An acpXL mutant of Rhizobium leguminosarum bv. phaseoli lacks 27-hydroxyoctacosanoic acid in its lipid a and is developmentally delayed during symbiotic infection of the determinate nodulating host plant Phaseolus vulgaris

Journal of Bacteriology

Volumn 193, Issue 18, 2011, Pages 4766-4778

  Brown, Dusty B ^a   Huang, Yu Chu ^b   Kannenberg, Elmar L ^a   Sherrier, D Janine ^b   Carlson, Russell W ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

27 HYDROXYOCTACOSANOIC ACID; BACTERIAL PROTEIN; DEOXYCHOLIC ACID; DODECYL SULFATE; LIPID A; POLYMYXIN B; PROTEIN ACPXL; SODIUM CHLORIDE; UNCLASSIFIED DRUG; VERY LONG CHAIN FATTY ACID;

ARTICLE; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE LOCATION; GENE MUTATION; MASS FRAGMENTOGRAPHY; MEMBRANE STABILIZATION; NONHUMAN; PHASEOLUS VULGARIS; PHENOTYPE; PRIORITY JOURNAL; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM PHASEOLI; SALT TOLERANCE; STRUCTURE ANALYSIS; SYMBIOSIS;

ACYL CARRIER PROTEIN; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHROMATOGRAPHY, GAS; DEOXYCHOLIC ACID; DETERGENTS; HYDROXY ACIDS; LIPID A; MASS SPECTROMETRY; MICROSCOPY, ELECTRON; PHASEOLUS; POLYMYXIN B; RHIZOBIUM LEGUMINOSARUM; SODIUM DODECYL SULFATE; SYMBIOSIS; VIRULENCE;

BACTERIA (MICROORGANISMS); BARTONELLA HENSELAE; BRUCELLA MELITENSIS; BRUCELLA MELITENSIS BIOVAR ABORTUS; FABACEAE; LEGIONELLA PNEUMOPHILA; NEGIBACTERIA; PHASEOLUS VULGARIS; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM LEGUMINOSARUM BV. PHASEOLI;

EID: 80052536962     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00392-11     Document Type: Article

References (41)

1. Basu, S. S., M. J. Karbarz, and C. R. H. Raetz. 2002. Expression cloning and characterization of the C28 acyltransferase of lipid A biosynthesis in Rhizobium leguminosarum. J. Biol. Chem. 277:28959-28971.
2. Basu, S. S., K. A. White, N. L. S. Que, and C. R. H. Raetz. 1999. A deacylase in Rhizobium leguminosarum membranes that cleaves the 3-O-linked beta-hydroxymyristoyl moiety of lipid A precursors. J. Biol. Chem. 274:11150-11158.
3. Becker, A., M. Schmidt, W. Jäger, and A. Pühler. 1995. New gentamicinresistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene 162:37-39.
4. Beedveld, M. W., and Karen J. Miller. 1998. Cell surface β-glucans. In H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas (ed.), The Rhizobiaceae: molecular biology of model plant-associated bacteria. Kluwer Academic Publishers, Dordrecht, Netherlands.
5. Beringer, J. E. 1974. R factor transfer in Rhizobium leguminosarum. Microbiology 84:188.
6. Bhat, U. R., R. W. Carlson, M. Busch, and H. Mayer. 1991. Distribution and phylogenetic significance of 27-hydroxy-octacosanoic acid in lipopolysaccharides from bacteria belonging to the alpha-2 subgroup of Proteobacteria. Int. J. Syst. Bacteriol. 41:213-217.
7. Bhat, U. R., L. S. Forsberg, and R. W. Carlson. 1994. Structure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. Unique nonphosphorylated lipid A containing 2-amino-2-deoxygluconate, galacturonate, and glucosamine. J. Biol. Chem. 269:14402.
8. Brozek, K. A., R. W. Carlson, and C. R. H. Raetz. 1996. A special acyl carrier protein for transferring long hydroxylated fatty acids to lipid A in Rhizobium. J. Biol. Chem. 271:32126-32136.
9. Brozek, K. A., J. L. Kadrmas, and C. R. H. Raetz. 1996. Lipopolysaccharide biosynthesis in Rhizobium leguminosarum: novel enzymes that process precursors containing 3-deoxy-D-manno-octulosonic acid. J. Biol. Chem. 271: 32112-32118.
10. Carlson, R. W. 1984. Heterogeneity of Rhizobium lipopolysaccharides. J. Bacteriol. 158:1012-1017.
11. Carlson, R. W., L. S. Forsberg, and E. L. Kannenberg. 2010. Lipopolysaccharides in Rhizobium-legume symbioses, p. 339-386. In P. J. Quinn and X. Wang (ed.), Subcellular biochemistry. Endotoxins: structure, function and recognition, vol. 53. Springer, New York, NY.
12. D'Haeze, W., C. Leoff, G. Freshour, K. D. Noel, and R. W. Carlson. 2007. Rhizobium etli CE3 bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J. Biol. Chem. 282:17101-17113.
13. Fahraeus, G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16:374-381.
14. Ferguson, G. P., A. Datta, R. W. Carlson, and G. C. Walker. 2005. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol. Microbiol. 56:68-80.
15. Fraysse, N., F. Couderc, and V. Poinsot. 2003. Surface polysaccharide involvement in establishing the Rhizobium/legume symbiosis. Eur. J. Biochem. 270:1365-1380.
16. Geurtsen, J., L. Steeghs, J. T. Hove, P. van der Ley, and J. Tommassen. 2005. Dissemination of lipid A deacylases (PagL) among gram-negative bacteria. J. Biol. Chem. 280:8248-8259.
17. Gudlavalleti, S. K., and L. S. Forsberg. 2003. Structural characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. J. Biol. Chem. 278:3957-3968.
18. Haag, A. F., et al. 2009. The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J. Bacteriol. 191:4681-4686.
19. Hoang, T. T., R. A. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
20. Kannenberg, E. L., and N. J. Brewin. 1994. Host-plant invasion by Rhizobium: the role of cell-surface components. Trends Microbiol. 2:277-283.
21. Kawasaki, K., R. K. Ernst, and S. I. Miller. 2004. 3-O-Deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 279:20044-20048.
22. Kittelberger, R., and F. Hilbink. 1993. Sensitive silver-staining detection of bacterial lipopolysaccharides in polyacrylamide gels. J. Biochem. Biophys. Methods 26:81-86.
23. Kovach, M. E., et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
24. Lamb, J. W., G. Hombrecher, and A. W. B. Johnston. 1982. Plasmid-determined nodulation and nitrogen-fixation abilities in Rhizobium phaseoli. Mol. Gen. Genet. 186:449-452.
25. Mollenhauer, H. H. 1964. Plastic embedding mixture for use in electron microscope. Stain Technol. 39:111-114.
26. Oldroyd, G. E. D., and J. A. Downie. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59:519-546.
27. Phadnis, S. H., and H. K. Das. 1987. Use of the plasmid pRK 2013 as a vehicle for transposition in Azotobacter vinelandii. J. Biosci. 12:131-135.
28. Que-Gewirth, N. L. S., M. J. Karbarz, S. R. Kalb, R. J. Cotter, and C. R. H. Raetz. 2003. Origin of the 2-amino-2-deoxy-gluconate unit in Rhizobium leguminosarum lipid A. J. Biol. Chem. 278:12120-12129.
29. Que-Gewirth, N. L. S., S. Lin, R. J. Cotter, and C. R. H. Raetz. 2003. An outer membrane enzyme that generates the 2-amino-2-deoxy-gluconate moiety of Rhizobium leguminosarum lipid A. J. Biol. Chem. 278:12109-12119.
30. Raetz, C. R. H., C. M. Reynolds, M. S. Trent, and R. E. Bishop. 2007. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76:295-329.
31. 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.
32. Ryan, J. M., and H. E. Conrad. 1974. Structural heterogeneity in the lipopolysaccharide of Salmonella newington. Arch. Biochem. Biophys. 162:530-536.
33. Sharypova, L. A., K. Niehaus, H. Scheidle, O. Holst, and A. Becker. 2003. Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J. Biol. Chem. 278:12946-12954.
34. Van de Velde, W., et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122-1126.
35. Vanderlinde, E. M., et al. 2009. Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155:3055-3069.
36. Vedam, V., J. G. Haynes, E. L. Kannenberg, R. W. Carlson, and D. J. Sherrier. 2004. A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol. Plant Microbe Interact. 17:283-291.
37. Vedam, V., et al. 2006. The pea nodule environment restores the ability of a Rhizobium leguminosarum lipopolysaccharide acpXL mutant to add 27-hydroxyoctacosanoic acid to its lipid A. J. Bacteriol. 188:2126-2133.
38. Vedam, V., et al. 2003. A Rhizobium leguminosarum acpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J. Bacteriol. 185: 1841-1850.
39. Westphal, O., and K. Jann. 1965. Endotoxins: extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5: 83-91.
40. White, S. W., J. Zheng, Y.-M. Zhang, and C. O. Rock. 2005. The structural biology of type II fatty acid biosynthesis. Annu. Rev. Biochem. 74:791-831.
41. York, W. S., A. G. Darvill, M. McNeil, T. T. Stevenson, and P. Albersheim. 1986. Isolation and characterization of plant-cell walls and cell-wall components. Methods Enzymol. 118:3-40.