The Sinorhizobium meliloti ExpE1 protein secreted by a type I secretion system involving ExpD1 and ExpD2 is required for biosynthesis or secretion of the exopolysaccharide galactoglucan

References

1. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K.editors 1990 Current Protocols in Molecular Biology Vols 1 and 2 New York: Greene Publishing and Wiley Interscience;
   [Google Scholar]
2. Bakás L., Veiga M. P., Soloaga A., Ostolaza H., Goñi F. M. 1998; Calcium-dependent conformation of E. coli α-hemolysin: implications for the mechanism of membrane insertion and lysis. Biochim Biophys Acta 1368:225–234 [CrossRef]
   [Google Scholar]
3. Baumann U. 1994; Crystal structure of the 50 kDa metalloprotease from Serratia marcescens. J Mol Biol 242:244–251 [CrossRef]
   [Google Scholar]
4. Baumann U., Wu S., Flaherty K. M., McKay D. B. 1993; Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12:3357–3364
   [Google Scholar]
5. Becker A., Pühler A. 1998; Production of exopolysaccharides. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria pp. 97–118Edited by Spaink H. P., Kondorosi A., Hooykaas P. J. J. Dordrecht: Kluwer;
   [Google Scholar]
6. Becker A., Schmidt M., Jäger W., Pühler A. 1995; New gentamicin resistance and lacZ promoter probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene 162:37–39 [CrossRef]
   [Google Scholar]
7. Becker A., Rüberg S., Küster H., Roxlau A., Keller M., Ivashina T., Cheng H.-P., Walker G. C., Pühler A. 1997; The 32-kilobase exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: genetic organization and properties of the encoded gene products. J Bacteriol 179:1375–1384
   [Google Scholar]
8. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198 [CrossRef]
   [Google Scholar]
9. Beutler H. O. 1984; Lactose and d-galactose: UV method. In Methods of Enzymatic Analysis pp. 104–112Edited by Bergemeyer H. U. Weinheim: Verlag Chemie;
   [Google Scholar]
10. Binet R., Létoffé S., Ghigo J. M., Delepelaire P., Wandersman C. 1997; Protein secretion by Gram-negative bacterial ABC-exporters: a review. Gene 192:7–11 [CrossRef]
    [Google Scholar]
11. Bliss J. M., Silver R. P. 1996; Coating the surface: a model for expression of capsular polysialic acid in Escherichia coli K1. Mol Microbiol 21:221–231 [CrossRef]
    [Google Scholar]
12. Breedveld M. W., Miller K. J. 1994; Cyclic β-glucans of members of the family Rhizobiaceae. Microbiol Rev 58:145–161
    [Google Scholar]
13. Bullock W. C., Fernandez J. M., Short J. M. 1987; XL1-Blue: a high efficient plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 5:376–379
    [Google Scholar]
14. Casse F., Boucher C., Hulliot J. S., Michel M., Dénarié J. 1979; Identification and characterization of large plasmids in Rhizobium meliloti using agarose gel electrophoresis. J Bacteriol 113:229–242
    [Google Scholar]
15. Chaplin M. F., Kennedy S. F. 1986 Carbohydrate Analysis: a Practical Approach Washington DC: IRL Press;
    [Google Scholar]
16. Delepelaire P., Wandersman C. 1990; Protein secretion in Gram-negative bacteria: the extracellular metalloproteases from Erwinia chrysanthemi contains a C-terminal secretion signal analogous to that of Escherichia coli α-hemolysin. J Biol Chem 265:17118–17125
    [Google Scholar]
17. Dinh T., Paulsen I. T., Saier M. H. Jr 1994; A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J Bacteriol 176:3825–3831
    [Google Scholar]
18. Duong F., Lazdunski A., Cami B., Murgier M. 1992; Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: relationships to other secretory pathways. Gene 121:47–54 [CrossRef]
    [Google Scholar]
19. Duong F., Soscia C., Lazdunski A., Murgier M. 1994; The Pseudomonas fluorescens lipase has a C-terminal secretion signal and is secreted by a three-component bacterial ABC-exporter system. Mol Microbiol 11:1117–1126 [CrossRef]
    [Google Scholar]
20. Economou A., Hamilton W. D. O., Johnston A. W. B., Downie J. A. 1990; The Rhizobium nodulation gene nodO encodes a Ca²⁺-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J 9:349–354
    [Google Scholar]
21. Fath M. J., Kolter R. 1993; ABC transporters: bacterial exporters. Microbiol Rev 57:995–1017
    [Google Scholar]
22. Finan T. M., Hartwieg E., LeMieux K., Bergman K., Walker G. C., Signer E. R. 1984; General transduction in Rhizobium meliloti. J Bacteriol 159:120–124
    [Google Scholar]
23. Geelen D., Van Montagu M., Holsters M. 1995; Cloning of an Azorhizobium caulinodans endoglucanase gene and analysis of its role in symbiosis. Appl Environ Microbiol 61:3304–3310
    [Google Scholar]
24. Ghigo J.-M., Wandersman C. 1992; Cloning, nucleotide sequence and characterization of the gene encoding the Erwinia chrysanthemi B374 PtrA metalloprotease: a third metalloprotease secreted via a C-terminal secretion signal. Mol Gen Genet 236:135–144
    [Google Scholar]
25. Glazebrook J., Walker G. C. 1989; A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 56:661–672 [CrossRef]
    [Google Scholar]
26. Gonzáles J. E., Reuhs B. L., Walker G. C. 1996; Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc Natl Acad Sci USA 93:8636–8641 [CrossRef]
    [Google Scholar]
27. Harlow E., Lane D. 1988 Antibodies: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
28. Katzen F., Becker A., Ielmini M. V., Oddo C. G., Ielpi L. 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
    [Google Scholar]
29. Kaufman E., Geisler N., Weber K. 1984; SDS-PAGE strongly overestimates the molecular masses of the neurofilament proteins. FEBS Lett 170:81–84 [CrossRef]
    [Google Scholar]
30. Keller M., Roxlau A., Weng W. M., Schmidt M., Quandt J., Niehaus K., Jording D., Arnold W., Pühler A. 1995; Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan. Mol Plant-Microbe Interact 8:267–277 [CrossRef]
    [Google Scholar]
31. Kessler C. 1992 Nonradioactive Labelling and Detection of Biomolecules Berlin: Springer;
    [Google Scholar]
32. Kunst A., Draeger B., Zoegenhorn J. 1984; UV methods with hexokinase and glucose-6-phosphate dehydrogenase. In Methods of Enzymatic Analysis pp. 163–172, 3rd edn.. vol. 6Edited by Bergemeyer H. U. Weinheim: Verlag Chemie;
    [Google Scholar]
33. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
34. Leigh J. A., Walker G. C. 1994; Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet 10:63–67 [CrossRef]
    [Google Scholar]
35. Ludwig A., Jarchau T., Benz R., Goebel W. 1988; The repeat domain of Escherichia coli haemolysin (HlyA) is responsible for its Ca²⁺-dependent binding to erythrocytes. Mol Gen Genet 214:553–561 [CrossRef]
    [Google Scholar]
36. Mackman N., Nicaud J. M., Gray V., Holland I. B. 1986; Secretion of hemolysin by Escherichia coli. Curr Top Microbiol Immunol 125:159–181
    [Google Scholar]
37. Maina C. V., Riggs P. D., Grandea A. G., Slatko B. E., Moran L. S., Tagliamonte J. A., McReynolds L. A., Guan C. 1988; An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein. Gene 74:365–373 [CrossRef]
    [Google Scholar]
38. Maruyama K., Mikawa T., Ebashi K. 1984; Detection of calcium binding proteins by ⁴⁵Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis. J Biochem 95:511–519
    [Google Scholar]
39. Mateos P. F., Jimenez-Zurdo J. I., Chen J., Aquartini A. S., Haack S. K., Martinez-Molina E., Hubbell D. H., Dazzo F. B. 1992; Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 58:1816–1822
    [Google Scholar]
40. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149:114–122
    [Google Scholar]
41. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
42. Neidhardt F. C., Bloch P. L., Smith D. F. 1974; Culture medium for enterobacteria. J Bacteriol 119:736–747
    [Google Scholar]
43. Poxton I. R., Bell G. T., Barclay G. R. 1985; The association on SDS-polyacrylamide gels of lipopolysaccharide and outer membrane proteins of Pseudomonas aeruginosa as revealed by monoclonal antibodies and western blotting. FEMS Microbiol 27:247–251 [CrossRef]
    [Google Scholar]
44. Priefer U. B., Simon R., Pühler A. 1985; Extension of the host range of Escherichia coli vectors by incorporation of RSF1010 replication and mobilization functions. J Bacteriol 163:324–330
    [Google Scholar]
45. Reinhold B. B., Chan S. Y., Reuber T. L., Marra A., Walker G. C., Reinhold V. N. 1994; Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021. J Bacteriol 176:1997–2002
    [Google Scholar]
46. Reuber T. L., Walker G. C. 1993; Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74:269–280 [CrossRef]
    [Google Scholar]
47. Rose T., Sebo P., Bellalou J., Ladant D. 1995; Interaction of calcium with Bordetella pertussis adenylate cyclase toxin: characterization of multiple calcium-binding sites and calcium-induced conformational changes. J Biol Chem 270:26370–26376 [CrossRef]
    [Google Scholar]
48. Rüberg S., Pühler A., Becker A. 1999; Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology 145:603–611 [CrossRef]
    [Google Scholar]
49. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
50. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A. 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 [CrossRef]
    [Google Scholar]
51. Schirmer F., Ehrt S., Hillen W. 1997; Expression, inducer spectrum, domain structure, and function of MopR, the regulator of phenol degradation in Acinetobacter calcoaceticus NCBI 8250. J Bacteriol 179:1329–1336
    [Google Scholar]
52. Sharypova L. A., Yurgel S. N., Keller M., Simarov B. V., Pühler A., Becker A. 1999; The eff-482 locus of Sinorhizobium meliloti CXM1-105 that influences symbiotic effectiveness consists of three genes encoding an endoglycanase, a transcriptional regulator and an adenylate cyclase. Mol Gen Genet 261:1032–1044 [CrossRef]
    [Google Scholar]
53. Simon R., Priefer U., Pühler A. 1983; A broad-host-range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1:784–791 [CrossRef]
    [Google Scholar]
54. Sutton J. M., Lea E. J. A., Downie J. A. 1994; The nodulation-signalling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91:9990–9994 [CrossRef]
    [Google Scholar]
55. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354 [CrossRef]
    [Google Scholar]
56. Wang L.-X., Wang Y., Pellock B., Walker G. C. 1999; Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J Bacteriol 181:6788–6796
    [Google Scholar]
57. Weigerber C., Troy F. A. 1990; Biosynthesis of the polysialic acid capsule in Escherichia coli K1: the endogenous acceptor of polysialic acid is a membrane protein of 20 kDa. J Biol Chem 265:1578–1587
    [Google Scholar]
58. York G. M., Walker G. C. 1997; The Rhizobium meliloti exoK gene and prsD/prsE/exsH genes are components of independent degradative pathways which contribute to production of low-molecular-weight succinoglycan. Mol Microbiol 25:117–134 [CrossRef]
    [Google Scholar]
59. Zhan H., Levery S. B., Lee C. C., Leigh J. A. 1989; A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion. Proc Natl Acad Sci USA 86:3055–3059 [CrossRef]
    [Google Scholar]
60. Zhan H., Lee C. C., Leigh J. A. 1991; Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti strain SU47 by low phosphate concentrations. J Bacteriol 173:7391–7394
    [Google Scholar]