In pursuit of protein targets: Proteomic characterization of bacterial spore outer layers

Journal of Proteome Research

Volumn 12, Issue 10, 2013, Pages 4507-4521

  Abhyankar, Wishwas ^a   Hossain, Abeer H ^a   Djajasaputra, André ^a   Permpoonpattana, Patima ^b,c   Ter Beek, Alexander ^a   Dekker, Henk L ^a   Cutting, Simon M ^b   Brul, Stanley ^a   De Koning, Leo J ^a   De Koster, Chris G ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c PRINCE OF SONGKLA UNIVERSITY   (Thailand)

Author keywords

B. cereus ATCC 14579; C. difficile 630; exosporium; insoluble protein fraction; spore coat

Indexed keywords

BACTERIAL PROTEIN; COAT PROTEIN;

ARTICLE; BACILLI; BACILLUS CEREUS; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIAL VIRULENCE; CLOSTRIDIUM; CLOSTRIDIUM DIFFICILE; FOOD; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEOMICS; SPOROGENESIS; SURVIVAL;

BACILLUS CEREUS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; CLOSTRIDIUM DIFFICILE; DRUG RESISTANCE, BACTERIAL; FOOD MICROBIOLOGY; PEPTIDOGLYCAN; PROTEIN STRUCTURE, TERTIARY; PROTEOME; SPORES, BACTERIAL;

EID: 84885217530     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4005629     Document Type: Article

References (82)

1. Tourasse, N. J.; Helgason, E.; Okstad, O. A.; Hegna, I. K.; Kolsto, A. B. The Bacillus cereus group: novel aspects of population structure and genome dynamics J. Appl. Microbiol. 2006, 101 (3) 579-93
2. Stenfors Arnesen, L. P.; Fagerlund, A.; Granum, P. E. From soil to gut: Bacillus cereus and its food poisoning toxins FEMS Microbiol. Rev. 2008, 32 (4) 579-606
3. Lund, T.; De Buyser, M. L.; Granum, P. E. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis Mol. Microbiol. 2000, 38 (2) 254-61
4. Bottone, E. J. Bacillus cereus, a volatile human pathogen Clin. Microbiol. Rev. 2010, 23 (2) 382-98
5. Bartlett, J. G.; Willey, S. H.; Chang, T. W.; Lowe, B. Cephalosporin-associated pseudomembranous colitis due to Clostridium difficile J. Am. Med. Assoc. 1979, 242 (24) 2683-5
6. Songer, J. G.; Anderson, M. A. Clostridium difficile: an important pathogen of food animals Anaerobe 2006, 12 (1) 1-4
7. Huang, H.; Weintraub, A.; Fang, H.; Nord, C. E. Antimicrobial resistance in Clostridium difficile Int. J. Antimicrob. Agents 2009, 34 (6) 516-22
8. Razavi, B.; Apisarnthanarak, A.; Mundy, L. M. Clostridium difficile: emergence of hypervirulence and fluoroquinolone resistance Infection 2007, 35 (5) 300-7
9. Bartlett, J. G. New drugs for Clostridium difficile infection Clin. Infect. Dis. 2006, 43 (4) 428-31
10. Brazier, J. S.; Raybould, R.; Patel, B.; Duckworth, G.; Pearson, A.; Charlett, A.; Duerden, B. I., Distribution and antimicrobial susceptibility patterns of Clostridium difficile PCR ribotypes in English hospitals, 2007-08. Eur. Commun. Dis. Bull. 2008, 13, (41).
11. Cairns, M. D.; Stabler, R. A.; Shetty, N.; Wren, B. W. The continually evolving Clostridium difficile species Future Microbiology 2012, 7 (8) 945-57
12. Dawson, L. F.; Valiente, E.; Wren, B. W. Clostridium difficile - a continually evolving and problematic pathogen Infect., Genet. Evol. 2009, 9 (6) 1410-7
13. Carter, G. P.; Rood, J. I.; Lyras, D. The role of toxin A and toxin B in Clostridium difficile -associated disease: Past and present perspectives Gut Microbes 2010, 1 (1) 58-64
14. Setlow, P. Spore germination Curr. Opin. Microbiol. 2003, 6 (6) 550-6
15. Henriques, A. O.; Moran, C. P., Jr. Structure, assembly, and function of the spore surface layers Annu. Rev. Microbiol. 2007, 61, 555-88
16. Lequette, Y.; Garénaux, E.; Tauveron, G.; Dumez, S.; Perchat, S.; Slomianny, C.; Lereclus, D.; Guerardel, Y.; Faille, C. Role played by exosporium glycoproteins in the surface properties of Bacillus cereus spores and in their adhesion properties to stainless steel Appl. Environ. Microbiol. 2011, 77 (14) 4905-11
17. Paredes, C. J.; Alsaker, K. V.; Papoutsakis, E. T. A comparative genomic view of clostridial sporulation and physiology Nat. Rev. Microbiol. 2005, 3 (12) 969-78
18. de Hoon, M. J.; Eichenberger, P.; Vitkup, D. Hierarchical evolution of the bacterial sporulation network Curr. Biol. 2010, 20 (17) R735-45
19. Leski, T. A.; Caswell, C. C.; Pawlowski, M.; Klinke, D. J.; Bujnicki, J. M.; Hart, S. J.; Lukomski, S. Identification and Classification of bcl Genes and Proteins of Bacillus cereus Group Organisms and Their Application in Bacillus anthracis Detection and Fingerprinting Appl. Environ. Microbiol. 2009, 75 (22) 7163-72
20. Thompson, B. M.; Hoelscher, B. C.; Driks, A.; Stewart, G. C. Localization and assembly of the novel exosporium protein BetA of Bacillus anthracis J. Bacteriol. 2011, 193 (19) 5098-104
21. Waller, L. N.; Stump, M. J.; Fox, K. F.; Harley, W. M.; Fox, A.; Stewart, G. C.; Shahgholi, M. Identification of a second collagen-like glycoprotein produced by Bacillus anthracis and demonstration of associated spore-specific sugars J. Bacteriol. 2005, 187 (13) 4592-7
22. Abhyankar, W.; Beek, A. T.; Dekker, H.; Kort, R.; Brul, S.; de Koster, C. G. Gel-free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction Proteomics 2011, 11 (23) 4541-50
23. McKenney, P. T.; Driks, A.; Eichenberger, P. The Bacillus subtilis endospore: assembly and functions of the multilayered coat Nat. Rev. Microbiol. 2013, 11 (1) 33-44
24. de Vries, Y. P.; Hornstra, L. M.; de Vos, W. M.; Abee, T. Growth and sporulation of Bacillus cereus ATCC 14579 under defined conditions: temporal expression of genes for key sigma factors Appl. Environ. Microbiol. 2004, 70 (4) 2514-9
25. Permpoonpattana, P.; Tolls, E. H.; Nadem, R.; Tan, S.; Brisson, A.; Cutting, S. M. Surface layers of Clostridium difficile endospores J. Bacteriol. 2011, 193 (23) 6461-70
26. Todd, S. J.; Moir, A. J.; Johnson, M. J.; Moir, A. Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium J. Bacteriol. 2003, 185 (11) 3373-8
27. Redmond, C.; Baillie, L. W.; Hibbs, S.; Moir, A. J.; Moir, A. Identification of proteins in the exosporium of Bacillus anthracis Microbiology 2004, 150 (Pt 2) 355-63
28. Hadžija, O. A simple method for the quantitative determination of muramic acid Anal. Biochem. 1974, 60 (2) 512-7
29. Taylor, K. C. C. A simple colorimetric assay for muramic acid and lactic acid Appl. Biochem. Biotechnol. 1996, 56 (1) 49-58
30. Thompson, B. M.; Binkley, J. M.; Stewart, G. C. Current physical and SDS extraction methods do not efficiently remove exosporium proteins from Bacillus anthracis spores J. Microbiol. Methods 2011, 85 (2) 143-8
31. Klobutcher, L. A.; Ragkousi, K.; Setlow, P. The Bacillus subtilis spore coat provides ″eat resistance″ during phagocytic predation by the protozoan Tetrahymena thermophila Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (1) 165-70
32. Scopes, R. K. Measurement of protein by spectrophotometry at 205 nm Anal. Biochem. 1974, 59 (1) 277-82
33. Abecasis, A. B.; Serrano, M.; Alves, R.; Quintais, L.; Pereira-Leal, J. B.; Henriques, A. O. A genomic signature and the identification of new sporulation genes J. Bacteriol. 2013, 195 (9) 2101-15
34. Barra-Carrasco, J.; Olguin-Araneda, V.; Plaza-Garrido, A.; Miranda-Cardenas, C.; Cofre-Araneda, G.; Pizarro-Guajardo, M.; Sarker, M. R.; Paredes-Sabja, D. The Clostridium difficile Exosporium Cysteine (CdeC) Rich Protein is Required for Exosporium Morphogenesis and Coat Assembly J. Bacteriol. 2013, 195 (17) 3863-75
35. Lawley, T. D.; Croucher, N. J.; Yu, L.; Clare, S.; Sebaihia, M.; Goulding, D.; Pickard, D. J.; Parkhill, J.; Choudhary, J.; Dougan, G. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores J. Bacteriol. 2009, 191 (17) 5377-86
36. Putnam, E. E.; Nock, A. M.; Lawley, T. D.; Shen, A. SpoIVA and SipL Are Clostridium difficile Spore Morphogenetic Proteins J. Bacteriol. 2013, 195 (6) 1214-25
37. Cutting, S.; Anderson, M.; Lysenko, E.; Page, A.; Tomoyasu, T.; Tatematsu, K.; Tatsuta, T.; Kroos, L.; Ogura, T. SpoVM, a small protein essential to development in Bacillus subtilis, interacts with the ATP-dependent protease FtsH J. Bacteriol. 1997, 179 (17) 5534-42
38. Ozin, A. J.; Henriques, A. O.; Yi, H.; Moran, C. P., Jr. Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat J. Bacteriol. 2000, 182 (7) 1828-33
39. Henriques, A. O.; Melsen, L. R.; Moran, C. P., Jr. Involvement of superoxide dismutase in spore coat assembly in Bacillus subtilis J. Bacteriol. 1998, 180 (9) 2285-91
40. Isticato, R.; Esposito, G.; Zilhao, R.; Nolasco, S.; Cangiano, G.; De Felice, M.; Henriques, A. O.; Ricca, E. Assembly of multiple CotC forms into the Bacillus subtilis spore coat J. Bacteriol. 2004, 186 (4) 1129-35
41. Isticato, R.; Pelosi, A.; Zilhao, R.; Baccigalupi, L.; Henriques, A. O.; De Felice, M.; Ricca, E. CotC-CotU heterodimerization during assembly of the Bacillus subtilis spore coat J. Bacteriol. 2008, 190 (4) 1267-75
42. Zilhão, R.; Serrano, M.; Isticato, R.; Ricca, E.; Moran, C. P., Jr.; Henriques, A. O. Interactions among CotB, CotG, and CotH during assembly of the Bacillus subtilis spore coat J. Bacteriol. 2004, 186 (4) 1110-9
43. McPherson, S. A.; Li, M.; Kearney, J. F.; Turnbough, C. L., Jr. ExsB, an unusually highly phosphorylated protein required for the stable attachment of the exosporium of Bacillus anthracis Mol. Microbiol. 2010, 76 (6) 1527-38
44. Permpoonpattana, P.; Phetcharaburanin, J.; Mikelsone, A.; Dembek, M.; Tan, S.; Brisson, M. C.; La Ragione, R.; Brisson, A. R.; Fairweather, N.; Hong, H. A.; Cutting, S. M. Functional Characterization of Clostridium difficile Spore Coat Proteins J. Bacteriol. 2013, 195 (7) 1492-503
45. Boydston, J. A.; Yue, L.; Kearney, J. F.; Turnbough, C. L., Jr. The ExsY protein is required for complete formation of the exosporium of Bacillus anthracis J. Bacteriol. 2006, 188 (21) 7440-8
46. Bagyan, I.; Noback, M.; Bron, S.; Paidhungat, M.; Setlow, P. Characterization of yhcN, a new forespore-specific gene of Bacillus subtilis Gene 1998, 212 (2) 179-88
47. Errington, J. Regulation of endospore formation in Bacillus subtilis Nat. Rev. Microbiol. 2003, 1 (2) 117-26
48. Aucher, W.; Davison, S.; Fouet, A. Characterization of the sortase repertoire in Bacillus anthracis PLoS One 2011, 6 (11) e27411
49. Fukushima, T.; Yao, Y.; Kitajima, T.; Yamamoto, H.; Sekiguchi, J. Characterization of new L,D-endopeptidase gene product CwlK (previous YcdD) that hydrolyzes peptidoglycan in Bacillus subtilis Mol. Genet. Genomics 2007, 278 (4) 371-83
50. Mirey, G.; Soulard, A.; Orange, C.; Friant, S.; Winsor, B. SH3 domain-containing proteins and the actin cytoskeleton in yeast Biochem. Soc. Trans. 2005, 33 (Pt 6) 1247-9
51. Kim, H. S.; Sherman, D.; Johnson, F.; Aronson, A. I. Characterization of a major Bacillus anthracis spore coat protein and its role in spore inactivation J. Bacteriol. 2004, 186 (8) 2413-7
52. Lehmann, Y.; Meile, L.; Teuber, M. Rubrerythrin from Clostridium perfringens: cloning of the gene, purification of the protein, and characterization of its superoxide dismutase function J. Bacteriol. 1996, 178 (24) 7152-8
53. 2 detoxification in Clostridium acetobutylicum Microbiology 2009, 155 (Pt 1) 16-24
54. Brahmbhatt, T. N.; Janes, B. K.; Stibitz, E. S.; Darnell, S. C.; Sanz, P.; Rasmussen, S. B.; O'Brien, A. D. Bacillus anthracis exosporium protein BclA affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity Infect. Immun. 2007, 75 (11) 5233-9
55. Kailas, L.; Terry, C.; Abbott, N.; Taylor, R.; Mullin, N.; Tzokov, S. B.; Todd, S. J.; Wallace, B. A.; Hobbs, J. K.; Moir, A.; Bullough, P. A. Surface architecture of endospores of the Bacillus cereus / anthracis / thuringiensis family at the subnanometer scale Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (38) 16014-9
56. Beck, K.; Brodsky, B. Supercoiled protein motifs: the collagen triple-helix and the alpha-helical coiled coil J. Struct. Biol. 1998, 122 (1-2) 17-29
57. Tan, L.; Turnbough, C. L., Jr. Sequence motifs and proteolytic cleavage of the collagen-like glycoprotein BclA required for its attachment to the exosporium of Bacillus anthracis J. Bacteriol. 2010, 192 (5) 1259-68
58. Steichen, C. T.; Kearney, J. F.; Turnbough, C. L., Jr. Characterization of the exosporium basal layer protein BxpB of Bacillus anthracis J. Bacteriol. 2005, 187 (17) 5868-76
59. Thompson, B. M.; Hoelscher, B. C.; Driks, A.; Stewart, G. C. Assembly of the BclB glycoprotein into the exosporium and evidence for its role in the formation of the exosporium 'cap' structure in Bacillus anthracis Mol. Microbiol. 2012, 86 (5) 1073-84
60. Liu, H.; Bergman, N. H.; Thomason, B.; Shallom, S.; Hazen, A.; Crossno, J.; Rasko, D. A.; Ravel, J.; Read, T. D.; Peterson, S. N.; Yates, J., 3rd; Hanna, P. C. Formation and composition of the Bacillus anthracis endospore J. Bacteriol. 2004, 186 (1) 164-78
61. Andersen, G. L.; Simchock, J. M.; Wilson, K. H. Identification of a region of genetic variability among Bacillus anthracis strains and related species J. Bacteriol. 1996, 178 (2) 377-84
62. Walker, J. R.; Gnanam, A. J.; Blinkova, A. L.; Hermandson, M. J.; Karymov, M. A.; Lyubchenko, Y. L.; Graves, P. R.; Haystead, T. A.; Linse, K. D. Clostridium taeniosporum spore ribbon-like appendage structure, composition and genes Mol. Microbiol. 2007, 63 (3) 629-43
63. Reiter, L.; Tourasse, N. J.; Fouet, A.; Loll, R.; Davison, S.; Okstad, O. A.; Piehler, A. P.; Kolsto, A. B. Evolutionary history and functional characterization of three large genes involved in sporulation in Bacillus cereus group bacteria J. Bacteriol. 2011, 193 (19) 5420-30
64. Driks, A. Surface appendages of bacterial spores Mol. Microbiol. 2007, 63 (3) 623-5
65. Rode, L. J.; Crawford, M. A.; Williams, M. G. Clostridium spores with ribbon-like appendages J. Bacteriol. 1967, 93 (3) 1160-73
66. Réty, S.; Salamitou, S.; Garcia-Verdugo, I.; Hulmes, D. J.; Le Hegarat, F.; Chaby, R.; Lewit-Bentley, A. The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins J. Biol. Chem. 2005, 280 (52) 43073-8
67. Bozue, J.; Cote, C. K.; Moody, K. L.; Welkos, S. L. Fully virulent Bacillus anthracis does not require the immunodominant protein BclA for pathogenesis Infect. Immun. 2007, 75 (1) 508-11
68. Ghebrehiwet, B.; Tantral, L.; Titmus, M. A.; Panessa-Warren, B. J.; Tortora, G. T.; Wong, S. S.; Warren, J. B. The exosporium of B. cereus contains a binding site for gC1qR/p33: implication in spore attachment and/or entry Adv. Exp. Med. Biol. 2007, 598, 181-97
69. Chesnokova, O. N.; McPherson, S. A.; Steichen, C. T.; Turnbough, C. L., Jr. The spore-specific alanine racemase of Bacillus anthracis and its role in suppressing germination during spore development J. Bacteriol. 2009, 191 (4) 1303-10
70. Liang, L.; He, X.; Liu, G.; Tan, H. The role of a purine-specific nucleoside hydrolase in spore germination of Bacillus thuringiensis Microbiology 2008, 154 (Pt 5) 1333-40
71. 2+-dipicolinate J. Bacteriol. 2003, 185 (7) 2315-29
72. Terry, C.; Shepherd, A.; Radford, D. S.; Moir, A.; Bullough, P. A. YwdL in Bacillus cereus: its role in germination and exosporium structure PLoS One 2011, 6 (8) e23801
73. Lambert, E. A.; Popham, D. L. The Bacillus anthracis SleL (YaaH) protein is an N-acetylglucosaminidase involved in spore cortex depolymerization J. Bacteriol. 2008, 190 (23) 7601-7
74. Dembek, M.; Stabler, R. A.; Witney, A. A.; Wren, B. W.; Fairweather, N. F. Transcriptional Analysis of Temporal Gene Expression in Germinating Clostridium difficile 630 Endospores PLoS One 2013, 8 (5) e64011
75. Ando, Y.; Tsuzuki, T. Energy-dependent activation of spore-lytic enzyme precursor by germinated spores of Clostridium perfringens Biochem. Biophys. Res. Commun. 1984, 123 (2) 463-7
76. Cybulski, R. J., Jr.; Sanz, P.; McDaniel, D.; Darnell, S.; Bull, R. L.; O'Brien, A. D. Recombinant Bacillus anthracis spore proteins enhance protection of mice primed with suboptimal amounts of protective antigen Vaccine 2008, 26 (38) 4927-39
77. Walper, S.; Lee, P.; Anderson, G.; Goldman, E. Selection and Characterization of Single Domain Antibodies Specific for Bacillus anthracis Spore Proteins Antibodies 2013, 2 (1) 152-167
78. Barry, C. S. The stay-green revolution: Recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants Plant Sci. 2009, 176 (3) 325-333
79. Fu, Z.; Chen, S.; Baldwin, M. R.; Boldt, G. E.; Crawford, A.; Janda, K. D.; Barbieri, J. T.; Kim, J. J. Light chain of botulinum neurotoxin serotype A: structural resolution of a catalytic intermediate Biochemistry 2006, 45 (29) 8903-11
80. Galperin, M. Y.; Mekhedov, S. L.; Puigbo, P.; Smirnov, S.; Wolf, Y. I.; Rigden, D. J. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes Environ. Microbiol. 2012, 14 (11) 2870-90
81. Traag, B. A.; Pugliese, A.; Eisen, J. A.; Losick, R. Gene conservation among endospore-forming bacteria reveals additional sporulation genes in Bacillus subtilis J. Bacteriol. 2013, 195 (2) 253-60
82. Escobar-Cortes, K.; Barra-Carrasco, J.; Paredes-Sabja, D. Proteases and sonication specifically remove the exosporium layer of spores of Clostridium difficile strain 630 J. Microbiol. Methods 2013, 93 (1) 25-31