RapA2 is a calcium-binding lectin composed of two highly conserved cadherin-like domains that specifically recognize rhizobium leguminosarum acidic exopolysaccharides

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2893-2904

  Abdian, Patricia L ^a   Caramelo, Julio J ^a,b   Ausmees, Nora ^c   Zorreguieta, Angeles ^a,b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; ARCHAEAL; BIOFILM FORMATION; BIOFILM MATRIX; CADHERINS; CALCIUM BINDING; CALCIUM IONS; CARBOHYDRATE BINDING; CELLULAR INTERACTION; CONSERVED PROTEINS; EXOPOLYSACCHARIDES; HOMO-OLIGOMERS; IN-SILICO; ISOTHERMAL TITRATION CALORIMETRY; PLANT ROOTS; PROTEIN MOLECULES; RHIZOBIUM LEGUMINOSARUM; STRUCTURAL SIMILARITY;

BACTERIA; BIOFILMS; CALCIUM; CIRCULAR DICHROISM SPECTROSCOPY; GLYCOPROTEINS; LIGHT SCATTERING; METABOLITES; OLIGOMERIZATION; OLIGOMERS; POLYSACCHARIDES;

PROTEINS;

CADHERIN; CALCIUM BINDING PROTEIN; CALCIUM ION; EXOPOLYSACCHARIDE; OLIGOMER; PROTEIN RAPA2; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CIRCULAR DICHROISM; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RHIZOBIUM LEGUMINOSARUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CADHERINS; CALCIUM; CALCIUM-BINDING PROTEINS; CALORIMETRY; LECTINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; RHIZOBIUM LEGUMINOSARUM; SEQUENCE HOMOLOGY, AMINO ACID; SOLVENTS;

EID: 84873823050     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.411769     Document Type: Article

References (56)

1. Downie, J. A. (2010) The roles of extracellular proteins, polysaccharides, and signals in the interactions of rhizobia with legume roots. FEMS Microbiol. Rev. 34, 150-170
2. Rinaudi, L. V., and Giordano, W. (2010) An integrated view of biofilm formation in rhizobia. FEMS Microbiol. Lett. 304, 1-11
3. Russo, D. M., Williams, A., Edwards, A., Posadas, D. M., Finnie, C., Dankert, M., Downie, J. A., and Zorreguieta, A. (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J. Bacteriol. 188, 4474-4486
4. Williams, A., Wilkinson, A., Krehenbrink, M., Russo, D. M., Zorreguieta, A., and Downie, J. A. (2008) Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J. Bacteriol. 190, 4706-4715
5. Krehenbrink, M., and Downie, J. A. (2008) Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae. BMC Genomics 9, 55
6. Ausmees, N., Jacobsson, K., and Lindberg, M. (2001) A unipolarly located, cell surface-associated agglutinin, RapA, belongs to a family of Rhizobiumadhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology 147, 549-559
7. Zorreguieta, A., Finnie, C., and 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
8. Mongiardini, E. J., Ausmees, N., Pérez-Giménez, J., Julia Althabegoiti, M., Ignacio Quelas, J., López-García, S. L., and Lodeiro, A. R. (2008) The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol. Ecol. 65, 279-288
9. Cao, L., Yan, X., Borysenko, C. W., Blair, H. C., Wu, C., and Yu, L. (2005) CHDL. A cadherin-like domain in Proteobacteria and Cyanobacteria. FEMS Microbiol. Lett. 251, 203-209
10. Nollet, F., Kools, P., and van Roy, F. (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299, 551-572
11. Fraiberg, M., Borovok, I., Bayer, E. A., Weiner, R. M., and Lamed, R. (2011) Cadherin domains in the polysaccharide-degrading marine bacterium Saccharophagus degradans 2-40 are carbohydrate binding modules. J. Bacteriol. 193, 283-285
12. Fraiberg, M., Borovok, I., Weiner, R. M., and Lamed, R. (2010) Discovery and characterization of cadherin domains in Saccharophagus degradans 2-40. J. Bacteriol. 192, 1066-1074
13. Dickens, N. J., Beatson, S., and Ponting, C. P. (2002) Cadherin-like domains in α-dystroglycan, α/ε-sarcoglycan, and yeast and bacterial proteins. Curr. Biol. 12, R197-R199
14. Young, J. P., Crossman, L. C., Johnston, A. W., Thomson, N. R., Ghazoui, Z. F., Hull, K. H., Wexler, M., Curson, A. R., Todd, J. D., Poole, P. S., Mauchline, T. H., East, A. K., Quail, M. A., Churcher, C., Arrowsmith, C., Cherevach, I., Chillingworth, T., Clarke, K., Cronin, A., Davis, P., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Mungall, K., Norbertczak, H., Rabbinowitsch, E., Sanders, M., Simmonds, M., Whitehead, S., and Parkhill, J. (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7, R34
15. Butcher, B. G., Lin, Y.-P., and Helmann, J. D. (2007) The yydFGHIJ operon of Bacillus subtilis encodes a peptide that induces the LiaRS two-component system. J. Bacteriol. 189, 8616-8625
16. Johnston, A. W., and Beringer, J. E. (1975) Identification of the Rhizobium strains in pea root nodules using genetic markers. J. Gen. Microbiol. 87, 343-350
17. Downie, J. A., Ma, Q. S., Knight, C. D., Hombrecher, G., and Johnston, A. W. (1983) Cloning of the symbiotic region of Rhizobium leguminosarum. The nodulation genes are between the nitrogenase genes and a nifA-like gene. EMBO J. 2, 947-952
18. Finnie, C., Hartley, N. M., Findlay, K. C., and 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
19. Beringer, J. E. (1974) R factor transfer in Rhizobium leguminosarum. J. Gen Microbiol. 84, 188-198
20. Sherwood, M. T. (1970) Improved synthetic medium for the growth of Rhizobium. J. Appl Bacteriol. 33, 708-713
21. Leigh, J. A., Signer, E. R., and Walker, G. C. (1985) Exopolysaccharidedeficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. U.S.A. 82, 6231-6235
22. Miller, K. J., Gore, R. S., Johnson, R., Benesi, A. J., and Reinhold, V. N. (1990) Cell-associated oligosaccharides of Bradyrhizobium spp. J. Bacteriol. 172, 136-142
23. Zevenhuizen, L. P. T. M., and Van Neerven, A. R. W. (1983) (1,2)-β-D Glucan and acidic oligosaccharides produced by Rhizobium meliloti. Carbohydr. Res. 118, 127-134
24. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
25. Edgar, R. C. (2004) MUSCLE. Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
26. Goodstadt, L., and Ponting, C. P. (2001) CHROMA. Consensus-based colouring of multiple alignments for publication. Bioinformatics 17, 845-846
27. Ginalski, K., Elofsson, A., Fischer, D., and Rychlewski, L. (2003) 3D-Jury. A simple approach to improve protein structure predictions. Bioinformatics 19, 1015-1018
28. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
29. Loewus, M. W., and Briggs, D. R. (1952) The number of catalytically active sites present on the chymotrypsin molecule. J. Biol. Chem. 199, 857-864
30. Filisetti-Cozzi, T. M., and Carpita, N. C. (1991) Measurement of uronic acids without interference from neutral sugars. Anal. Biochem. 197, 157-162
31. Jefferson, K. K., and Cerca, N. (2006) Methods in Molecular Biology. Cell- Cell Interactions: Methods and Protocols, pp. 119-126, Humana Press Inc., Totowa, NJ
32. Sandford, P. A., Pittsley, J. E., Knutson, C. A., Watson, P. R., Cadmus, M. C., and Janes, A. (1977) Variation in Xanthomonas campestris NRRL B-1459. Characterization of xanthan products of differing pyruvic acid content: American Chemical Society Symposium Series No. 45, pp. 192-210 (Sandford, P. A., and Laskin, A., eds) American Chemical Society, Washington, D. C.
33. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb- Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723
34. Nagar, B., Overduin, M., Ikura, M., and Rini, J. M. (1996) Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380, 360-364
35. Pertz, O., Bozic, D., Koch, A. W., Fauser, C., Brancaccio, A., and Engel, J. (1999) A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18, 1738-1747
36. Robertsen, B. K., Aman, P., Darvill, A. G., McNeil, M., and Albersheim, P. (1981) Host-symbiont interactions. V. The structure of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii. Plant Physiol. 67, 389-400
37. Laus, M. C., Logman, T. J., Van Brussel, A. A., Carlson, R. W., Azadi, P., Gao, M. Y., and Kijne, J. W. (2004) Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J. Bacteriol. 186, 6617-6625
38. Chen, C. P., Song, S. C., Gilboa-Garber, N., Chang, K. S., and Wu, A. M. (1998) Studies on the binding site of the galactose-specific agglutinin PA-IL from Pseudomonas aeruginosa. Glycobiology 8, 7-16
39. McNeil, M., Darvill, J., Darvill, A. G., Albersheim, P., van Veen, R., Hooykaas, P., Schilperoort, R., and Dell, A. (1986) The discernible, structural features of the acidic polysaccharides secreted by different Rhizobium species are the same. Carbohydr. Res. 146, 307-326
40. Zeng, X., Andrade, C. A., Oliveira, M. D., and Sun, X. L. (2012) Carbohydrate- protein interactions and their biosensing applications. Anal. Bioanal. Chem. 402, 3161-3176
41. Finnie, C., Zorreguieta, A., Hartley, N. M., and 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
42. Abbott, D. W., and Boraston, A. B. (2007) The structural basis for exopolygalacturonase activity in a family 28 glycoside hydrolase. J. Mol. Biol. 368, 1215-1222
43. Kataeva, I. A., Seidel, R. D., 3rd, Shah, A., West, L. T., Li, X. L., and Ljungdahl, L. G. (2002) The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl. Environ. Microbiol. 68, 4292-4300
44. Dazzo, F. B., Truchet, G. L., Sherwood, J. E., Hrabak, E. M., and 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
45. Watkins, N. J., Knight, M. R., Trewavas, A. J., and Campbell, A. K. (1995) Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin. Biochem. J. 306, 865-869
46. Delepelaire, P. (2004) Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 1694, 149-161
47. Holland, I. B., Schmitt, L., and Young, J. (2005) Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol. Membr. Biol. 22, 29-39
48. Chenal, A., Guijarro, J. I., Raynal, B., Delepierre, M., and Ladant, D. (2009) RTX calcium binding motifs are intrinsically disordered in the absence of calcium. Implication for protein secretion. J. Biol. Chem. 284, 1781-1789
49. Wolff, N., Sapriel, G., Bodenreider, C., Chaffotte, A., and Delepelaire, P. (2003) Antifolding activity of the SecB chaperone is essential for secretion of HasA, a quickly folding ABC pathway substrate. J. Biol. Chem. 278, 38247-38253
50. Michiels, J., Xi, C., Verhaert, J., and Vanderleyden, J. (2002) The functions of Ca2+ in bacteria. A role for EF-hand proteins? Trends Microbiol. 10, 87-93
51. Orans, J., Johnson, M. D., Coggan, K. A., Sperlazza, J. R., Heiniger, R. W., Wolfgang, M. C., and Redinbo, M. R. (2010) Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc. Natl. Acad. Sci. U.S.A. 107, 1065-1070
52. Aravind, P., Mishra, A., Suman, S. K., Jobby, M. K., Sankaranarayanan, R., and Sharma, Y. (2009) The βγ-crystallin superfamily contains a universal motif for binding calcium. Biochemistry 48, 12180-12190
53. Aravind, P., Suman, S. K., Mishra, A., Sharma, Y., and Sankaranarayanan, R. (2009) Three-dimensional domain swapping in nitrollin, a single-domain βγ-crystallin from Nitrosospira multiformis, controls protein conformation and stability but not dimerization. J. Mol. Biol. 385, 163-177
54. Vu, B., Chen, M., Crawford, R. J., and Ivanova, E. P. (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14, 2535-2554
55. Ghafoor, A., Hay, I. D., and Rehm, B. H. (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl. Environ. Microbiol. 77, 5238-5246
56. Begun, J., Gaiani, J. M., Rohde, H., Mack, D., Calderwood, S. B., Ausubel, F. M., and Sifri, C. D. (2007) Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3, e57