Role of BacA in lipopolysaccharide synthesis, peptide transport, and nodulation by Rhizobium sp. strain NGR234

Journal of Bacteriology

Volumn 193, Issue 9, 2011, Pages 2218-2228

  Ardissone, Silvia ^a   Kobayashi, Hajime ^b,d   Kambara, Kumiko ^a   Rummel, Coralie ^a   Noel, K Dale ^c   Walker, Graham C ^b   Broughton, William J ^a,e   Deakin, William J ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MARQUETTE UNIVERSITY   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e BAM FEDERAL INSTITUTE FOR MATERIALS RESEARCH AND TESTING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; VERY LONG CHAIN FATTY ACID;

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; GENE BACA; GENE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TRANSPORT; RHIZOBIUM; SYMBIOSIS; WILD TYPE;

MEDICAGO; RHIZOBIUM; RHIZOBIUM SP.; SINORHIZOBIUM MELILOTI;

EID: 79955536823     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01260-10     Document Type: Article

References (55)

1. Ausubel, F. M., et al. (ed.). 1991. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
2. Basu, S. S., M. J. Karbarz, and C. R. Raetz. 2002. Expression cloning and characterization of the C28 acyltransferase of lipid A biosynthesis in Rhizobium leguminosarum. J. Biol. Chem. 277:28959-28971.
3. Beringer, J. E. 1974. R-factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:188-198.
4. 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.
5. Broughton, W. J., et al. 2006. Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strain NGR234-legume symbioses. J. Bacteriol. 188:3654-3663.
6. Broughton, W. J., S. Jabbouri, and X. Perret. 2000. Keys to symbiotic harmony. J. Bacteriol. 182:5641-5652.
7. Broughton, W. J., et al. 1986. Identification of Rhizobium plasmid sequences involved in recognition of Psophocarpus, Vigna, and other legumes. J. Cell Biol. 102:1173-1182.
8. Brozek, K. A., R. W. Carlson, and C. R. 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. Campbell, G. R., et al. 2003. Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J. Bacteriol. 185:3853-3862.
10. Campbell, G. R. O., 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. U. S. A. 99:3938-3943.
11. Cava, J. R., P. M. Elias, D. A. Turowski, and K. D. Noel. 1989. Rhizobium leguminosarum CFN42 genetic regions encoding lipopolysaccharide structures essential for complete nodule development on bean plants. J. Bacteriol. 171:8-15.
12. Deakin, W. J., and W. J. Broughton. 2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:312-320.
13. Den Herder, G., and M. Parniske. 2009. The unbearable naivety of legumes in symbiosis. Curr. Opin. Plant Biol. 12:491-499.
14. D'Haeze, W., and M. Holsters. 2004. Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol. 12:555-561.
15. 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.
16. Ferguson, G. P., et al. 2004. Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc. Natl. Acad. Sci. U. S. A. 101:5012-5017.
17. 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.
18. Ferguson, G. P., A. Jansen, V. L. Marlow, and G. C. Walker. 2006. BacAmediated bleomycin sensitivity in Sinorhizobium meliloti is independent of the unusual lipid A modification. J. Bacteriol. 188:3143-3148.
19. Ferguson, G. P., R. M. Roop, and G. C. Walker. 2002. Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope. J. Bacteriol. 184:5625-5632.
20. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652.
21. Fraysse, N., S. Jabbouri, M. Treilhou, F. Couderc, and V. Poinsot. 2002. Symbiotic conditions induce structural modifications of Sinorhizobium sp. NGR234 surface polysaccharides. Glycobiology 12:741-748.
22. Gibson, K. E., H. Kobayashi, and G. C. Walker. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441.
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. 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.
25. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
26. Ichige, A., and G. C. Walker. 1997. Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J. Bacteriol. 179:209-216.
27. Jones, K. M., H. Kobayashi, B. W. Davies, and G. C. Walker. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-633.
28. Kanipes, M. I., A. A. Ribeiro, S. Lin, R. J. Cotter, and C. R. Raetz. 2003. A mannosyl transferase required for lipopolysaccharide inner core assembly in Rhizobium leguminosarum. Purification, substrate specificity, and expression in Salmonella waaC mutants. J. Biol. Chem. 278:16356-16364.
29. Kannenberg, E. L., and R. W. Carlson. 2001. Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol. Microbiol. 39:379-391.
30. Karunakaran, R., et al. 2010. BacA is essential for bacteroid development in nodules of galegoid, but not phaseoloid, legumes. J. Bacteriol. 192:2920-2928.
31. Le Quéré, A. J.-L., et al. 2006. Structural characterization of a K-antigen capsular polysaccharide essential for normal symbiotic infection in Rhizobium sp. NGR234. J. Biol. Chem. 281:28981-28992.
32. Le Vier, K., R. W. Phillips, V. K. Grippe, R. M. Roop, and G. C. Walker. 2000. Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492-2493.
33. Le Vier, K., and G. C. Walker. 2001. Genetic analysis of the Sinorhizobium meliloti BacA protein: differential effects of mutations on phenotypes. J. Bacteriol. 183:6444-6453.
34. Long, S., S. McCune, and G. C. Walker. 1988. Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis. J. Bacteriol. 170:4257-4265.
35. Marlow, V. L., et al. 2009. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J. Bacteriol. 191:1519-1527.
36. Mergaert, P., et al. 2006. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl. Acad. Sci. U. S. A. 103:5230-5235.
37. Miller, W. G., J. H. Leveau, and S. E. Lindow. 2000. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol. Plant-Microbe Interact. 13: 1243-1250.
38. Noel, K. D., J. M. Box, and V. J. Bonne. 2004. 2-O-methylation of fucosyl residues of a rhizobial lipopolysaccharide is increased in response to host exudate and is eliminated in a symbiotically defective mutant. Appl. Environ. Microbiol. 70:1537-1544.
39. Noel, K. D., K. A. Vandenbosch, and B. Kulpaca. 1986. Mutations in Rhizobium phaseoli that lead to arrested development of infection threads. J. Bacteriol. 168:1392-1401.
40. Pueppke, S. G., and W. J. Broughton. 1999. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host-ranges. Mol. Plant-Microbe Interact. 12:293-318.
41. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127: 15-21.
42. Que, N. L., S. Lin, R. J. Cotter, and C. R. Raetz. 2000. Purification and mass spectrometry of six lipid A species from the bacterial endosymbiont Rhizobium etli. Demonstration of a conserved distal unit and a variable proximal portion. J. Biol. Chem. 275:28006-28016.
43. Que, N. L., A. A. Ribeiro, and C. R. Raetz. 2000. Two-dimensional NMR spectroscopy and structures of six lipid A species from Rhizobium etli CE3. Detection of an acyloxyacyl residue in each component and origin of the aminogluconate moiety. J. Biol. Chem. 275:28017-28027.
44. Reuhs, B. L., et al. 2005. Structural characterization of a flavonoid-inducible Pseudomonas aeruginosa A-band-like O antigen of Rhizobium sp. strain NGR234, required for the formation of nitrogen-fixing nodules. J. Bacteriol. 187:6479-6487.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis (ed.). 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Schäfer, A., et al. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73.
47. Scocchi, M., et al. 2009. The proline-rich antibacterial peptide Bac7 binds to and inhibits in vitro the molecular chaperone DnaK. Int. J. Pept. Res. Ther. 15:147-155.
48. 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.
49. Skorpil, et al. 2005. NopP, a phosphorylated effector of Rhizobium sp. strain NGR234, is a major determinant of modulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol. Microbiol. 57:1304-1317.
50. Stanley, J., D. N. Dowling, and W. J. Broughton. 1988. Cloning of hemA from Rhizobium sp. NGR234 and symbiotic phenotype of a gene-directed mutant in diverse legume genera. Mol. Gen. Genet. 215:32-37.
51. Tan, X. J., Y. Cheng, Y. X. Li, Y. G. Li, and J. C. Zhou. 2009. BacA is indispensable for successful Mesorhizobium-Astragalus symbiosis. Appl. Microbiol. Biotechnol. 84:519-526.
52. Van de Velde, W., et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122-1126.
53. 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.
54. Vedam, V., et al. 2003. A Rhizobium leguminosarum acpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J. Bacteriol. 185: 1841-1850.
55. Zahringer, U., et al. 1995. The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog. Clin. Biol. Res. 392:113-139.