Lipoprotein PssN of Rhizobium leguminosarum bv. trifolii: Subcellular localization and possible involvement in exopolysaccharide export

Journal of Bacteriology

Volumn 188, Issue 19, 2006, Pages 6943-6952

  Marczak, Małgorzata ^a   Mazur, Andrzej ^a   Król, Jarosław E ^a   Gruszecki, Wiesław I ^a   Skorupska, Anna ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; EXOPOLYSACCHARIDE; FLUORESCEIN ISOTHIOCYANATE; HISTIDINE; LIPOPROTEIN; MONOMER; OLIGOMER; OUTER MEMBRANE PROTEIN; PALMITIC ACID; PROTEIN PSSN; PROTEINASE; UNCLASSIFIED DRUG;

ACYLATION; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BETA SHEET; CELL MEMBRANE; CELLULAR DISTRIBUTION; CENTRIFUGATION; CROSS LINKING; CYTOPLASM; ESCHERICHIA COLI; FRACTIONATION; GENE FUSION; GENE IDENTIFICATION; GRAM NEGATIVE BACTERIUM; IMMUNOFLUORESCENCE; INFRARED SPECTROSCOPY; LACZ GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PHENOTYPE; PHOA GENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; PSSN GENE; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM TRIFOLII; SPHEROPLAST; SUCROSE GRADIENT;

ARTIFICIAL GENE FUSION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BIOLOGICAL TRANSPORT; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; LIPOPROTEINS; MOLECULAR WEIGHT; PERIPLASMIC PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; POLYSACCHARIDES, BACTERIAL; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; RHIZOBIUM LEGUMINOSARUM; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STAINING AND LABELING;

NEGIBACTERIA; RHIZOBIUM LEGUMINOSARUM BV. TRIFOLII;

EID: 33749350775     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00651-06     Document Type: Article

References (75)

1. Bagos, P. G., T. D. Liakopoulos, I. C. Spyropoulos, and S. J. Hamodrakas. 1 July 2004. PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res. 32:W400-W404. [Online.] doi:10.1093/nar/gkh417.
2. Becker, A., and A. Pühler. 1998. Production of exopolysaccharides, p. 97-118. In H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas (ed.), Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands.
3. Beringer, J. E., N. Brewin, A. W. Johnston, H. M. Schulman, and D. A. Hopwood. 1979. The Rhizobium-legume symbiosis. Proc. R. Soc. Lond. B Biol. Sci. 204:219-233.
4. Bhasin, M., A. Garg, and G. P. S. Raghava. 2005. PSLpred: prediction of subcellular localization of bacterial proteins. Bioinformatics 21:2522-2524.
5. Bliss, J. M., and R. P. Silver. 1996. Coating the surface: a model for expression of capsular polysialic acid in Escherichia coli K1. Mol. Microbiol. 21: 221-231.
6. Bugert, P., and K. Geider. 1995. Molecular analysis of the ams operon required for exopolysaccharide synthesis of Erwinia amylovora. Mol. Microbiol. 15:917-933.
7. Byler, D. M., and H. Susi. 1986. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25:469-487.
8. Chakravorty, A. K., W. Żurkowski, J. Shine, and B. G. J. Rolfe. 1982. Symbiotic nitrogen fixation: molecular cloning of Rhizobium genes involved in exopolysaccharide synthesis and effective nodulation. J. Mol. Appl. Genet. 1:585-596.
9. Chopra, I., and S. W. Shales. 1980. Comparison of the polypeptide composition of Escherichia coli outer membranes prepared by two methods. J. Bacteriol. 144:425-427.
10. de Maagd, R. A., R. de Rijk, I. H. M. Mulders, and B. J. J. Lugtenberg. 1989. Immunochemical characterization of Rhizobium leguminosarum outer membrane antigens by use of polyclonal and monoclonal antibodies. J. Bacteriol. 171:1136-1142.
11. Drummelsmith, J., and C. Whitfield. 1999. Gene products required for surface expression of the capsular form of the group 1 K antigen in Escherichia coli (O9a:K30). Mol. Microbiol. 31:1321-1332.
12. Drummelsmith, J., and C. Whitfield. 2000. Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J. 19:57-66.
13. Eisenhaber, F., F. Imperiale, P. Argos, and C. Frommel. 1996. Prediction of secondary structural content of proteins from their amino acid composition alone. I. New analytic vector decomposition methods. Proteins 25:157-168.
14. Filip, C., G. Fletcher, J. L. Wulff, and C. F. Earhart. 1973. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 115:717-722.
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. Frosch, M., D. Müller, K. Bousset, and A. Müller. 1992. Conserved outer membrane protein of Neisseria meningitidis involved in capsule expression. Infect. Immun. 60:798-803.
17. Gardy, J. L., M. R. Laird, F. Chen, S. Rey, C. J. Walsh, M. Ester, and F. S. L. Brinkman. 2005. PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21:617-623.
18. Garg, B., R. C. Dogra, and P. K. Sharma. 1999. High-efficiency transformation of Rhizobium leguminosarum by electroporation. Appl. Environ. Microbiol. 65:2802-2804.
19. Giacomini, A., F. J. Ollero, A. Squartini, and M. P. Nuti. 1994. Construction of multipurpose gene cartridges based on a novel synthetic promoter for high-level expression in Gram-negative bacteria. Gene 144:17-24.
20. Glenn, A. R., P. S. Poole, and J. F. Hudman. 1980. Succinate uptake by free-living and bacteroid forms of Rhizobium leguminosarum. J. Gen. Microbiol. 119:267-271.
21. Gonzalez, J. E., C. E. Semino, L. Wang, L. E. Castellano-Torres, and G. C. Walker. 1998. Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 95: 13477-13482.
22. Guy-Caffey, J. K., M. P. Rapoza, K. A. Jolley, and R. E. Webster. 1992. Membrane localization and topology of a viral assembly protein. J. Bacteriol. 174:2460-2465.
23. Hashimoto, Y., N. Li, H. Yokoyama, and T. Ezaki. 1993. Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. S. Bacteriol. 175:4456-4465.
24. Hu, N. T., M. N. Hung, C. T. Liao, and M. H. Lin. 1995. Subcellular location of XpsD, a protein required for extracellular protein secretion by Xanthomonas campestris pv. campestris. Microbiology 141:1395-1406.
25. Huang, J., and M. Schell. 1995. Molecular characterization of the eps gene cluster of Pseudomonas solanacearum and its transcriptional regulation at a single promoter. Mol. Microbiol. 16:977-989.
26. Janczarek, M., and A. Skorupska. 2001. The Rhizobium leguminosarum bv. trifolii pssB gene product is an inositol monophosphatase that influences exopolysaccharide synthesis. Arch. Microbiol. 175:143-151.
27. Janczarek, M., J. Król, J. Kutkowska, A. Mazur, J. Wielbo, W. Borucki, J. Kopcińska, B. Łotocka, T. Urbanik-Sypniewska, and A. Skorupska. 2001. Mutation in the pssB-pssA intergenic region of Rhizobium leguminosarum bv. trifolii affects the surface polysaccharides biosynthesis and nitrogen fixation ability. J. Plant Physiol. 158:1565-1574.
28. Jarvis, B. D. W., C. E. Pankhurst, and J. J. Patel. 1982. Rhizobium loti, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 32:378-380.
29. Jayakumar, A., I. Schulman, D. McNeil, and E. M. Barnes, Jr. 1986. Role of the Escherichia coli glnALG operon in regulation of ammonium transport. J. Bacteriol. 166:281-284.
30. Juncker, A. S., H. Willenbrock, G. von Heijne, S. Brunak, H. Nielsen, and A. Krogh. 2003. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12:1652-1662.
31. Katzen, F., A. Becker, M. V. Ielmini, C. G. Oddo, and L. Ielpi. 1999. New mobilizable vectors suitable for gene replacement in gram-negative bacteria and their use in mapping of the 3′ end of the Xanthomonas campestris pv. campestris gum operon. Appl. Environ. Microbiol. 65:278-282.
32. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239-253.
33. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
34. Król, J. E., J. Wielbo, A. Mazur, J. Kopcińska, B. Łotocka, W. Golinowski, and A. Skorupska. 1998. Molecular characterization of pssCDE genes of Rhizobium leguminosarum bv. trifolii strain TA1: pssD mutant is affected in exopolysaccharide synthesis and endocytosis of bacteria. Mol. Plant-Microbe Interact. 11:1142-1148.
35. Kroll, J. S., B. Loynds, L. N. Brophy, and E. R. Moxon. 1990. The bex locus in encapsulated Haemophilus influenzae: a chromosomal region involved in capsule polysaccharide export. Mol. Microbiol. 4:1853-1862.
36. Kuykendall, L. D., and G. H. Elkan. 1976. Rhizobium japonicum derivatives differing in nitrogen-fixing efficiency and carbohydrate utilization. Appl. Environ. Microbiol. 32:511-519.
37. Lattemann, C. T., J. Maurer, E. Gerland, and T. F. Meyer. 2000. Autodisplay: functional display of active β-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J. Bacteriol. 182:3726-3733.
38. Leduc, M., K. Ishidate, N. Shakibai, and L. Rothfield. 1992. Interactions of Escherichia coli membrane lipoproteins with the murein sacculus. J. Bacteriol. 174:7982-7988.
39. Madan Babu, M., and K. Sankaran. 2002. DOLOP-database of bacterial lipoproteins. Bioinformatics 18:641-643,
40. Manoil, C. 1991. Analysis of membrane protein topology using alkaline phosphatase and beta-galactosidase gene fusions. Methods Cell Biol. 34:61-75.
41. Mazur, A., J. E. Król, and A. Skorupska. 2001. Isolation and sequencing of Rhizobium leguminosarum bv. trifolii pssN, pssO and pssP genes encoding the proteins involved in polymerization and translocation of exopolysaccharide. DNA Seq. 12:1-12.
42. Mazur, A., J. Król, M. Marczak, and A. Skorupska. 2003. Membrane topology of PssT, the transmembrane protein component of the type I exopolysaccharide transport system in Rhizobium leguminosarum bv. trifolii strain TA1. J. Bacteriol. 185:2503-2511.
43. Mazur, A., J. E. Król, J. Wielbo, T. Urbanik-Sypniewska, and A. Skorupska. 2002. Rhizobium leguminosarum bv. trifolii PssP protein is required for exopolysaccharide biosynthesis and polymerization. Mol. Plant-Microbe Interact. 15:388-397.
44. Mazur, A., M. Marczak, J. Król, and A. Skorupska. 2005. Topological and transcriptional analysis of pssL gene product: a putative Wzx-like exopolysaccharide translocase in Rhizobium leguminosarum bv. trifolii TA1. Arch. Microbiol. 184:1-10.
45. McNulty, C., J. Thompson, B. Barrett, L. Lord, C. Andersen, and I. S. Roberts. 2006. The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol. Microbiol. 59:907-922.
46. E, an Escherichia coli heat-inducible σ factor, is modulated by expression of outer membrane proteins. Genes Dev. 7:2618-2628.
47. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Minton, N. P. 1984. Improved plasmid vectors for the isolation of translational lac gene fusions. Gene 31:269-273.
49. Nesper, J., C. M. D. Hill, A. Paiment, G. Harauz, K. Beis, J. H. Naismith, and C. Whitfield. 2003. Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. J. Biol. Chem. 278:49763-49772.
50. Niemeyer, D., and A. Becker. 2001. The molecular weight distribution of succinoglycan produced by Sinorhizobium meliloti is influenced by specific tyrosine phosphorylation and ATPase activity of the cytoplasmic domain of the ExoP protein. J. Bacteriol. 183:5163-5170.
51. Osborn, M. J., J. E. Gander, E. Parisi, and J. Garson. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. J. Biol. Chem. 247:3962-3972.
52. Paulsen, I. T., A. M. Beness, and M. H. Saier, Jr. 1997. Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology 143:2685-2699.
53. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence analysis. Proc. Natl. Acad. Sci. USA 85:2444-2448.
54. Peleg, A., Y. Shifrin, O. Ilan, C. Nadler-Yona, S. Nov, S. Koby, K. Baruch, S. Alluvia, M. Elgrably-Weiss, C. M. Abe, S. Knutton, M. A. Saper, and I. Rosenshine. 2005. Identification of an Escherichia coli operon required for formation of the O-antigen capsule. J. Bacteriol. 187:5259-5266.
55. Prossnitz, E., K. Nikaido, S. J. Ulbrich, and G. F. Ames. 1988. Formaldehyde and photoactivatable cross-linking of the periplasmic binding protein to a membrane component of the histidine transport system of Salmonella typhimurium. J. Biol. Chem. 263:17917-17920.
56. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
57. Pugsley, A. P., M. G. Kornacker, and A. Ryter. 1990. Analysis of the sub-cellular location of pullulanase produced by Escherichia coli carrying the pulA gene from Klebsiella pneumoniae strain UNF5023. Mol. Microbiol. 4:59-72.
58. Que-Gewirth, N. L., S. Lin, R. J. Cotter, and C. R. 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.
59. Reuber, T. L., and G. C. Walker. 1993. Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74: 269-280.
60. Rosenberg, C., and T. Huguet. 1984. The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction. Mol. Gen. Genet. 196:533-536.
61. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
62. Sankaran, K., and H. C. Wu. 1994. Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J. Biol. Chem. 269:19701-19706.
63. Segovia, L., J. P. W. Young, and E. Martinez-Romero. 1993. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43:374-377.
64. Seydel, A., P. Gounon, and A. P. Pugsley. 1999. Testing the '+2 rule' for lipoprotein sorting in the Escherichia coli cell envelope with a new genetic selection. Mol. Microbiol. 34:810-821.
65. Skare, J. T., B. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
66. Skorupska, A., U. Białek, T. Urbanik-Sypniewska, and A. van Lammeren. 1995. Two types of nodules induced on Trifolium pratense by mutants of Rhizobium leguminosarum bv. trifolii deficient in exopolysaccharide production. J. Plant Physiol. 147:93-100.
67. Skorupska, A., M. Janczarek, M. Marczak, A. Mazur, and J. Król. 2006. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5:7. [Online.] doi:10.1186/1475-2859-5-7.
68. Tamm, L. K., and S. A. Tatulian. 1997. Infrared spectroscopy of proteins and peptides in lipid bilayers. Q. Rev. Biophys. 30:365-429.
69. Vincent, J. M. 1941. Serological properties of the root-nodule bacteria. I. Strains of Rhizobium meliloti. Proc. Linn. Soc. N. S. W. 66:145-154.
70. von Heijne, G. 1990. The signal peptide. J. Membr. Biol. 115:195-201.
71. Ward, C. K., and T. J. Inzana. 1997. Identification and characterization of a DNA region involved in the export of capsular polysaccharide by Actinobacillus pleuropneumoniae serotype 5a. Infect. Immun. 65:2491-2496.
72. Whitfield, C., and A. Paiment. 2003. Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr. Res. 338:2491-2502.
73. Whitfield, C., and I. S. Roberts. 1999. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 31:1307-1319.
74. Wugeditsch, T., A. Paiment, J. Hocking, J. Drummelsmith, C. Forrester, and C. Whitfield. 2001. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem. 276:2361-2371.
75. Yu, C. S., C. J. Lin, and J. K. Hwang. 2004. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 13:1402-1406.