Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants

Journal of Bacteriology

Volumn 185, Issue 13, 2003, Pages 3853-3862

  Campbell, Gordon R O ^a   Sharypova, Larissa A ^b   Scheidle, Heiko ^b   Jones, Kathryn M ^a   Niehaus, Karsten ^b   Becker, Anke ^b   Walker, Graham C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; LIPOPOLYSACCHARIDE; PROTEIN DDHB; PROTEIN IPSB; PROTEIN IPSC; PROTEIN IPSE; QUEUINE; UNCLASSIFIED DRUG;

ALFALFA; ARTICLE; CARBOHYDRATE SYNTHESIS; CHEMOTAXIS; CONTROLLED STUDY; GENE INSERTION; GENE ISOLATION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC TRANSDUCTION; MOLECULAR WEIGHT; NONHUMAN; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; SINORHIZOBIUM MELILOTI; STRAIN DIFFERENCE; SYMBIOSIS;

ACETYLENE; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; CARBOHYDRATE METABOLISM; DNA TRANSPOSABLE ELEMENTS; LIPOPOLYSACCHARIDES; MEDICAGO; MEDICAGO SATIVA; MICROBIAL SENSITIVITY TESTS; MUTATION; OPEN READING FRAMES; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TRANSDUCTION, GENETIC;

INSERTION SEQUENCES; MEDICAGO; MEDICAGO SATIVA; NEGIBACTERIA; SINORHIZOBIUM; SINORHIZOBIUM MELILOTI; TRIFOLIUM;

EID: 0038039198     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.13.3853-3862.2003     Document Type: Article

References (55)

1. Allen, C. A., L. G. Adams, and T. A. Ficht. 1998. Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival. Infect. Immun. 66:1008-1016.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1994. Current protocol in molecular biology, vol. 1. John Wiley and Sons, Inc., New York, N.Y.
3. Barnett, M. J., R. F. Fisher, T. Jones, C. Komp, A. P. Abola, F. Barloy-Hubler, L. Bowser, D. Capela, F. Galibert, J. Gouzy, M. Gurjal, A. Hong, L. Huizar, R. W. Hyman, D. Kahn, M. L. Kahn, S. Kalman, D. H. Keating, C. Palm, M. C. Peck, R. Surzycki, D. H. Wells, K. C. Yeh, R. W. Davis, N. A. Federspiel, and S. R. Long. 2001. Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc. Natl. Acad. Sci. USA 98:9883-9888.
4. Borukhov, S., A. Polyakov, V. Nikiforov, and A. Goldfarb. 1992. GreA protein: a transcription elongation factor from Escherichia coli. Proc. Natl. Acad. Sci. USA 89:8899-8902.
5. 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.
6. Campbell, G. R. O., B. L. Reuhs, and G. C. Walker. 1998. Different phenotypic classes of Sinorhizobium meliloti mutants defective in synthesis of K antigen. J. Bacteriol. 180:5432-5436.
7. Campbell, J. A., G. J. Davies, V. Bulone, and B. Henrissat. 1997. A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326:929-939.
8. Capela, D., F. Barloy-Hubler, J. Gouzy, G. Bothe, F. Ampe, J. Batut, P. Boistard, A. Becker, M. Boutry, E. Cadieu, S. Dreano, S. Gloux, T. Godrie, A. Goffeau, D. Kahn, E. Kiss, V. Lelaure, D. Masuy, T. Pohl, D. Portetelle, A. Pühler, B. Purnelle, U. Ramsperger, C. Renard, P. Thebault, M. Vandenbol, S. Weidner, and F. Galibert. 2001. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. USA 98:9877 9882.
9. Cloeckaert, A., J. M. Verger, M. Grayon, M. S. Zygmunt, and O. Grepinet. 1996. Nucleotide sequence and expression of the gene encoding the major 25-kilodalton outer membrane protein of Brucella ovis: evidence for antigenic shift, compared with other Brucella species, due to a deletion in the gene. Infect. Immun. 64:2047-2055.
10. Cloeckaert, A., M. S. Zygmunt, G. Bezard, and G. Dubray. 1996. Purification and antigenic analysis of the major 25-kilodalton outer membrane protein of Brucella abortus. Res. Microbiol. 147:225-235.
11. Clover, R. H., J. Kieber, and E. R. Signer. 1989. Lipopolysaccharide mutants of Rhizobium meliloti are not defective in symbiosis. J. Bacteriol. 171:3961-3967.
12. De Vos, G. F., G. C. Walker, and E. R. Signer. 1986. Genetic manipulations in Rhizobium meliloti using two new transposon Tn5 derivatives. Mol. Gen. Genet. 204:485-49.
13. Djordjevic, S., and A. M. Stock. 1998. Structural analysis of bacterial chemotaxis proteins: components of a dynamic signaling system. J. Struct. Biol. 124:189-200.
14. Epand, R. M., and H. J. Vogel. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462:11-28.
15. Erie, D. A., O. Hajiseyedjavadi, M. C. Young, and P. H. von Hippel. 1993. Multiple RNA polymerase conformations and GreA: Control of the fidelity of transcription. Science 262:867-873.
16. Ernst, R. K., T. Guina, and S. I. Miller. 2001. Salmonella typhimurium outer membrane remodeling: Role in resistance to host innate immunity. Microbes Infect. 3:1327-1334.
17. Ferguson, G. P., R. M. Roop 1I, and G. C. Walker. 2002. Deficiency of Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of cell envelope. J. Bacteriol. 184:5625-5632.
18. Finan, T. M., E. K. Hartwieg, K. LeMieux, K. Bergman, G. C. Walker, and E. R. Signer. 1984. General transduction in Rhizobium meliloti. J. Bacteriol. 159:120-124.
19. Finan, T. M., S. Weidner, K. Wong, J. Buhmester, P. Chain, F. J. Vorhölter, I. Hernandez-Lucas, A. Becker, A. Cowie, J. Gouzy, B. Golding, and A. Pühler. 2001. The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymhiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 98:9889 9894.
20. Freer, E., J. Plzarro-Cerda, A. Weintraub, J. A. Bengoecbea, I. Moriyon, K. Hultenby, J. P. Gorvel, and E. Moreno. 1999. The outer membrane of Brucella ovis shows increased permeability to hydrophobic probes and is more susceptible to cationic peptides than are the outer membranes of mutant rough Brucella abortus strains. Infect. Immun. 67:6181-6186.
21. Galibert, F., T. M. Flnan, S. R. Long, A. Pühler P. Abola, F. Ampe, F. Barloy-Hubler, M. J. Barnett, A. Becker, P. Boistard, G. Botbe, M. Boutry, L. Bowser, J. Buhmester, 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. Porletelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vaodenbol, F. J. Vorhölter 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.
22. Genevaux, P., P. Bauda, M. S. DuBow, and B. Oudega. 1999. Identification of Tn10 insertions in the rfaG, rfaP, and galU genes involved in lipopolysaccharide core biosynthesis that affect Escherichia coli adhesion. Arch. Microbiol. 172:1-8.
23. Glazebrook, J., A. Ichige, and G. C. Walker. 1993. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev. 7:1485-1497.
24. Gunn, J. S., K. B. Lim, J. Krueger, K. Kim, L. Guo, M. Hackett, and S. I. Miller. 1998. PmrA-PmrB-regulated genes necessary for 4 -aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
25. Hanke, W., C. Methfessel, H. U. Wilmsen, E. Katz, G. Jung, and G. Boheim, 1983. Melittin and a chemically modified lrichotoxin form alamethicin-type multi-state pores. Biochim. Biophys. Acta 727:108-114.
26. Herrler, M., H. Bang, and M. A. Marahlel. 1994. Cloning and characterization of ppiB, a Bacillus subtilis gene which encodes a cyclosporin A-sensitive peptidyl-prolyl cis-trans isomerase. Mol. Microbiol. 11:1073-1083.
27. Kannenberg, E. L., B. L. Reuhs, L. S. Forsberg, and R. W. Carlson. 1998. Lipopolysaccharides and K-antigens: Their structures, biosynthesis, and functions. Kluwer Academic Publishers, Dordrechl, The Netherlands.
28. Kereszt, A., E. Kiss, B. L. Reuhs, R. W. Carlson, A. Kondorosi, and P. Putnoky. 1998. Novel rkp gene clusters of Sinorhizobium meliloti involved in capsular polysaccharide production and invasion of the symbiotic nodule: The rkpK gene encodes a UDP-glucose dehydrogenase. J. Bacteriol. 180:5426-5431.
29. Kessler, A. C., A. Haase, and P. R. Reeves. 1993. Molecular analysis of the 3,6-dideoxyhexose pathway genes of Yersinia pseudotuberculosis serogroup IIA. J. Bacteriol. 175:1412-1422.
30. Kushner, S. R. 1978. An improved method for transformation of Escherichia coli with ColEl derived plasmids. Elsevier, Amsterdam, The Netherlands.
31. Lagares, A., G. Caelano-Anolles, K. Niehaus, J. Lorenzen, H. D. Ljunggren, A. Pühler, and G. Favelukes. 1992. A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J. Bacteriol. 174:5941-5952.
32. Lagares, A., D. F. Hozbor, K. Niehaus, A. J. Otero, J. Lorenzen, W. Arnold, and A. Pühler. 2001. Genetic characterization of a Sinorhizobium meliloti chromosomal region in lipopolysaccharide biosynthesis. J. Bacteriol. 183:1248-1258.
33. 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. 82:6231-6235.
34. Lesse, A. J., A. A. Campagnari, W. E. Bittner, and M. A. Apicella. 1990. Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Immunol. Methods 126:109-117.
35. Martinez de Tejada, G., J. Pizarro-Cerda, E. Moreno, and I. Moriyon. 1995. The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect. Immun. 63:3054-3061.
36. Niehaus, K., and A. Becker. 1998. The role of microbial surface polysaccharides in the Rhizobium-legume interaction. Subcell. Biochem. 29:73-116.
37. Niebaus, K., A. Lagares, and A. Pühler. 1998. A Sinorhizobium meliloti lipopolysaccharide mutant induces effective nodules on the host plant Medicago sativa (alfalfa) but fails to establish a symbiosis with Medicago truncatula. Mol. Plant Microbe Interact. 11:906-914.
38. Noel, K. D., D. M. Duelli, H. Tao, and N. J. Brewin. 2000. Rhizobium lipopolysaccharide and its role in symbiosis, p. 415-431. In E. W. Triplett (ed.), Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific Press, Wymondham, United Kingdom.
39. Perez-Galdona, R., and M. L. Kahn. 1994. Effects of organic acids and low pH on Rhizobium meliloti 104A14. Microbiology. 140:1231-1235.
40. Perret, X., J. Parsons, V. Vlprey, K. Reichwald, and W. J. Broughton. 2001. Repeated sequences of Rhizobium sp, NGR234 and Sinorhizobium meliloti genomes - a comparative analysis using random sequencing. Can J. Microbiol. 47:548-558.
41. Pliyev, B. K., and B. Y. Gurvits. 1999. Peptidyl-prolyl cis-trans isomerases: Structure and functions. Biochemistry (Moscow) 64:738-751.
42. Prehm, P., G. Schmidt, and S. Stirm. 1976. On the mutations responsible for the rough phenotype of Escherichia coli B. J. Gen. Microbiol. 97:121-124.
43. Raetz, C. R., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
44. Reeves, P. R., M. Hobbs, M. A. Valvano, M. Skurnik, C. Whitfield, D. Coplin, N. Kido, J. Klena, D. Maskell, C. R. Raetz, and P. D. Rick. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4:495-503.
45. Reuter, K., R. Slany, F. Ullrich, and H. Kersten. 1991. Structure and organization of Escherichia coli genes involved in biosynthesis of the deazaguanine derivative queuine, a nutrient factor for eukaryotes. J. Bacteriol. 173:2256-2264.
46. Roest, H. P., I. H. Mulders, C. A. Wijffelman, and B. J. Lugtenberg. 1995. Isolation of ropB, a gene encoding a 22-kDa Rhizobium leguminosarum outer membrane protein. Mol. Plant-Microbe Interact. 8:576-583.
47. Srimal, S., N. Surolia, S. Balasubramanian, and A. Surolia. 1996. Titration calorimetric studies to elucidate the specificity of the interactions of polymyxin B with lipopolysaccharides and lipid A. Biochem. J. 315:679-686.
48. Teplova, M., V. Tereshko, R. Sanishvili, A. Joachimiak, T. Bushueva, W. F. Anderson, and M. Egli. 2000. The structure of the yrdC gene product from Escherichia coli reveals a new fold and suggests a role in RNA binding. Protein Sci. 9:2557-2566.
49. Thorson, J. S., S. F. Lo, O. Ploux, X. He, and H.-W. Liu. 1994. Studies of the biosynthesis of 3,6-dideoxyhexoses: Molecular cloning and characterization of the asc (ascarylose) region from Yersinia pseudotuberculosis serogroup VA. J. Bacteriol. 176:5483-5493.
50. Tsai, C., and C. E. Frisch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
51. Unger, T., Z. Oren, and Y. Shai. 2001. The effect of cyclization of magainin 2 and melittin analogues on structure, function, and model membrane interactions: Implication to their mode of action. Biochemistry 40:6388-A397.
52. Vaara, M. 1992. Agents that increase the permeability of the outer memhrane. Microbiol. Rev. 56:395-411.
53. Vinuesa, P., B. L. Reuhs, C. Breton, and D. Werner. 1999. identification of a plasmid-borne locus in Rhizobium etli KIM5s involved in lipopolysaccharide O-chain biosynthesis and nodulation of Phaseolus vulgaris. J. Bacteriol. 181:5606-5614.
54. Whitfield, C., and I. S. Roberts. 1999. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 31:1307-1319.
55. Yethon, J. A., J. S. Gunn, R. K. Ernst, S. I. Miller, L. Laroche, D. Malo, and C. Whitfield. 2000. Salmonella enterica serovar typhimurium waaP mutants show increased susceptibility to polymyxin and loss of virulence in vivo. Infect. Immun. 68:4485-4491.