The influence of sporulation conditions on the spore coat protein composition of Bacillus subtilis spores

Frontiers in Microbiology

Volumn 7, Issue OCT, 2016, Pages

  Abhyankar, Wishwas R ^a   Kamphorst, Kiki ^a   Swarge, Bhagyashree N ^a   van Veen, Henk ^b   van der Wel, Nicole N ^b   Brul, Stanley ^a   de Koster, Chris G ^a   de Koning, Leo J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Bacillus; Proteomics; Quantitative proteomics; Spores; Sporulation conditions

Indexed keywords

DIPICOLINIC ACID;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; CONTROLLED STUDY; CULTURE MEDIUM; HEAT TOLERANCE; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHASE CONTRAST MICROSCOPY; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; SPOROGENESIS; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84996940141     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01636     Document Type: Article

References (28)

1. Abhyankar, W., Pandey, R., Ter Beek, A., Brul, S., De Koning, L. J., and De Koster, C. G. (2015). Reinforcement of Bacillus subtilis spores by cross-linking of outer coat proteins during maturation. Food Microbiol. 45, 54-62. doi: 10.1016/j.fm.2014.03.007
2. Abhyankar, W., Ter Beek, A., Dekker, H., Kort, R., Brul, S., and De Koster, C. G. (2011). Gel-free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction. Proteomics 11, 4541-4550. doi: 10.1002/pmic.201100003
3. Checinska, A., Paszczynski, A., and Burbank, M. (2015). Bacillus and other spore-forming genera: variations in responses and mechanisms for survival. Annu. Rev. Food Sci. Technol. 6, 351-369. doi: 10.1146/annurev-food-030713-092332
4. Dadd, A. H., Mccormick, K. E., and Daley, G. M. (1983). Factors influencing the resistance of biological monitors to ethylene oxide. J. Appl. Bacteriol. 55, 39-48. doi: 10.1111/j.1365-2672.1983.tb02645.x
5. Driks, A. (1999). Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 63, 1-20.
6. Driks, A. (2002). Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol. 10, 251-254. doi: 10.1016/S0966-842X(02)02373-9
7. Driks, A., and Eichenberger, P. (2016). The spore coat. Microbiol. Spectr. 4, 1-22. doi: 10.1128/microbiolspec.TBS-0023-2016
8. Gerhardt, P., and Marquis, R. E. (1989). "Spore thermoresistance mechanisms," in Regulation of Prokaryotic Development, eds I. Smith, R. A. Slepecky, and P. Setlow (Washington, DC: American Society for Microbiology), 43-63.
9. Hullo, M. F., Moszer, I., Danchin, A., and Martin-Verstraete, I. (2001). CotA of Bacillus subtilis is a copper-dependent laccase. J. Bacteriol. 183, 5426-5430. doi: 10.1128/JB.183.18.5426-5430.2001
10. Imamura, D., Kuwana, R., Takamatsu, H., and Watabe, K. (2010). Localization of proteins to different layers and regions of Bacillus subtilis spore coats. J. Bacteriol. 192, 518-524. doi: 10.1128/JB.01103-09
11. Imamura, D., Kuwana, R., Takamatsu, H., and Watabe, K. (2011). Proteins involved in formation of the outermost layer of Bacillus subtilis spores. J. Bacteriol. 193, 4075-4080. doi: 10.1128/JB.05310-11
12. Janssen, F. W., Lund, A. J., and Anderson, L. E. (1958). Colorimetric assay for dipicolinic acid in bacterial spores. Science 127, 26-27. doi: 10.1126/science.127.3288.26
13. Kim, H., Hahn, M., Grabowski, P., Mcpherson, D. C., Otte, M. M., Wang, R., et al. (2006). The Bacillus subtilis spore coat protein interaction network. Mol. Microbiol. 59, 487-502. doi: 10.1111/j.1365-2958.2005.04968.x
14. Kooiman, W. J., Barker, A. N., Gould, G. W., and Wolf, J. (1973). "The screw cap tube technique: a new and accurate technique for the determination of the wet heat resistance of bacterial spores," in Spore Research, eds A. N. Barker, G. W. Gould, and J. Wolf (London: Academic Press), 87-92.
15. Little, S., and Driks, A. (2001). Functional analysis of the Bacillus subtilis morphogenetic spore coat protein CotE. Mol. Microbiol. 42, 1107-1120. doi: 10.1046/j.1365-2958.2001.02708.x
16. Mckenney, P. T., Driks, A., and Eichenberger, P. (2013). The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11, 33-44. doi: 10.1038/nrmicro2921
17. McKenney, P. T., Driks, A., Eskandarian, H. A., Grabowski, P., Guberman, J., Wang, K. H., et al. (2010). A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr. Biol. 20, 934-938. doi: 10.1016/j.cub.2010.03.060
18. Melly, E., Genest, P. C., Gilmore, M. E., Little, S., Popham, D. L., Driks, A., et al. (2002). Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J. Appl. Microbiol. 92, 1105-1115. doi: 10.1046/j.1365-2672.2002.01644.x
19. Mundra, R. V., Mehta, K. K., Wu, X., Paskaleva, E. E., Kane, R. S., and Dordick, J. S. (2014). Enzyme-driven Bacillus spore coat degradation leading to spore killing. Biotechnol. Bioeng. 111, 654-663. doi: 10.1002/bit.25132
20. Orsburn, B., Melville, S. B., and Popham, D. L. (2008). Factors contributing to heat resistance of Clostridium perfringens endospores. Appl. Environ. Microbiol. 74, 3328-3335. doi: 10.1128/AEM.02629-07
21. Ragkousi, K., and Setlow, P. (2004). Transglutaminase-mediated cross-linking of GerQ in the coats of Bacillus subtilis spores. J. Bacteriol. 186, 5567-5575. doi: 10.1128/JB.186.17.5567-5575.2004
22. Rose, R., Setlow, B., Monroe, A., Mallozzi, M., Driks, A., and Setlow, P. (2007). Comparison of the properties of Bacillus subtilis spores made in liquid or on agar plates. J. Appl. Microbiol. 103, 691-699. doi: 10.1111/j.1365-2672.2007.03297.x
23. Sanchez-Salas, J. L., Setlow, B., Zhang, P., Li, Y. Q., and Setlow, P. (2011). Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl. Environ. Microbiol. 77, 6746-6754. doi: 10.1128/AEM.05031-11
24. Scopes, R. K. (1974). Measurement of protein by spectrophotometry at 205 nm. Anal. Biochem. 59, 277-282. doi: 10.1016/0003-2697(74)90034-7
25. Setlow, B., Atluri, S., Kitchel, R., Koziol-Dube, K., and Setlow, P. (2006). Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J. Bacteriol. 188, 3740-3747. doi: 10.1128/JB.00212-06
26. Setlow, P. (1988). Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function, and degradation. Annu. Rev. Microbiol. 42, 319-338. doi: 10.1146/annurev.mi.42.100188.001535
27. van Ooij, C., Eichenberger, P., and Losick, R. (2004). Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis. J. Bacteriol. 186, 4441-4448. doi: 10.1128/JB.186.14.4441-4448.2004
28. Vizcaíno, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., et al. (2014). ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotech. 32, 223-226. doi: 10.1038/nbt.2839