Bacillus spore germination at moderate high pressure: A review on underlying mechanisms, influencing factors, and its comparison with nutrient germination.
bacillus
germination
high pressure
spore
Journal
Comprehensive reviews in food science and food safety
ISSN: 1541-4337
Titre abrégé: Compr Rev Food Sci Food Saf
Pays: United States
ID NLM: 101305205
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
14
05
2021
received:
09
03
2021
accepted:
18
05
2021
pubmed:
20
6
2021
medline:
26
10
2021
entrez:
19
6
2021
Statut:
ppublish
Résumé
Spore-forming bacteria are resistant to stress conditions owing to their ability to form highly resistant dormant spores. These spores can survive adverse environmental conditions in nature, as well as decontamination processes in the food and related industries. Bacterial spores may return to their vegetative state through a process called germination. As spore germination is critical for the loss of resistance, outgrowth, and development of pathogenicity and spoilage potential, the germination pathway has piqued the interest of the scientific community. The inhibition and induction of germination have critical applications in the food industry. Targeted germination can aid in decreasing the resistance of spores and allow the application of milder inactivation procedures. This germination-inactivation strategy allows better maintenance of important food quality attributes. Different stimuli are reported to trigger germination. Among those, isostatic high pressure (HP) has gained increasing attention due to its potential applications in industrial processes. However, pressure-mediated spore germination is extremely heterogeneous as some spores germinate rapidly, while others exhibit slow germination or do not undergo germination at all. The successful and safe implementation of the germination-inactivation strategy, however, depends on the germination of all spores. Therefore, there is a need to elucidate the mechanisms of HP-mediated germination. This work aimed to critically review the current state of knowledge on Bacillus spore germination at a moderate HP of 50-300 MPa. In this review, the germination mechanism, heterogeneity, and influencing factors have been outlined along with knowledge gaps.
Identifiants
pubmed: 34147040
doi: 10.1111/1541-4337.12789
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
4159-4181Informations de copyright
© 2021 The Authors. Comprehensive Reviews in Food Science and Food Safety published by Wiley Periodicals LLC on behalf of Institute of Food Technologists.
Références
Aertsen, A., Van Opstal, I., Vanmuysen, S. C., Wuytack, E. Y., & Michiels, C. W. (2005). Screening for Bacillus subtilis mutants deficient in pressure induced spore germination: Identification of ykvU as a novel germination gene. FEMS Microbiology Letters. 243(2), 385-391. https://doi.org/10.1016/j.femsle.2004.12.029
Basset, J., Macheboeuf, M. ., & Roux, M. E. (1932). Etude sur les effets biologiques des ultra-pressions. Resistance des bacteries, des diastases et des toxines aux pressions elevees. Comptes Rendus de l'Académie Des Sciences, 196, 1431-1440.
Beaman, T. C., & Gerhardt, P. (1986). Heat resistance of bacterial spores correlated with protoplast dehydration, mineralization, and thermal adaptation. Applied and Environmental Microbiology. 52(6), 1242-1246. https://doi.org/10.1128/aem.52.6.1242-1246.1986
Berendsen, E. M., Boekhorst, J., Kuipers, O. P., & Wells-Bennik, M. H. J. (2016). A mobile genetic element profoundly increases heat resistance of bacterial spores. ISME Journal, 10(11), 2633-2642. https://doi.org/10.1038/ismej.2016.59
Bhattacharjee, D., McAllister, K. N., & Sorg, J. A. (2016). Germinants and their receptors in Clostridia. Journal of Bacteriology. 198(20), 2767-2775. https://doi.org/10.1128/JB.00405-16
Black, E. P., Koziol-Dube, K., Guan, D., Wei, J., Setlow, B., Cortezzo, D. E., Hoover, D. G., & Setlow, P. (2005). Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Applied Environmental Microbiology, 71(10), 5879-5887. https://doi.org/10.1128/AEM.71.10.5879-5887.2005
Black, E. P., Linton, M., McCall, R. D., Curran, W., Fitzgerald, G. F., Kelly, A. L., & Patterson, M. F. (2008). The combined effects of high pressure and nisin on germination and inactivation of Bacillus spores in milk. Journal of Applied Microbiology. 105(1), 78-87. https://doi.org/10.1111/j.1365-2672.2007.03722.x
Black, E. P., Setlow, P., Hocking, A. D., Stewart, C. M., Kelly, A. L., & Hoover, D. G. (2007). Response of spores to high-pressure processing. Comprehensive Reviews in Food Science and Food Safety, 6(4), 103-119. https://doi.org/10.1111/j.1541-4337.2007.00021.x
Black, E. P., Wei, J., Atluri, S., Cortezzo, D. E., Koziol-Dube, K., Hoover, D. G., & Setlow, P. (2007). Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. Journal of Applied Microbiology, 102(1), 65-76. https://doi.org/10.1111/j.1365-2672.2006.03062.x
Borch-Pedersen, K., Mellegård, H., Reineke, K., Boysen, P., Sevenich, R., Lindbäck, T., & Aspholm, M. (2017). Effects of high pressure on Bacillus licheniformis spore germination and inactivation. Applied and Environmental Microbiology, 83(14), e00503-17. https://doi.org/10.1128/AEM.00503-17
Cabrera-Martinez, R. M., Tovar-Rojo, F., Vepachedu, V. R., & Setlow, P. (2003). Effects of overexpression of nutrient receptors on germination of spores of Bacillus subtilis. Journal of Bacteriology. 185(8), 2457-2465. https://doi.org/10.1128/JB.185.8.2457-2464.2003
Cano, R. J., & Borucki, M. K. (1995). Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber. Science, 268(5213), 1060-1064. https://doi.org/10.1126/science.7538699
Chen, D., Huang, S. S., & Li, Y. Q. (2006). Real-time detection of kinetic germination and heterogeneity of single Bacillus spores by laser tweezers Raman spectroscopy. Analytical Chemistry. 78, 6936-6941. https://doi.org/10.1021/ac061090e
Chen, Y., Ray, W. K., Helm, R. F., Melville, S. B., & Popham, D. L. (2014). Levels of germination proteins in Bacillus subtilis dormant, superdormant, and germinating spores. PLoS One, 9(4), e95781. https://doi.org/10.1371/journal.pone.0095781
Christie, G., & Setlow, P. (2020). Bacillus spore germination: Knowns, unknowns and what we need to learn. Cellular Signalling. 74, 109729. https://doi.org/10.1016/j.cellsig.2020.109729
Clouston, J. G., & Wills, P. A. (1969). Initiation of germination and inactivation of Bacillus pumilus spores by hydrostatic pressure. Journal of Bacteriology. 97(2), 684-690. https://doi.org/10.1128/jb.97.2.684-690.1969
Cohn, F. (1876). Untersuchungen über Bacterien IV. Beiträge zur Biologie der Bacillen. Beiträge Zur Biologie Der Pflanze, 2, 249-276.
Condon, S., Bayarte, M., & Sala, F. J. (1992). Influence of the sporulation temperature upon the heat resistance of Bacillus subtilis. Journal of Applied Bacteriology. 73(3), 251-256. https://doi.org/10.1111/j.1365-2672.1992.tb02985.x
Cortezzo, D. E., Setlow, B., & Setlow, P. (2004). Analysis of the action of compounds that inhibit the germination of spores of Bacillus species. Journal of Applied Microbiology. 96(4), 725-741. https://doi.org/10.1111/j.1365-2672.2004.02196.x
Cortezzo, D. E., & Setlow, P. (2005). Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. Journal of Applied Microbiology. 98(3), 606-617. https://doi.org/10.1111/j.1365-2672.2004.02495.x
Cowan, A. E., Olivastro, E. M., Koppel, D. E., Loshon, C. A., Setlow, B., & Setlow, P. (2004). Lipids in the inner membrane of dormant spores of Bacillus species are largely immobile. Proceedings of the National Academy of Sciences of the United States of America. 101(20), 7733-7738. https://doi.org/10.1073/pnas.0306859101
Cronin, U. P., & Wilkinson, M. G. (2007). The use of flow cytometry to study the germination of Bacillus cereus endospores. Cytometry Part A, 71A(3), 143-153. https://doi.org/10.1002/cyto.a.20368
Delbrück, A. I., Zhang, Y., Hug, V., Trunet, C., & Mathys, A. (2021). Isolation, stability, and characteristics of high-pressure superdormant Bacillus subtilis spores. International Journal of Food Microbiology. 343, 109088. https://doi.org/10.1016/j.ijfoodmicro.2021.109088
Dong, P., Georget, E., Aganovic, K., Heinz, V., & Mathys, A. (2015). Ultra high pressure homogenization (UHPH) inactivation of Bacillus amyloliquefaciens spores in phosphate buffered saline (PBS) and milk. Frontiers in Microbiology. 6, 712. https://doi.org/10.3389/fmicb.2015.00712
Doona, C. J., Feeherry, F. E., Setlow, B., Wang, S., Li, W., Nichols, F. C., Talukdar, P. K., Sarker, M. R., Li, Y.-Q., Shen, A., & Setlow, P. (2016). Effects of high-pressure treatment on spores of Clostridium species. Applied and Environmental Microbiology, 82(17), 5287-5297. https://doi.org/10.1128/AEM.01363-16
Doona, C. J., Ghosh, S., Feeherry, F. F., Ramirez-Peralta, A., Huang, Y., Chen, H., & Setlow, P. (2014). High pressure germination of Bacillus subtilis spores with alterations in levels and types of germination proteins. Journal of Applied Microbiology, 117(3), 711-720. https://doi.org/10.1111/jam.12557
Furukawa, S., Shimoda, M., & Hayakawa, I. (2003). Mechanism of the inactivation of bacterial spores by reciprocal pressurization treatment. Journal of Applied Microbiology. 94(5), 836-841. https://doi.org/10.1046/j.1365-2672.2003.01913.x
Georget, E., Kapoor, S., Winter, R., Reineke, K., Song, Y., Callanan, M., Ananta, E., Heinz, V., & Mathys, A. (2014). In situ investigation of Geobacillus stearothermophilus spore germination and inactivation mechanisms under moderate high pressure. Food Microbiology, 41, 8-18. https://doi.org/10.1016/J.FM.2014.01.007
Georget, E., Miller, B., Callanan, M., Heinz, V., & Mathys, A. (2014). (Ultra) high pressure homogenization for continuous high pressure sterilization of pumpable foods - A review. Frontiers in Nutrition. 1(15), 1-6. https://doi.org/10.3389/fnut.2014.00015
Ghosh, S., Scotland, M., & Setlow, P. (2012). Levels of germination proteins in dormant and superdormant spores of Bacillus subtilis. Journal of Bacteriology, 194(9), 2221-2227. https://doi.org/10.1128/JB.00151-12
Ghosh, S., & Setlow, P. (2009). Isolation and characterization of superdormant spores of Bacillus species. Journal of Bacteriology, 191(6), 1787-1797. https://doi.org/10.1128/JB.01668-08
Ghosh, S., & Setlow, P. (2010). The preparation, germination properties and stability of superdormant spores of Bacillus cereus. Journal of Applied Microbiology, 108(2), 582-590. https://doi.org/10.1111/j.1365-2672.2009.04442.x
Gould, G. W., & Hitchins, A. D. (1963). Sensitization of bacterial spores to lysozyme and to hydrogen peroxide with agents which rupture disulphide bonds. Journal of General Microbiology. 33(3), 413-423. https://doi.org/10.1099/00221287-33-3-413
Gould, G. W., & Sale, A. J. (1970). Initiation of germination of bacterial spores by hydrostatic pressure. Journal of General Microbiology. 60(3), 335-346. https://doi.org/10.1099/00221287-60-3-335
Hashimoto, T., Frieben, W. R., & Conti, S. F. (1969). Germination of single bacterial spores. Journal of Bacteriology. 98(3), 1011-1020. https://doi.org/10.1128/JB.98.3.1011-1020.1969
Heard, B. R., & Miller, S. A. (2016). Critical research needed to examine the environmental impacts of expanded refrigeration on the food system. Environmental Science and Technology. 50, 12060-12071. https://doi.org/10.1021/acs.est.6b02740
Heinz, V., & Knorr, D. (1998). High pressure germination and inactivation kinetics of bacterial spores. In N. S. Isaacs (Ed.), High pressure food science, bioscience and chemistry (pp. 435-441). Woodhead Publishing.
Heinz, V., & Knorr, D. (2001). Effect of high pressure on spores. In M. E. G. Hendrickx, D. Knorr, L. Ludikhuyze, A. Van Loey, & V. Heinz (Eds.), Ultra high pressure treatments of foods (pp. 77-113). Springer Science+Business Media.
Hills, G. M. (1949). Chemical factors in the germination of spore-bearing aerobes; The effects of amino acids on the germination of Bacillus anthracis, with some observations on the relation of optical form to biological activity. Biochemical Journal. 45(3), 363-370. https://doi.org/10.1042/bj0450363
Hindle, A. A., & Hall, E. A. H. (1999). Dipicolinic acid (DPA) assay revisited and appraised for spore detection. Analyst. 124, 1599-1604. https://doi.org/10.1039/a906846e
Hite, B. H. (1899). The effect of pressure in the preservation of milk. West Virginia Agricultural Experimental Station Bulletin, 58, 15-35.
Hofstetter, S., Denter, C., Winter, R., McMullen, L. M., & Ganzle, M. G. (2012). Use of the fluorescent probe LAURDAN to label and measure inner membrane fluidity of endospores of Clostridium spp. Journal of Microbiological Methods, 91(1), 93-100. https://doi.org/10.1016/j.mimet.2012.07.023
Hornstra, L. M., De Vries, Y. P., De Vos, W. M., & Abee, T. (2006). Influence of sporulation medium composition on transcription of ger operons and the germination response of spores of Bacillus cereus ATCC 14579. Applied and Environmental Microbiology. 72(5), 3746-3749. https://doi.org/10.1128/AEM.72.5.3746-3749.2006
Igarashi, T., Setlow, B., Paidhungat, M., & Setlow, P. (2004). Effects of a gerF (lgt) mutation on the germination of spores of Bacillus subtilis. Journal of Bacteriology. 186(10), 2984-2991. https://doi.org/10.1128/JB.186.10.2984-2991.2004
Igura, N., Kamimura, Y., Islam, M. S., Shimoda, M., & Hayakawa, I. (2003). Effects of minerals on resistance of Bacillus subtilis spores to heat and hydrostatic pressure. Applied and Environmental Microbiology. 69(10), 6307-6310. https://doi.org/10.1128/AEM.69.10.6307-6310.2003
Kitamura, Y., & Itoh, T. (1987). Reaction volume of protonic ionization for buffering agents. Prediction of pressure dependence of pH and pOH. Journal of Solution Chemistry. 16, 715-725. https://doi.org/10.1007/BF00652574
Knorr, D., Reineke, K., Mathys, A., Heinz, V., & Buckow, R. (2010). High pressure-induced effects on bacterial spores, vegetative microorganisms, and enzymes. In J. M. Aguilera, R. Simpson, J. Welti-Chanes, D. Bermudez-Aguirre, & G. Barbosa-Canovas (Eds.), Food engineering interfaces. (pp. 325-340). Springer.
Knorr, D., Heinz, V., Schlüter, O., & Zenker, M. (1998). The potential impact of high pressure as unit operation for food processing. In N. S. Isaacs (Ed.), High pressure food science, bioscience and chemistry (pp. 227-235). The Royal Society of Chemistry.
Kong, L., Doona, C. J., Setlow, P., & Li, Y. (2014). Monitoring rates and heterogeneity of high-pressure germination of Bacillus spores by phase-contrast microscopy of individual spores. Applied and Environmental Microbiology, 80(1), 345-353. https://doi.org/10.1128/AEM.03043-13
Kong, L., Zhang, P., Wang, G., Yu, J., Setlow, P., & Li, Y. Q. (2011). Characterization of bacterial spore germination using phase-contrast and fluorescence microscopy, Raman spectroscopy and optical tweezers. Nature Protocols, 6(5), 625-639. https://doi.org/10.1038/nprot.2011.307
Kong, L., Zhang, P., Yu, J., Setlow, P., & Li, Y. (2010). Monitoring the kinetics of uptake of a nucleic acid dye during the germination of single spores of Bacillus species. Analytical Chemistry, 82(20), 8717-8724. https://doi.org/10.1021/ac1022327
Krawczyk, A. O., Berendsen, E. M., de Jong, A., Boekhorst, J., Wells-Bennik, M. H. J., Kuipers, O. P., & Eijlander, R. T. (2016). A transposon present in specific strains of Bacillus subtilis negatively affects nutrient- and dodecylamine-induced spore germination. Environmental Microbiology. 18(12), 4830-4846. https://doi.org/10.1111/1462-2920.13386
Krawczyk, A. O., de Jong, A., Omony, J., Holsappel, S., Wells-Bennik, M. H. J., Kuipers, O. P., & Eijlander, R. T. (2017). Spore heat activation requirements and germination responses correlate with sequences of germinant receptors and with the presence of a specific spoVA2mob operon in foodborne strains of Bacillus subtilis. Applied and Environmental Microbiology, 83(7), e03122-16. https://doi.org/10.1128/AEM.03122-16
Larson, W. P., Hartzell, T. B., & Diehl, H. S. (1918). The effect of high pressures on bacteria. Journal of Infectious Diseases. 22(3), 271-279. https://doi.org/10.1093/infdis/22.3.271
Laue, M., Han, H. M., Dittmann, C., & Setlow, P. (2018). Intracellular membranes of bacterial endospores are reservoirs for spore core membrane expansion during spore germination. Scientific Reports, 8, 11388. https://doi.org/10.1038/s41598-018-29879-5
Leggett, M. J., Mcdonnell, G., Denyer, S. P., Setlow, P., & Maillard, J. Y. (2012). Bacterial spore structures and their protective role in biocide resistance. Journal of Applied Microbiology. 113(3), 485-498. https://doi.org/10.1111/j.1365-2672.2012.05336.x
Lenz, C. A., & Vogel, R. F. (2015). Pressure-based strategy for the inactivation of spores. K. Akasaka & H. Matsuki High Pressure Bioscience. (469-537). Springer. https://doi.org/10.1007/978-94-017-9918-8_23
Levinson, H. S., & Hyatt, M. T. (1966). Sequence of events during Bacillus megaterium spore germination. Journal of Bacteriology. 91(5), 1811-1818. https://doi.org/10.1128/jb.91.5.1811-1818.1966
Li, Y., Jin, K., Ghosh, S., Devarakonda, P., Carlson, K., Davis, A., Stewart, K. A. V., Cammett, E., Rossi, P. P., Setlow, B., Lu, M., Setlow, P., & Hao, B. (2014). Structural and functional analysis of the GerD spore germination protein of Bacillus species. Journal of Molecular Biology. 426(9), 1995-2008. https://doi.org/10.1016/j.jmb.2014.02.004
Li, Z., Schottroff, F., Simpson, D. J., & Gänzle, M. G. (2019). The copy number of the spoVA 2mob operon determines pressure resistance of Bacillus endospores. Applied and Environmental Microbiology. 85(19), e01596-19. https://doi.org/10.1128/aem.01596-19
López, C. S., Garda, H. A., & Rivas, E. A. (2002). The effect of osmotic stress on the biophysical behavior of the Bacillus subtilis membrane studied by dynamic and steady-state fluorescence anisotropy. Archives of Biochemistry and Biophysics. 408(2), 220-228. https://doi.org/10.1016/S0003-9861(02)00566-0
López, C. S., Heras, H., Ruzal, S. M., Sánchez-Rivas, C., & Rivas, E. A. (1998). Variations of the envelope composition of Bacillus subtilis during growth in hyperosmotic medium. Current Microbiology. 36, 55-61. https://doi.org/10.1007/s002849900279
López, T. J., Roig, A. X., Capellas, M., Trujillo, A. J., Hernández, M., & Guamis, B. (2003). Evaluation of the importance of germinative cycles for destruction of Bacillus cereus spores in miniature cheeses. High Pressure Research. 23(1-2), 81-85. https://doi.org/10.1080/0895795031000147812
Luu, S., Cruz-Mora, J., Setlow, B., Feeherry, F. E., Doona, C. J., & Setlow, P. (2015). The effects of heat activation on Bacillus spore germination, with nutrients or under high pressure, with or without various germination proteins. Applied and Environmental Microbiology, 81(8), 2927-2938. https://doi.org/10.1128/AEM.00193-15
Machado, M. C., López, C. S., Heras, H., & Rivas, E. A. (2004). Osmotic response in Lactobacillus casei ATCC 393: Biochemical and biophysical characteristics of membrane. Archives of Biochemistry and Biophysics. 422(1), 61-70. https://doi.org/10.1016/j.abb.2003.11.001
Martínez-Monteagudo, S. I., Gänzle, M. G., & Saldaña, M. D. A. (2014). High-pressure and temperature effects on the inactivation of Bacillus amyloliquefaciens, alkaline phosphatase and storage stability of conjugated linoleic acid in milk. Innovative Food Science and Emerging Technologies. 26, 59-66. https://doi.org/10.1016/j.ifset.2014.05.003
Mason, J. M., & Setlow, P. (1986). Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light. Journal of Bacteriology. 167(1), 174-178. https://doi.org/10.1128/jb.167.1.174-178.1986
Mathys, A., Chapman, B., Bull, M., Heinz, V., & Knorr, D. (2007). Flow cytometric assessment of Bacillus spore response to high pressure and heat. Innovative Food Science & Emerging Technologies, 8(4), 519-527. https://doi.org/10.1016/J.IFSET.2007.06.010
Mathys, A., Kallmeyer, R., Heinz, V., & Knorr, D. (2008). Impact of dissociation equilibrium shift on bacterial spore inactivation by heat and pressure. Food Control. 19(12), 1165-1173. https://doi.org/10.1016/j.foodcont.2008.01.003
Melly, E., Genest, P. C., Gilmore, M. E., Little, S., Popham, D. L., Driks, A., & Setlow, P. (2002). Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. Journal of Applied Microbiology, 92(6), 1105-1115. https://doi.org/10.1046/j.1365-2672.2002.01644.x
Olguín-Araneda, V., Banawas, S., Sarker, M. R., & Paredes-Sabja, D. (2015). Recent advances in germination of Clostridium spores. Research in Microbiology. 166(4), 236-243. https://doi.org/10.1016/j.resmic.2014.07.017
Paidhungat, M., Ragkousi, K., & Setlow, P. (2001). Genetic requirements for induction of germination of spores of Bacillus subtilis by Ca2+-dipicolinate. Journal of Bacteriology, 183(16), 4886-4893. https://doi.org/10.1128/jb.183.16.4886-4893.2001
Paidhungat, M., Setlow, B., Daniels, W. B., Hoover, D., Papafragkou, E., & Setlow, P. (2002). Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. Applied and Environmental Microbiology, 68(6), 3172-3175. https://doi.org/10.1128/AEM.68.6.3172-3175.2002
Paidhungat, M., Setlow, B., Driks, A., & Setlow, P. (2000). Characterization of spores of Bacillus subtilis which lack dipicolinic acid. Journal of Bacteriology, 182(19), 5505-5512. https://doi.org/10.1128/JB.182.19.5505-5512.2000
Paidhungat, M., & Setlow, P. (1999). Isolation and characterization of mutations in Bacillus subtilis that allow spore germination in the novel germinant D-alanine. Journal of Bacteriology. 181(11), 3341-3350. https://doi.org/10.1128/jb.181.11.3341-3350.1999
Paidhungat, M., & Setlow, P. (2000). Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. Journal of Bacteriology, 182(9), 2513-2519. https://doi.org/10.1128/JB.182.9.2513-2519.2000
Paidhungat, M., & Setlow, P. (2001). Localization of a germinant receptor protein (GerBA) to the inner membrane of Bacillus subtilis spores. Journal of Bacteriology. 183(13), 3982-3990. https://doi.org/10.1128/JB.183.13.3982-3990.2001
Palop, A., Mañas, P., & Condón, S. (1999). Sporulation temperature and heat resistance of Bacillus spores: A review. Journal of Food Safety. 19(1), 57-72. https://doi.org/10.1111/j.1745-4565.1999.tb00234.x
Paredes-Sabja, D., Setlow, P., & Sarker, M. R. (2011). Germination of spores of Bacillales and Clostridiales species: Mechanisms and proteins involved. Trends in Microbiology. 19(2), 85-94. https://doi.org/10.1016/j.tim.2010.10.004
Pelczar, P. L., Igarashi, T., Setlow, B., & Setlow, P. (2007). Role of GerD in germination of Bacillus subtilis spores. Journal of Bacteriology. 189(3), 1090-1098. https://doi.org/10.1128/JB.01606-06
Postgate, J. R. (1969). Viable counts and viability. Methods in Microbiology, 1, 611-628.
Ramirez-Peralta, A., Gupta, S., Butzin, X. Y., Setlow, B., Korza, G., Leyva-Vazquez, M. A., Christie, G., & Setlow, P. (2013). Identification of new proteins that modulate the germination of spores of Bacillus species. Journal of Bacteriology. 195(13), 3009-3021. https://doi.org/10.1128/JB.00257-13
Ramirez-Peralta, A., Stewart, K. A. V., Thomas, S. K., Setlow, B., Chen, Z., Li, Y. Q., & Setlow, P. (2012). Effects of the SpoVT regulatory protein on the germination and germination protein levels of spores of Bacillus subtilis. Journal of Bacteriology. 194(13), 3417-3425. https://doi.org/10.1128/JB.00504-12
Ramirez-Peralta, A., Zhang, P., Li, Y. qing, & Setlow, P. (2012). Effects of sporulation conditions on the germination and germination protein levels of Bacillus subtilis spores. Applied and Environmental Microbiology. 78(8), 2689-2697. https://doi.org/10.1128/AEM.07908-11
Rao, L., Feeherry, F. E., Ghosh, S., Liao, X., Lin, X., Zhang, P., Li, Y., Doona, C. J., & Setlow, P. (2018). Effects of lowering water activity by various humectants on germination of spores of Bacillus species with different germinants. Food Microbiology, 72, 112-127. https://doi.org/10.1016/J.FM.2017.11.012
Raso, J., Góngora-Nieto, M. M., Barbosa-Cánovas, G. V., & Swanson, B. G. (1998). Influence of several environmental factors on the initiation of germination and inactivation of Bacillus cereus by high hydrostatic pressure. International Journal of Food Microbiology. 44(1-2), 125-132. https://doi.org/10.1016/S0168-1605(98)00130-5
Reineke, K., Doehner, I., Schlumbach, K., Baier, D., Mathys, A., & Knorr, D. (2012). The different pathways of spore germination and inactivation in dependence of pressure and temperature. Innovative Food Science and Emerging Technologies, 13, 31-41. https://doi.org/10.1016/j.ifset.2011.09.006
Reineke, K., Ellinger, N., Berger, D., Baier, D., Mathys, A., Setlow, P., & Knorr, D. (2013). Structural analysis of high pressure treated Bacillus subtilis spores. Innovative Food Science & Emerging Technologies, 17, 43-53. https://doi.org/10.1016/J.IFSET.2012.10.009
Reineke, K., & Mathys, A. (2020). Endospore inactivation by emerging technologies: A review of target structures and inactivation mechanisms. Annual Review of Food Science and Technology. 11, 255-274. https://doi.org/10.1146/annurev-food-032519-051632
Reineke, K., Mathys, A., Heinz, V., & Knorr, D. (2013). Mechanisms of endospore inactivation under high pressure. Trends in Microbiology, 21(6), 296-304. https://doi.org/10.1016/J.TIM.2013.03.001
Reineke, K., Mathys, A., & Knorr, D. (2011). Shift of pH-value during thermal treatments in buffer solutions and selected foods. International Journal of Food Properties. 14(4), 870-881. https://doi.org/10.1080/10942910903456978
Reineke, K., Schlumbach, K., Baier, D., Mathys, A., & Knorr, D. (2013). The release of dipicolinic acid - The rate-limiting step of Bacillus endospore inactivation during the high pressure thermal sterilization process. International Journal of Food Microbiology, 162(1), 55-63. https://doi.org/10.1016/J.IJFOODMICRO.2012.12.010
Riemann, H., & John Ordal, Z. (1961). Germination of bacterial endospores with calcium and dipicolinic acid. Science. 133(3465), 1703-1704. https://doi.org/10.1126/science.133.3465.1703
Rode, L. J., & Foster, J. W. (1960). The action of surfactants on bacterial spores. Archiv Für Mikrobiologie, 36, 67-94. https://doi.org/10.1007/BF00405943
Sale, A. J., Gould, G. W., & Hamilton, W. A. (1970). Inactivation of bacterial spores by hydrostatic pressure. Journal of General Microbiology. 60(3), 323-334. https://doi.org/10.1099/00221287-60-3-323
Setlow, B., Melly, E., & Setlow, P. (2001). Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. Journal of Bacteriology. 183(16), 4894-4899. https://doi.org/10.1128/JB.183.16.4894-4899.2001
Setlow, B., & Setlow, P. (1993). Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide. Applied and Environmental Microbiology. 59(10), 3418-3423. https://doi.org/10.1128/aem.59.10.3418-3423.1993
Setlow, B., & Setlow, P. (1996). Role of DNA repair in Bacillus subtilis spore resistance. Journal of Bacteriology, 178(12), 3486-3495. https://doi.org/10.1128/jb.178.12.3486-3495.1996
Setlow, P. (2003). Spore germination. Current Opinion in Microbiology, 6(6), 550-556. https://doi.org/10.1016/J.MIB.2003.10.001
Setlow, P. (2006). Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals. Journal of Applied Microbiology, 101(3), 514-525. https://doi.org/10.1111/j.1365-2672.2005.02736.x
Setlow, P. (2007). I will survive: DNA protection in bacterial spores. Trends in Microbiology, 15(4), 172-180. https://doi.org/10.1016/j.tim.2007.02.004
Setlow, P. (2013). Summer meeting 2013 - When the sleepers wake: The germination of spores of Bacillus species. Journal of Applied Microbiology. 115(6), 1251-1268. https://doi.org/10.1111/jam.12343
Setlow, P. (2014). Germination of spores of Bacillus species: What we know and do not know. Journal of Bacteriology, 196(7), 1297-1305.
Setlow, P., Wang, S., & Li, Y.-Q. (2017). Germination of spores of the orders Bacillales and Clostridiales. Annual Review of Microbiology, 71(1), 459-477. https://doi.org/10.1146/annurev-micro-090816-093558
Sevenich, R., & Mathys, A. (2018). Continuous versus discontinuous ultra-high-pressure systems for food sterilization with focus on ultra-high-pressure homogenization and high-pressure thermal sterilization: A review. Comprehensive Reviews in Food Science and Food Safety, 17(3), 646-662. https://doi.org/10.1111/1541-4337.12348
Sinai, L., Rosenberg, A., Smith, Y., Segev, E., & Ben-Yehuda, S. (2015). The molecular timeline of a reviving bacterial spore. Molecular Cell. 57(4), 695-707. https://doi.org/10.1016/j.molcel.2014.12.019
Smith, D. A., Moir, A., & Sammons, R. (1978). Progress in genetics of spore germination in Bacillus subtilis. In G. Chambliss, & J. C. Vary (Eds.), Spores (pp. 158-163). American Society for Microbiology.
Stringer, S. C., Webb, M. D., George, S. M., Pin, C., & Peck, M. W. (2005). Heterogeneity of times required for germination and outgrowth from single spores of nonproteolytic Clostridium botulinum. Applied and Environmental Microbiology. 71(9), 4998-5003. https://doi.org/10.1128/AEM.71.9.4998-5003.2005
Stringer, S. C., Webb, M. D., & Peck, M. W. (2011). Lag time variability in individual spores of Clostridium botulinum. Food Microbiology. 28(2), 228-235. https://doi.org/10.1016/j.fm.2010.03.003
Sunde, E. P., Setlow, P., Hederstedt, L., & Halle, B. (2009). The physical state of water in bacterial spores. Proceedings of the National Academy of Sciences of the United States of America. 106(46), 19334-19339. https://doi.org/10.1073/pnas.0908712106
Traag, B. A., Ramirez-Peralta, A., Wang Erickson, A. F., Setlow, P., & Losick, R. (2013). A novel RNA polymerase-binding protein controlling genes involved in spore germination in Bacillus subtilis. Molecular Microbiology. 89(1), 113-122. https://doi.org/10.1111/mmi.12262
Van Opstal, I., Bagamboula, C. F., Vanmuysen, S. C. M., Wuytack, E. Y., & Michiels, C. W. (2004). Inactivation of Bacillus cereus spores in milk by mild pressure and heat treatments. International Journal of Food Microbiology. 92(2), 227-234. https://doi.org/10.1016/j.ijfoodmicro.2003.09.011
Velásquez, J., Schuurman-Wolters, G., Birkner, J. P., Abee, T., & Poolman, B. (2014). Bacillus subtilis spore protein SpoVAC functions as a mechanosensitive channel. Molecular Microbiology. 92(4), 813-823. https://doi.org/10.1111/mmi.12591
Vepachedu, V. R., Hirneisen, K., Hoover, D. G., & Setlow, P. (2007). Studies of the release of small molecules during pressure germination of spores of Bacillus subtilis. Letters in Applied Microbiology, 45(3), 342-348. https://doi.org/10.1111/j.1472-765X.2007.02204.x
Vreeland, R. H., Rosenzweig, W. D., & Powers, D. W. (2000). Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature. 407, 897-900. https://doi.org/10.1038/35038060
Wei, J., Shah, I. M., Ghosh, S., Dworkin, J., Hoover, D. G., & Setlow, P. (2010). Superdormant spores of Bacillus species germinate normally with high pressure, peptidoglycan fragments, and bryostatin. Journal of Bacteriology, 192(5), 1455-1458. https://doi.org/10.1128/JB.01497-09
Wells-Bennik, M. H. J., Eijlander, R. T., Besten den, H. M. W., Berendsen, E. M., Warda, A. K., Krawczyk, A. O., Groot, M. N. N., Xiao, Y. H., Zwietering, M. H., Kuipers, O. P., & Abee, T. (2016). Bacterial spores in food: Survival, emergence, and outgrowth. Annual Review of Food Science and Technology, 7, 457-482. https://doi.org/10.1146/annurev-food-041715-033144
Wuytack, E. Y., Boven, S., & Michiels, C. W. (1998). Comparative study of pressure-induced germination of Bacillus subtilis spores at low and high pressures. Applied and Environmental Microbiology, 64(9), 3220-3224. http://www.ncbi.nlm.nih.gov/pubmed/9726863
Wuytack, E. Y., & Michiels, C. W. (2001). A study on the effects of high pressure and heat on Bacillus subtilis spores at low pH. International Journal of Food Microbiology. 64(3), 333-341. https://doi.org/10.1016/S0168-1605(00)00478-5
Wuytack, E. Y., Soons, J., Poschet, F., & Michiels, C. W. (2000). Comparative study of pressure- and nutrient-induced germination of Bacillus subtilis spores. Applied and Environmental Microbiology. 66(1), 257-261. https://doi.org/10.1128/AEM.66.1.257-261.2000
Zhang, H., & Mittal, G. S. (2008). Effects of high-pressure processing (HPP) on bacterial spores: An overview. Food Reviews International. 24(3), 330-351. https://doi.org/10.1080/87559120802089290
Zhang, P., Garner, W., Yi, X., Yu, J., Li, Y. Q., & Setlow, P. (2010). Factors affecting variability in time between addition of nutrient germinants and rapid dipicolinic acid release during germination of spores of Bacillus species. Journal of Bacteriology. 192(14), 3608-3619. https://doi.org/10.1128/JB.00345-10
Zhang, P., Kong, L., Wang, G., Scotland, M., Ghosh, S., Setlow, B., Setlow, P., & Li, Y.-Q. (2012). Analysis of the slow germination of multiple individual superdormant Bacillus subtilis spores using multifocus Raman microspectroscopy and differential interference contrast microscopy. Journal of Applied Microbiology, 112(3), 526-536. https://doi.org/10.1111/j.1365-2672.2011.05230.x
Zhang, P., Kong, L., Wang, G., Setlow, P., & Li, Y. (2010). Combination of Raman tweezers and quantitative differential interference contrast microscopy for measurement of dynamics and heterogeneity during the germination of individual bacterial spores. Journal of Biomedical Optics. 15(5), 056010. https://doi.org/10.1117/1.3494567
Zhang, P., Liang, J., Yi, X., Setlow, P., & Li, Y. Q. (2014). Monitoring of commitment, blocking, and continuation of nutrient germination of individual Bacillus subtilis spores. Journal of Bacteriology. 196(13), 2443-2454. https://doi.org/10.1128/JB.01687-14
Zhang, Y., Delbrück, A. I., Off, C. L., Benke, S., & Mathys, A. (2020). Flow cytometry combined with single cell sorting to study heterogeneous germination of Bacillus spores under high pressure. Frontiers in Microbiology. 10, 3118. https://doi.org/10.3389/fmicb.2019.03118
Zhang, Y., & Mathys, A. (2019). Superdormant spores as a hurdle for gentle germination-inactivation based spore control strategies. Frontiers in Microbiology, 9, 3163. https://doi.org/10.3389/fmicb.2018.03163