The crystal structure of the lipid II-degrading bacteriocin syringacin M suggests unexpected evolutionary relationships between colicin M-like bacteriocins

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38876-38888

  Grinter, Rhys ^a   Roszak, Aleksander W ^b   Cogdell, Richard J ^a   Milner, Joel J ^a   Walker, Daniel ^a  

^a School of Life Sciences   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ASPARTIC ACIDS; BACTERIOCINS; CALCIUM IONS; CATALYTIC DOMAINS; COLICINS; EVOLUTIONARY RELATIONSHIPS; HIGH POTENCY; MICROBIAL COMMUNITIES; MUTANT PROTEINS; PATHOGENIC SPECIES; PEPTIDOGLYCANS; PHOSPHATASE ACTIVITY; POTENTIAL APPLICATIONS; PSEUDOMONAS SYRINGAE; RECEPTOR BINDING; RECEPTOR-BINDING DOMAINS; SEQUENCE HOMOLOGY; SIDE-CHAINS; STRUCTURAL SIMILARITY;

AMINO ACIDS; MANGANESE; MANGANESE COMPOUNDS; METAL IONS;

PROTEINS;

BACTERIOCIN; CALCIUM ION; COLICIN; COLICIN M; MAGNESIUM ION; MANGANESE; PEPTIDOGLYCAN; PHOSPHATASE; SYRINGACIN M; UNCLASSIFIED DRUG;

ARTICLE; BIOCATALYSIS; CARBOXY TERMINAL SEQUENCE; CELL KILLING; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; INHIBITION KINETICS; LIPID DEGRADATION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; PSEUDOMONAS SYRINGAE; RECEPTOR BINDING; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; SPECIES DIVERSITY; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ASPARTIC ACID; BACTERIOCINS; CALCIUM; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; IONS; MAGNESIUM; MANGANESE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PHYLOGENY; PSEUDOMONAS SYRINGAE; SEQUENCE HOMOLOGY, AMINO ACID; URIDINE DIPHOSPHATE N-ACETYLMURAMIC ACID;

PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 84869012885     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.400150     Document Type: Article

References (59)

1. Riley, M. A. (1998) Molecular mechanisms of bacteriocin evolution. Annu. Rev. Genet. 32, 255-278
2. Kleanthous, C. (2010) Swimming against the tide. Progress and challenges in our understanding of colicin translocation. Nat. Rev. Microbiol. 8, 843-848
3. Michel-Briand, Y., and Baysse, C. (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84, 499-510
4. Graham, A. C., and Stocker, B. A. (1977) Genetics of sensitivity of Salmonella Species to colicin M and bacteriophages T5, T1, and ES18. J. Bacteriol. 130, 1214-1223
5. Feldgarden, M., and Riley, M. A. (1998) High levels of colicin resistance in Escherichia coli. Evolution 52, 1270-1276
6. Chuang, D. Y., Chien, Y. C., and Wu, H. P. (2007) Cloning and expression of the Erwinia carotovora subsp. carotovora gene encoding the low-molecular-weight bacteriocin carocin S1. J. Bacteriol. 189, 620-626
7. Roh, E., Park, T. H., Kim, M. I., Lee, S., Ryu, S., Oh, C. S., Rhee, S., Kim, D. H., Park, B. S., and Heu, S. (2010) Characterization of a new bacteriocin, carocin D, from Pectobacterium carotovorum subsp. carotovorum Pcc21. Appl. Environ. Microbiol. 76, 7541-7549
8. Grinter, R., Milner, J., and Walker, D. (2012) Ferredoxin containing bacteriocins suggest a novel mechanism of iron uptake in Pectobacterium spp. PLoS ONE 7, e33033
9. Cascales, E., Buchanan, S. K., Duché, D., Kleanthous, C., Lloubès, R., Postle, K., Riley, M., Slatin, S., and Cavard, D. (2007) Colicin biology. Microbiol. Mol. Biol. Rev. 71, 158-229
10. Walker, D., Moore, G. R., James, R., and Kleanthous, C. (2003) Thermodynamic consequences of bipartite immunity protein binding to the ribosomal ribonuclease colicin E3. Biochemistry 42, 4161-4171
11. El Ghachi, M., Bouhss, A., Barreteau, H., Touzé, T., Auger, G., Blanot, D., and Mengin-Lecreulx, D. (2006) Colicin M exerts Its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J. Biol. Chem. 281, 22761-22772
12. Harkness, R. E., and Braun, V. (1989) Colicin M inhibits peptidoglycan biosynthesis by interfering with lipid carrier recycling. J. Biol. Chem. 264, 6177-6182
13. Kleanthous, C., and Walker, D. (2001) Immunity proteins. Enzyme inhibitors that avoid the active site. Trends Biochem. Sci. 26, 624-631
14. Zhang, X. Y., Lloubès, R., and Duché, D. (2010) Channel domain of colicin Amodifies the dimeric organization of its immunity protein. J. Biol. Chem. 285, 38053-38061
15. Usón, I., Patzer, S. I., Rodríguez, D. D., Braun, V., and Zeth, K. (2012) The crystal structure of the dimeric colicin M immunity protein displays a three-dimensional domain swap. J. Struct. Biol. 178, 45-53
16. Riley, M. A., and Wertz, J. E. (2002) Bacteriocins. Evolution, ecology, and application. Annu. Rev. Microbiol. 56, 117-137
17. Sano, Y., Kobayashi, M., and Kageyama, M. (1993) Functional domains of S-type pyocins deduced from chimeric molecules. J. Bacteriol. 175, 6179-6185
18. Wojdyla, J. A., Fleishman, S. J., Baker, D., and Kleanthous, C. (2012) Structure of the ultra-high-affinity colicin E2 DNase-Im2 complex. J. Mol. Biol. 417, 79-94
19. Fyfe, J. A., Harris, G., and Govan, J. R. (1984) Revised pyocin typing method for Pseudomonas aeruginosa. J. Clin. Microbiol. 20, 47-50
20. Gorrec, F. (2009) The MORPHEUS protein crystallization screen. J. Appl. Crystallogr. 42, 1035-1042
21. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
22. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
23. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
24. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M., and Paciorek, W. (2003) Generation, representation, and flow of phase information in structure determination. Recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59, 2023-2030
25. Vonrhein, C., Blanc, E., Roversi, P., and Bricogne, G. (2007) in Macromolecular Crystallography Protocols (Doublié, S., ed) pp. 215-230, Humana Press, New Jersey
26. Sheldrick, G. (2010) Experimental phasing with SHELXC/D/E. Combining chain tracing with density modification. Acta Crystallogr.DBiol. Crystallogr. 66, 479-485
27. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/ wARP version 7. Nat. Protoc. 3, 1171-1179
28. Cowtan, K. (2008) Fitting molecular fragments into electron density. Acta Crystallogr. D Biol. Crystallogr. 64, 83-89
29. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
30. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
31. Cruickshank, D. (1999) Remarks about protein structure precision. Acta Crystallogr. D Biol. Crystallogr. 55, 583-601
32. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
33. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry. φ,ψ and Cβ deviation. Proteins 50, 437-450
34. Dong, A., Xu, X., and Edwards, A. M. (2007) In situ proteolysis for protein crystallization and structure determination. Nat. Methods 4, 1019-1021
35. Barreteau, H., Bouhss, A., Fourgeaud, M., Mainardi, J. L., Touzé, T., Gérard, F., Blanot, D., Arthur, M., and Mengin-Lecreulx, D. (2009) Humanand plant-pathogenic Pseudomonas species produce bacteriocins exhibiting colicin M-like hydrolase activity toward peptidoglycan precursors. J. Bacteriol. 191, 3657-3664
36. Clarke, T. B., Kawai, F., Park, S. Y., Tame, J. R., Dowson, C. G., and Roper, D. I. (2009) Mutational analysis of the substrate specificity of Escherichia coli penicillin-binding protein 4. Biochemistry 48, 2675-2683
37. Lloyd, A. J., Gilbey, A. M., Blewett, A. M., De Pascale, G., El Zoeiby, A., Levesque, R. C., Catherwood, A. C., Tomasz, A., Bugg, T. D., Roper, D. I., and Dowson, C. G. (2008) Characterization of tRNA-dependent peptide bond formation by MurM in the synthesis of Streptococcus pneumoniae peptidoglycan. J. Biol. Chem. 283, 6402-6417
38. Soelaiman, S., Jakes, K., Wu, N., Li, C., and Shoham, M. (2001) Crystal structure of colicin E3. Implications for cell entry and ribosome inactivation. Mol. Cell 8, 1053-1062
39. Zeth, K., Römer, C., Patzer, S. I., and Braun, V. (2008) Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. J. Biol. Chem. 283, 25324-25331
40. Barreteau, H., Bouhss, A., Gérard, F., Duché, D., Boussaid, B., Blanot, D., Lloubès, R., Mengin-Lecreulx, D., and Touzé, T. (2010) Deciphering the catalytic domain of colicin M, a peptidoglycan lipid II-degrading enzyme. J. Biol. Chem. 285, 12378-12389
41. Helbig, S., and Braun, V. (2011) Mapping functional domains of colicin M. J. Bacteriol. 193, 815-821
42. Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138
43. Zheng, H., Chruszcz, M., Lasota, P., Lebioda, L., and Minor, W. (2008) Data mining of metal ion environments present in protein structures. J. Inorg. Biochem. 102, 1765-1776
44. Katz, A. K., Glusker, J. P., Beebe, S. A., and Bock, C. W. (1996) Calcium ion coordination. A comparison with that of beryllium, magnesium, and zinc. J. Am. Chem. Soc. 118, 5752-5763
45. Moncrief, M. B., and Maguire, M. E. (1999) Magnesium transport in prokaryotes. J. Biol. Inorg. Chem. 4, 523-527
46. Pilsl, H., Glaser, C., Gross, P., Killmann, H., Olschläger, T., and Braun, V. (1993) Domains of colicin M involved in uptake and activity. Mol. Gen. Genet. 240, 103-112
47. Holm, L., and Sander, C. (1997) Decision support system for the evolutionary classification of protein structures. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 140-146
48. Arnold, T., Zeth, K., and Linke, D. (2009) Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J. Biol. Chem. 284, 6403-6413
49. Wiener, M., Freymann, D., Ghosh, P., and Stroud, R. M. (1997) Crystal structure of colicin Ia. Nature 385, 461-464
50. Smith, E. E., Sims, E. H., Spencer, D. H., Kaul, R., and Olson, M. V. (2005) Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J. Bacteriol. 187, 2138-2147
51. Tümmler, B., and Cornelis, P. (2005) Pyoverdine receptor. A case of positive Darwinian selection in Pseudomonas aeruginosa. J. Bacteriol. 187, 3289-3292
52. Bajaj, M., and Blundell, T. (1984) Evolution and the tertiary structure of proteins. Annu. Rev. Biophys. Bioeng. 13, 453-492
53. Cuff, J. A., and Barton, G. J. (2000) Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins 40, 502-511
54. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0. Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
55. 2+ between the periplasm and the cytosol of Escherichia coli. Cell Calcium 32, 183-192
56. Chang, C. F., Shuman, H., and Somlyo, A. P. (1986) Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium, magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells. J. Bacteriol. 167, 935-939
57. Schaller, K., Dreher, R., and Braun, V. (1981) Structural and functional properties of colicin M. J. Bacteriol. 146, 54-63
58. 2+-binding site in the P-type ATPase and phosphatase member of the HAD (haloacid dehalogenase) superfamily by structural similarity to the response regulator protein CheY. Biochem. J. 339, 223-226
59. Lu, Z., Dunaway-Mariano, D., and Allen, K. N. (2008) The catalytic scaffold of the haloalkanoic acid dehalogenase enzyme superfamily acts as a mold for the trigonal bipyramidal transition state. Proc. Natl. Acad. Sci. U.S.A. 105, 5687-5692