1887

Abstract

The phage-display cloning technique was used to find rhizobial proteins that bind to receptors located on the bacterial cell surface. The aim was to clone the gene(s) encoding rhicadhesin, a universal rhizobial adhesion protein, and/or other cell-surface-binding proteins. Four such -dhering roteins (Rap) were revealed in bv. strain R200. The binding is mediated by homologous Ra domains in these proteins. One member of the Rap protein family, named RapA1, is a secreted calcium-binding protein, which are also properties expected for rhicadhesin. However, the size of the protein (24 kDa instead of 14 kDa) and its distribution among different rhizobia (present in only biovars and instead of all members of ) argue against RapA1 being rhicadhesin. Protein RapA1 consists of two homologous Ra domains and agglutinates R200 cells by binding to specific receptors located at one cell pole during exponential growth. Expression of these cell-surface receptors was detected only in rhizobia that produce the RapA proteins. The authors propose that the homologous Ra domains, found to be present also in other proteins with different structure, represent lectin domains, which confer upon these proteins the ability to recognize their cognate carbohydrate structures.

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2001-03-01
2019-10-22
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References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment tool. J Mol Biol 215, 403-410.[CrossRef]
    [Google Scholar]
  2. Bhuvaneswari, T. V., Pueppke, S. G. & Bauer, W. D. ( 1977; ). Role of lectins in plant–microorganism interactions. I. Binding of soybean lectin to rhizobia. Plant Physiol 60, 486-491.[CrossRef]
    [Google Scholar]
  3. Bhuvaneswari, T. V., Mills, K. K., Crist, D. K., Evans, W. R. & Bauer, W. D. ( 1983; ). Effects of culture age on symbiotic infectivity of Rhizobium japonicum. J Bacteriol 153, 443-451.
    [Google Scholar]
  4. Dazzo, F. B. & Hubbell, D. H. ( 1975; ). Cross-reactive antigens and lectin as determinants of symbiotic specificity in the Rhizobium–clover association. Appl Microbiol 30, 1017-1033.
    [Google Scholar]
  5. Dazzo, F. B., Urbano, M. R. & Brill, W. J. ( 1979; ). Transient appearance of lectin receptors on Rhizobium trifolii. Curr Microbiol 2, 15-20.[CrossRef]
    [Google Scholar]
  6. Dazzo, F. B., Truchet, G. L., Sherwood, J. E., Hrabak, E. M. & Gardiol, A. E. ( 1982; ). Alteration of the trifoliin A-binding capsule of Rhizobium trifolii 0403 by enzymes released from clover roots. Appl Environ Microbiol 44, 478-490.
    [Google Scholar]
  7. Dazzo, F. B., Truchet, G. L., Sherwood, J. E., Hrabak, E. M., Abe, M. & Pankratz, S. H. ( 1984; ). Specific phases of root hair attachment in the Rhizobium trifoli–clover symbiosis. Appl Environ Microbiol 48, 1140-1150.
    [Google Scholar]
  8. Finnie, C., Hartley, N. M., Findlay, K. C. & Downie, J. A. ( 1997; ). The Rhizobium leguminosarum prsDE genes are required for secretion of several proteins, some of which influence nodulation, symbiotic nitrogen fixation and exopolysaccharide modification. Mol Microbiol 25, 135-146.[CrossRef]
    [Google Scholar]
  9. Finnie, C., Zorreguieta, A., Hartley, N. M. & Downie, J. A. ( 1998; ). Characterization of Rhizobium leguminosarum exopolysaccharide glycanases that are secreted via a type I exporter and have a novel heptapeptide repeat motif. J Bacteriol 180, 1691-1699.
    [Google Scholar]
  10. Glucksmann, M. A., Reuber, T. L. & Walker, G. C. ( 1993; ). Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175, 7045-7055.
    [Google Scholar]
  11. Ho, S. C., Wang, J. L. & Schindler, M. ( 1990; ). Carbohydrate binding activities of Bradyrhizobium japonicum. I. Saccharide-specific inhibition of homotypic and heterotypic adhesion. J Cell Biol 111, 1631-1638.[CrossRef]
    [Google Scholar]
  12. Ho, S. C., Wang, J. L., Schindler, M. & Loh, J. T. ( 1994; ). Carbohydrate binding activities of Bradyrhizobium japonicum. III. Lectin expression, bacterial binding, and nodulation efficiency. Plant J 5, 873-884.[CrossRef]
    [Google Scholar]
  13. Hrabak, E. M., Urbano, M. R. & Dazzo, F. B. ( 1981; ). Growth-phase-dependent immunodeterminants of Rhizobium trifolii lipopolysaccharide which bind trifoliin A, a white clover lectin. J Bacteriol 148, 697-711.
    [Google Scholar]
  14. Jacobsson, K. & Frykberg, L. ( 1995; ). Cloning of ligand-binding domains of bacterial receptors by phage display. Biotechniques 18, 878-885.
    [Google Scholar]
  15. Jacobsson, K. & Frykberg, L. ( 1996; ). Phage display shot-gun cloning of ligand-binding domains of prokaryotic receptors approaches 100% correct clones. Biotechniques 20, 1070-1076.
    [Google Scholar]
  16. Jacobsson, K. & Frykberg, L. ( 1999; ). Gene VIII-based, phage display vectors for selection against complex mixtures of ligands. In Expression Genetics: High-throughput Methods , pp. 225-238. Edited by M. McClelland & A. B. Pardee. Natick, MA:Eaton Publishing.
  17. Kijne, J. W., Smit, G., Diaz, C. L. & Lugtenberg, B. J. ( 1988; ). Lectin-enhanced accumulation of manganese-limited Rhizobium leguminosarum cells on pea root hair tips. J Bacteriol 170, 2994-3000.
    [Google Scholar]
  18. Lilie, H., Haehnel, W., Rudolph, R. & Baumann, U. ( 2000; ). Folding of a synthetic parallel beta-roll protein. FEBS Lett 470, 173-177.[CrossRef]
    [Google Scholar]
  19. Lodeiro, A. R., Lagares, A., Martinez, E. N. & Favelukes, G. ( 1995; ). Early interactions of Rhizobium leguminosarum bv phaseoli and bean roots – specificity in the process of adsorption and its requirement of Ca2+ and Mg2+ ions. Appl Environ Microbiol 61, 1571-1579.
    [Google Scholar]
  20. Loh, J. T., Ho, S. C., de Feijter, A. W., Wang, J. L. & Schindler, M. ( 1993; ). Carbohydrate binding activities of Bradyrhizobium japonicum: unipolar localization of the lectin BJ38 on the bacterial cell surface. Proc Natl Acad Sci USA 90, 3033-3037.[CrossRef]
    [Google Scholar]
  21. de Lorenzo, V., Herrero, M., Jakubzik, U. & Timmis, K. N. ( 1990; ). Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172, 6568-6572.
    [Google Scholar]
  22. Maruyama, K., Mikawa, T. & Ebashi, S. ( 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]
  23. Sambrook, J., Fritch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  24. Schäfer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. & Pühler, A. ( 1994; ). Small mobilizable multipurpose 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]
  25. Sherwood, J. E., Vasse, J. M., Dazzo, F. B. & Truchet, G. L. ( 1984; ). Development and trifoliin A-binding ability of the capsule of Rhizobium trifolii. J Bacteriol 159, 145-152.
    [Google Scholar]
  26. Smit, G., Kijne, J. W. & Lugtenberg, B. J. ( 1987; ). Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol 169, 4294-4301.
    [Google Scholar]
  27. Smit, G., Logman, T. J., Boerrigter, M. E., Kijne, J. W. & Lugtenberg, B. J. ( 1989; ). Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol 171, 4054-4062.
    [Google Scholar]
  28. Smit, G., Tubbing, D. M. J., Kijne, J. W. & Lugtenberg, B. J. J. ( 1991; ). Role of Ca2+ in the activity of rhicadhesin from Rhizobium leguminosarum biovar viciae, which mediates the first step in attachment of Rhizobiaceae cells to plant-root hair tips. Arch Microbiol 155, 278-283.[CrossRef]
    [Google Scholar]
  29. Smit, G., Swart, S., Lugtenberg, B. J. & Kijne, J. W. ( 1992; ). Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6, 2897-2903.[CrossRef]
    [Google Scholar]
  30. Štyriak, I., Laukova, A., Fallgren, C. & Wadström, T. ( 1999; ). Binding of selected extracellular matrix proteins to enterococci and Streptococcus bovis of animal origin. Curr Microbiol 39, 327-335.[CrossRef]
    [Google Scholar]
  31. Vasse, J. M., Dazzo, F. B. & Truchet, G. L. ( 1984; ). Re-examination of capsule development and lectin-binding sites on Rhizobium japonicum 3I1B110 by the glutaraldehyde/ruthenium red/uranyl acetate staining method. J Gen Microbiol 130, 3037-3047.
    [Google Scholar]
  32. Wisniewski, J. P. & Delmotte, F. M. ( 1996; ). Modulation of carbohydrate-binding capacities and attachment ability of Bradyrhizobium sp. (lupinus) to white lupin roots. Can J Microbiol 42, 234-242.[CrossRef]
    [Google Scholar]
  33. Zorreguieta, A., Finnie, C. & Downie, J. A. ( 2000; ). Extracellular glycanases of Rhizobium leguminosarum are activated on the cell surface by an exopolysaccharide-related component. J Bacteriol 182, 1304-1312.[CrossRef]
    [Google Scholar]
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