure of UDP-N-Acetylglucosamine acyltransferase. Science 270:997-999.
36. Rather, P. N., Orosz, E., Shaw, K. J., Hare, R., and Miller, G. 1993. Characterization and transcriptional regulation of the 2′-N- acetyltransferase gene from Providencia stuartii. J. Bacteriol. 175:6492-6498.
37. Reeves, P. 1995. Role of O-antigen variation in the immune response. Trends Microbiol. 3:381-386.
38. Rocchetta, H. L., Burrows, L. L., and Lam, J. S. 1999. Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 63:523-553.
39. Rosemeyer, V., Michiels, J., Verreth, C., and Vanderleyden, J. 1998. luxI-and luxR-homologous genes of Rhizobium etli CNPAF512 contribute to synthesis of autoinducer molecules and nodulation of Phaseolus vulgaris. J. Bacteriol. 180:815-821.
40. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, NY, U.S.A.
41. Slauch, J. M., Mahan, M. J., Michetti, P., Neutra, M. R., and Mekalanos, J. J. 1995. Acetylation (O-factor 5) affects the structural and immunological properties of Salmonella typhimurium lipopolysaccharide O antigen. Infect Immun. 63:437-441.
42. Spaink, H. P. 2000. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54:257-288.
43. Stingele, F., Neeser, J. R., and Mollet, B. 1996. Identification and characterization of the eps (Exopolysaccharide) gene cluster from Streptococcus thermophilus Sfi6. J. Bacteriol. 178:1680-1690.
44. Surin, B. P., and Downie, J. A. 1988. Characterization of the Rhizobium leguminosarum genes nodLMN involved in efficient host-specific nodulation. Mol. Microbiol. 2:173-183.
45. Thompson, J. D., Higgins, D. G., and Gibson, T. J. 1994. CLUSTAL W - improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids. Res. 22:4673-4680.
46. Tsai, C. M., and Frasch, C. E. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115-119.
47. Valverde, C., Hozbor, D. F., and Lagares, A: 1997. Rapid preparation of affinity-purified lipopolysaccharide samples for electrophoretic analysis. Biotechniques 22:230-232, 234, 236.
48. Villalobos, M. A., Nava, N., Vazquez, M., and Quinto, C. 1994. Nucleotide sequence of the Rhizobium etli nodS gene. Gene 150:201-202.
49. Yanisch-Perron, C., Vieira, J., and Messing, J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.