Role played by exosporium glycoproteins in the surface properties of Bacillus cereus spores and in their adhesion to stainless steel

Applied and Environmental Microbiology

Volumn 77, Issue 14, 2011, Pages 4905-4911

  Lequette, Yannick ^a   Garénaux, Estelle ^d   Tauveron, Grégoire ^a   Dumez, Sylvain ^a   Perchat, Stéphane ^b   Slomianny, Christian ^c   Lereclus, Didier ^b   Guérardel, Yann ^d   Faille, Christine ^a  

^a CEMAGREF   (France)

^b UMR1319 MICALIS   (France)

^c Université des Sciences et Technologies de Lille   (France)

^d UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION PROPERTIES; ANTHRACIS; BACILLUS CEREUS SPORES; GLYCOSYL RESIDUES; ISO-ELECTRIC POINTS; MONOSACCHARIDE ANALYSIS;

ADHESION; BACILLI; BACILLUS CEREUS; BACTERIOLOGY; CORROSION RESISTANT ALLOYS; GLUCOSE; GLYCOPROTEINS; HYDROPHOBICITY; SURFACE PROPERTIES;

STAINLESS STEEL;

2 O METHYLRHAMNOSE; 2-O-METHYLRHAMNOSE; BACTERIAL PROTEIN; MEMBRANE PROTEIN; METHYL MANNOSIDE; STAINLESS STEEL;

ADHESION; BACTERIUM; HYDROPHOBICITY; PROTEIN; SPORE; STEEL;

ARTICLE; BACILLUS CEREUS; BACTERIAL SPORE; BACTERIUM ADHERENCE; CELL WALL; CHEMICAL PHENOMENA; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SURFACE PROPERTY;

BACILLUS CEREUS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL WALL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE GLYCOPROTEINS; METHYLMANNOSIDES; MOLECULAR SEQUENCE DATA; SPORES, BACTERIAL; STAINLESS STEEL; SURFACE PROPERTIES;

BACILLUS ANTHRACIS; BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

EID: 79961073409     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02872-10     Document Type: Article

References (42)

1. Arantes, O., and D. Lereclus. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119.
2. Bos, R., and H. J. Busscher. 1999. Role of acid-base interactions on the adhesion of oral streptococci and actinomyces to hexadecane and chloroform. Influence of divalent cations and comparison between free energies of partitioning and free energies obtained by extended DLVO analysis. Coll. Surf. B Biointerfaces 14:169-177.
3. Boydston, J. A., P. Chen, C. T. Steichen, and C. L. Turnbough. 2005. Ori-entation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis. J. Bacteriol. 187:5310-5317.
4. Bozue, J., et al. 2007. Bacillus anthracis spores of the bclA mutant exhibit increased adherence to epithelial cells, fibroblasts, and endothelial cells but not to macrophages. Infect. Immun. 75:4498-4505.
5. Bozue, J. A., et al. 2005. Construction of a rhamnose mutation in Bacillus anthracis affects adherence to macrophages but not virulence in guinea pigs. Microb. Pathog. 38:1-12.
6. Brahmbhatt, T. N., et al. 2007. Bacillus anthracis exosporium protein Bc1A affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity. Infect. Immun. 75:5233-5239.
7. Chen, G., A. Driks, K. Tawfiq, M. Mallozzi, and S. Patil. 2010. Bacillus anthracis and Bacillus subtilis spore surface properties and transport. Coll. Surf. B Biointerfaces 76:512-518.
8. Daubenspeck, J. M., et al. 2004. Novel oligosaccharide side chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J. Biol. Chem. 279:30945-30953.
9. Dong, S. L., et al. 2008. Anthrose biosynthetic operon of Bacillus anthracis. J. Bacteriol. 190:2350-2359.
10. Etiennetoumelin, I., J. C. Sirard, E. Duflot, M. Mock, and A. Fouet. 1995. Characterization of the Bacillus anthracis S-layer: cloning and sequencing of the structural gene. J. Bacteriol. 177:614-620.
11. Faille, C., et al. 2002. Adhesion of Bacillus spores and Escherichia coli cells to inert surfaces: role of surface hydrophobicity. Can. J. Microbiol. 48:728-738.
12. Faille, C., et al. 2010. Morphology and physico-chemical properties of Bacillus spores surrounded or not with an exosporium: consequences on their ability to adhere to stainless steel. Int. J. Food Microbiol. 143:125-135.
13. Faille, C., et al. 2010. Viability and surface properties of spores subjected to a cleaning-in-place procedure. Consequences on their ability to contaminate surfaces of equipment. Food Microbiol. 27:769-776.
14. Faille, C., G. Tauveron, C. Le Gentil-Lelièvre, and C. Slomianny. 2007. Occurrence of Bacillus cereus spores with a damaged exosporium: Consequences on the spore adhesion on surfaces of food processing lines. J. Food Prot. 70:2346-2353.
15. Fox, A., et al. 2003. Carbohydrates and glycoproteins of Bacillus anthracis and related bacilli: targets for biodetection. J. Microbiol. Methods 54:143-152.
16. Giorno, R., et al. 2007. Morphogenesis of the Bacillus anthracis spore. J. Bacteriol. 189:691-705.
17. Guerout-Fleury, A. M., K. Shazand, N. Frandsen, and P. Stragier. 1995. Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167:335-336.
18. Henriques, A. O., and C. P. Moran. 2007. Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61:555-588.
19. Hüsmark, U., and U. Rönner. 1992. The influence of hydrophobic, electrostatic and morphologic properties on the adhesion of Bacillus spores. Biofouling 5:335-344.
20. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
21. Lereclus, D., M. Vallade, J. Chaufaux, O. Arantes, and S. Rambaud. 1992. Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination. Biotechnology 10:418-421.
22. Leski, T. A., et al. 2009. 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. 75:7163-7172.
23. Lichtenberg, D., M. Rosenberg, N. Sharfman, and I. Ofek. 1985. A kinetic approach to bacterial adherence to hydrocarbon. J. Microbiol. Methods 4:141-146.
24. Oliva, C., C. L. Turnbough, and J. F. Kearney. 2009. CD14-Mac-1 interactions in Bacillus anthracis spore internalization by macrophages. Proc. Natl. Acad. Sci. U. S. A. 106:13957-13962.
25. Oliva, C. R., et al. 2008. The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc. Natl. Acad. Sci. U. S. A. 105:1261-1266.
26. Rajkovic, A., M. Uyttendaele, T. Courtens, M. Heyndrickx, and J. Debevere. 2006. Prevalence and characterisation of Bacillus cereus in vacuum packed potato puree. Int. J. Food Sci. Technol. 41:878-884.
27. Ramarao, N., and D. Lereclus. 2005. The InhA1 metalloprotease allows spores of the B. cereus group to escape macrophages. Cell Microbiol. 7:1357-1364.
28. Rety, S., et al. 2005. The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins. J. Biol. Chem. 280:43073-43078.
29. Rönner, U., U. Hüsmark, and A. Henriksson. 1990. Adhesion of Bacillus spores in relation to hydrophobicity. J. Appl. Bacteriol. 69:550-556.
30. Sanchis, V., H. Agaisse, J. Chaufaux, and D. Lereclus. 1996. Construction of new insecticidal Bacillus thuringiensis recombinant strains by using the sporulation non-dependent expression system of cryIIIA and a site specific recombination vector. J. Biotechnol. 48:81-96.
31. Seale, R. B., P. J. Bremer, S. H. Flint, and A. J. McQuillan. 2010. Characterization of spore surfaces from a Geobacillus sp. isolate by pH dependence of surface charge and infrared spectra. J. Appl. Microbiol. 109:1339-1348.
32. Simmonds, P., B. L. Mossel, T. Intaraphan, and H. C. Deeth. 2003. Heat resistance of Bacillus spores when adhered to stainless steel and its relationship to spore hydrophobicity. J. Food Prot. 66:2070-2075.
33. Svensson, B., et al. 2006. Occurrence of emetic toxin producing Bacillus cereus in the dairy production chain. Int. Dairy J. 16:740-749.
34. Sylvestre, P., E. Couture-Tosi, and M. Mock. 2002. A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol. Microbiol. 45:169-178.
35. Sylvestre, P., E. Couture-Tosi, and M. Mock. 2003. Polymorphism in the collagen-like region of the Bacillus anthracis BclA protein leads to variation in exosporium filament length. J. Bacteriol. 185:1555-1563.
36. Tamborrini, M., et al. 2009. Immuno-detection of anthrose containing tetrasaccharide in the exosporium of Bacillus anthracis and Bacillus cereus strains. J. Appl. Microbiol. 106:1618-1628.
37. Tauveron, G., C. Slomianny, C. Henry, and C. Faille. 2006. Variability among Bacillus cereus strains in the spore surface properties and influence on their ability to contaminate food surface equipment. Int. J. Food Microbiol. 110:254-262.
38. Thompson, B. M., and G. C. Stewart. 2008. Targeting of the BclA and BclB proteins to the Bacillus anthracis spore surface. Mol. Microbiol. 70:421-434.
39. Thompson, B. M., L. N. Waller, K. F. Fox, A. Fox, and G. C. Stewart. 2007. The BclB glycoprotein of Bacillus anthracis is involved in exosporium integrity. J. Bacteriol. 189:6704-6713.
40. Todd, S. J., A. J. Moir, M. J. Johnson, and A. Moir. 2003. Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J. Bacteriol. 185:3373-3378.
41. Waller, L. N., N. Fox, K. F. Fox, A. Fox, and R. L. Price. 2004. Ruthenium red staining for ultrastructural visualization of a glycoprotein layer surrounding the spore of Bacillus anthracis and Bacillus subtilis. J. Microbiol. Methods 58:23-30.
42. Waller, L. N., et al. 2005. Identification of a second collagen-like glycoprotein produced by Bacillus anthracis and demonstration of associated sporespecific sugars. J. Bacteriol. 187:4592-4597.