The underlying mechanism of bacterial spore germination: An update review.
bacterial spores
germination
high hydrostatic pressure
molecular mechanisms
nutrient germinants
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:
Jul 2023
Jul 2023
Historique:
revised:
22
03
2023
received:
14
12
2022
accepted:
01
04
2023
medline:
17
7
2023
pubmed:
1
5
2023
entrez:
1
5
2023
Statut:
ppublish
Résumé
Bacterial spores are highly resilient and universally present on earth and can irreversibly enter the food chain to cause food spoilage or foodborne illness once revived to resume vegetative growth. Traditionally, extensive thermal processing has been employed to efficiently kill spores; however, the relatively high thermal load adversely affects food quality attributes. In recent years, the germination-inactivation strategy has been developed to mildly kill spores based on the circumstance that germination can decrease spore-resilient properties. However, the failure to induce all spores to geminate, mainly owing to the heterogeneous germination behavior of spores, hampers the success of applying this strategy in the food industry. Undoubtedly, elucidating the detailed germination pathway and underlying mechanism can fill the gap in our understanding of germination heterogeneity, thereby facilitating the development of full-scale germination regimes to mildly kill spores. In this review, we comprehensively discuss the mechanisms of spore germination of Bacillus and Clostridium species, and update the molecular basis of the early germination events, for example, the activation of germination receptors, ion release, Ca-DPA release, and molecular events, combined with the latest research evidence. Moreover, high hydrostatic pressure (HHP), an advanced non-thermal food processing technology, can also trigger spore germination, providing a basis for the application of a germination-inactivation strategy in HHP processing. Here, we also summarize the diverse germination behaviors and mechanisms of spores of Bacillus and Clostridium species under HHP, with the aim of facilitating HHP as a mild processing technology with possible applications in food sterilization. Practical Application: This work provides fundamental basis for developing efficient killing strategies of bacterial spores in food industry.
Identifiants
pubmed: 37125461
doi: 10.1111/1541-4337.13160
doi:
Types de publication
Review
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2728-2746Subventions
Organisme : National Natural Science Foundation of China
ID : 32001658
Organisme : National Natural Science Foundation of China
ID : 31872913
Organisme : Ministry of Agriculture and Rural Affairs of the People's Republic of China
ID : 13210317
Informations de copyright
© 2023 Institute of Food Technologists®.
Références
Adams, C. M., Eckenroth, B. E., Putnam, E. E., Doublié, S., & Shen, A. (2013). Structural and functional analysis of the CspB protease required for Clostridium spore germination. PLoS Pathogens, 9(2), e1003165. https://doi.org/10.1371/journal.ppat.1003165
Aertsen, A., Opstal, I. V., 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
Aganovic, K., Hertel, C., Vogel, R. F., Johne, R., Schlüter, O., Schwarzenbolz, U., Jäger, H., Holzhauser, T., Bergmair, J., Roth, A., Sevenich, R., Bandick, N., Kulling, S. E., Knorr, D., Engel, K.-H., & Heinz, V. (2021). Aspects of high hydrostatic pressure food processing: Perspectives on technology and food safety. Comprehensive Reviews in Food Science and Food Safety, 20(4), 3225-3266. https://doi.org/10.1111/1541-4337.12763
Akhtar, S., Paredes-Sabja, D., Torres, J. A., & Sarker, M. R. (2009). Strategy to inactivate Clostridium perfringens spores in meat products. Food Microbiology, 26(3), 272-277. https://doi.org/10.1016/j.fm.2008.12.011
Amon, J. D., Artzi, L., & Rudner, D. Z. (2022). Genetic evidence for signal transduction within the Bacillus subtilis GerA germinant receptor. Journal of Bacteriology, 204(2), e00470-00421. https://doi.org/10.1128/jb.00470-21
Amon, J. D., Yadav, A. K., Ramirez-Guadiana, F. H., Meeske, A. J., Cava, F., & Rudner, D. Z. (2020). SwsB and SafA are required for CwlJ-dependent spore germination in Bacillus subtilis. Journal of Bacteriology, 202(6), e00668-00619. https://doi.org/10.1128/JB.00668-19
Aronson, A. I., & Fitz-James, P. (1976). Structure and morphogenesis of the bacterial spore coat. Bacteriological Reviews, 40(2), 360-402. https://doi.org/10.1128/br.40.2.360-402.1976
Artzi, L., Alon, A., Brock, K. P., Green, A. G., Tam, A., Ramírez-Guadiana, F. H., Marks, D., Kruse, A., & Rudner, D. Z. (2021). Dormant spores sense amino acids through the B subunits of their germination receptors. Nature Communications, 12(1), 1-8. https://doi.org/10.1038/s41467-021-27235-2
Atrih, A., Zöllner, P., Allmaier, G., & Foster, S. J. (1996). Structural analysis of Bacillus subtilis 168 endospore peptidoglycan and its role during differentiation. Journal of Bacteriology, 178(21), 6173-6183. https://doi.org/10.1128/jb.178.21.6173-6183.1996
Bagyan, I., & Setlow, P. (2002). Localization of the cortex lytic enzyme CwlJ in spores of Bacillus subtilis. Journal of Bacteriology, 184(4), 1219-1224. https://doi.org/10.1128/jb.184.4.1219-1224.2002
Balasubramaniam, V. M. (2021). Process development of high pressure-based technologies for food: Research advances and future perspectives. Current Opinion in Food Science, 42, 270-277. https://doi.org/10.1016/j.cofs.2021.10.001
Baloh, M., Nerber, H. N., & Sorg, J. A. (2022). Imaging Clostridioides difficile spore germination and germination proteins. Journal of Bacteriology, 204(7), e00210-00222. https://doi.org/10.1128/jb.00210-22
Banawas, S., Paredes-Sabja, D., Korza, G., Li, Y., Hao, B., Setlow, P., & Sarker, M. R. (2013). The Clostridium perfringens germinant receptor protein GerKC is located in the spore inner membrane and is crucial for spore germination. Journal of Bacteriology, 195(22), 5084-5091. https://doi.org/10.1128/JB.00901-13
Behravan, J., Chirakkal, H., Masson, A., & Moir, A. (2000). Mutations in the gerP locus of Bacillus subtilis and Bacillus cereus affect access of germinants to their targets in spores. Journal of Bacteriology, 182(7), 1987-1994. https://doi.org/10.1128/JB.182.7.1987-1994.2000
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 and 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
Blinker, S., Vreede, J., Setlow, P., & Brul, S. (2021). Predicting the structure and dynamics of membrane protein GerAB from Bacillus subtilis. International Journal of Molecular Sciences, 22(7), 3793. https://doi.org/10.3390/ijms22073793
Boone, T., & Driks, A. (2016). Protein synthesis during germination: Shedding new light on a classical question. Journal of Bacteriology, 198(24), 3251-3253. https://doi.org/10.1128/JB.00721-16
Brown, K. L. (2000). Control of bacterial spores. British Medical Bulletin, 56(1), 158-171. https://doi.org/10.1258/0007142001902860
Brunt, J., Plowman, J., Gaskin, D. J., Itchner, M., Carter, A. T., & Peck, M. W. (2014). Functional characterisation of germinant receptors in Clostridium botulinum and Clostridium sporogenes presents novel insights into spore germination systems. PLoS Pathogens, 10(9), e1004382. https://doi.org/10.1371/journal.ppat.1004382
Brunt, J., van Vliet, A. H. M., van den Bos, F., Carter, A. T., & Peck, M. W. (2016). Diversity of the germination apparatus in Clostridium botulinum groups I, II, III, and IV. Frontiers in Microbiology, 7, 1702. https://doi.org/10.3389/fmicb.2016.01702
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), 2457-2464. https://doi.org/10.1128/JB.185.8.2457-2464.2003
Carlin, F. (2011). Origin of bacterial spores contaminating foods. Food Microbiology, 28(2), 177-182. https://doi.org/10.1016/j.fm.2010.07.008
Cebrián, G., Condón, S., & Mañas, P. (2017). Physiology of the inactivation of vegetative bacteria by thermal treatments: Mode of action, influence of environmental factors and inactivation kinetics. Foods, 6(12), 107. https://doi.org/10.3390/foods6120107
Chirakkal, H., O'Rourke, M., Atrih, A., Foster, S. J., & Moir, A. (2002). Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology, 148(8), 2383-2392. https://doi.org/10.1099/00221287-148-8-2383
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
Cohn, F. (1876). Untersuchungen über Bakterien IV. Beiträge zur Biologie der Bazillen. Beitrage zur Biol der Pflanz, 249-276.
Cooper, G. R., & Moir, A. (2011). Amino acid residues in the GerAB protein important in the function and assembly of the alanine spore germination receptor of Bacillus subtilis 168. Journal of Bacteriology, 193(9), 2261-2267. https://doi.org/10.1128/jb.01397-10
Daniels, J. K., Caldwell, T. P., Christensen, K. A., & Chumanov, G. (2006). Monitoring the kinetics of Bacillus subtilis endospore germination via surface-enhanced Raman scattering spectroscopy. Analytical Chemistry, 78(5), 1724-1729. https://doi.org/10.1021/ac052009v
Delbrück, A. I., Zhang, Y., Heydenreich, R., & Mathys, A. (2021). Bacillus spore germination at moderate high pressure: A review on underlying mechanisms, influencing factors, and its comparison with nutrient germination. Comprehensive Reviews in Food Science and Food Safety, 20(4), 4159-4181. https://doi.org/10.1111/1541-4337.12789
DeMarco, A. M., Korza, G., Granados, M. R., Mok, W. W. K., & Setlow, P. (2021). Dodecylamine rapidly kills of spores of multiple Firmicute species: Properties of the killed spores and the mechanism of the killing. Journal of Applied Microbiology, 131(6), 2612-2625. https://doi.org/10.1111/jam.15137
Donnelly, M. L., Fimlaid, K. A., & Shen, A. (2016). Characterization of Clostridium difficile spores lacking either SpoVAC or dipicolinic acid synthetase. Journal of Bacteriology, 198(11), 1694-1707. https://doi.org/10.1128/JB.00986-15
Doona, C. J., Feeherry, F. E., Kustin, K., Chen, H., Huang, R., Philip Ye, X., & Setlow, P. (2017). A quasi-chemical model for bacterial spore germination kinetics by high pressure. Food Engineering Reviews, 9(3), 122-142. https://doi.org/10.1007/s12393-016-9155-1
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
Driks, A. (1999). Bacillus subtilis spore coat. Microbiology and Molecular Biology Reviews, 63(1), 1-20. https://doi.org/10.1128/MMBR.63.1.1-20.1999
Driks, A. (2002). Maximum shields: The assembly and function of the bacterial spore coat. Trends in Microbiology, 10(6), 251-254. https://doi.org/10.1016/S0966-842X(02)02373-9
Ehrenberg, C. G. (1838). Die Infusionsthierchen als vollkommene organismen. Ein blick in das tiefere organische leben der natur (pp. 1795-1876). L. Voss. https://doi.org/10.5962/bhl.title.58475
Fimlaid, K. A., Jensen, O., Donnelly, M. L., Francis, M. B., Sorg, J. A., & Shen, A. (2015). Identification of a novel lipoprotein regulator of Clostridium difficile spore germination. PLoS Pathogens, 11(10), e1005239. https://doi.org/10.1371/journal.ppat.1005239
Francis, M. B., Allen, C. A., Shrestha, R., & Sorg, J. A. (2013). Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection. PLoS Pathogens, 9(5), e1003356. https://doi.org/10.1371/journal.ppat.1003356
Francis, M. B., Allen, C. A., & Sorg, J. A. (2015). Spore cortex hydrolysis precedes dipicolinic acid release during Clostridium difficile spore germination. Journal of Bacteriology, 197(14), 2276-2283. https://doi.org/10.1128/JB.02575-14
Francis, M. B., & Sorg, J. A. (2016). Dipicolinic acid release by germinating Clostridium difficile spores occurs through a mechanosensing mechanism. mSphere, 1(6), e00306-00316. https://doi.org/10.1128/mSphere.00306-16
Gao, X., Swarge, B. N., Roseboom, W., Setlow, P., Brul, S., & Kramer, G. (2022). Time-resolved proteomics of germinating spores of Bacillus cereus. International Journal of Molecular Sciences, 23(21), 13614. https://doi.org/10.3390/ijms232113614
Gao, Y., Barajas-Ornelas, R. D. C., Amon, J. D., Ramírez-Guadiana, F. H., Alon, A., Brock, K. P., Marks, D. S., Kruse, A. C., & Rudner, D. Z. (2022). The SpoVA membrane complex is required for dipicolinic acid import during sporulation and export during germination. Genes & Development, 36(9-10), 634-646. https://doi.org/10.1101/gad.349488.122
Ghosh, A., Manton, J. D., Mustafa, A. R., Gupta, M., Ayuso-Garcia, A., Rees, E. J., & Christie, G. (2018). Proteins encoded by the gerP operon are localized to the inner coat in Bacillus cereus spores and are dependent on GerPA and SafA for assembly. Applied and Environmental Microbiology, 84(14), e00760-00718. https://doi.org/10.1128/AEM.00760-18
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
Gould, G. W. (1970). Germination and the problem of dormancy. Journal of Applied Bacteriology, 33(1), 34-49. https://doi.org/10.1111/j.1365-2672.1970.tb05232.x
Gould, G. W. (1989). Heat-induced injury and inactivation. In G. W. Gould (Ed.), Mechanisms of action of food preservation procedures (pp. 11-42). Elsevier Applied Science.
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
Heffron, J. D., Sherry, N., & Popham, D. L. (2011). In vitro studies of peptidoglycan binding and hydrolysis by the Bacillus anthracis germination-specific lytic enzyme SleB. Journal of Bacteriology, 193(1), 125-131. https://doi.org/10.1128/JB.00869-10
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
Jing, X., Robinson, H. R., Heffron, J. D., Popham, D. L., & Schubot, F. D. (2012). The catalytic domain of the germination-specific lytic transglycosylase SleB from Bacillus anthracis displays a unique active site topology. Proteins: Structure, Function & Bioinformatics, 80(10), 2469-2475. https://doi.org/10.1002/prot.24140
Jungnickel, K. E., Parker, J. L., & Newstead, S. (2018). Structural basis for amino acid transport by the CAT family of SLC7 transporters. Nature Communications, 9(1), 1-12. https://doi.org/10.1038/s41467-018-03066-6
Kennedy, M. J., Reader, S. L., & Swierczynski, L. M. (1994). Preservation records of micro-organisms: Evidence of the tenacity of life. Microbiology, 140(10), 2513-2529. https://doi.org/10.1099/00221287-140-10-2513
Kevorkian, Y., & Shen, A. (2017). Revisiting the role of Csp family proteins in regulating Clostridium difficile spore germination. Journal of Bacteriology, 199(22), e00266-00217. https://doi.org/10.1128/JB.00266-17
Kikuchi, K., Galera-Laporta, L., Weatherwax, C., Lam, J. Y., Moon, E. C., Theodorakis, E. A., Garcia-Ojalvo, J., & Süel, G. M. (2022). Electrochemical potential enables dormant spores to integrate environmental signals. Science, 378(6615), 43-49. https://doi.org/10.1126/science.abl7484
Knorr, D., & Augustin, M. A. (2021). Food processing needs, advantages and misconceptions. Trends in Food Science & Technology, 108, 103-110. https://doi.org/10.1016/j.tifs.2020.11.026
Koch, R. (1876). Untersuchungen über Bakterien V. Die Aetiologie der Milzbrand-Krankheit, begründent auf die Entwicklungsgeschichte des Bacillus Anthracis. Beitrage zur Biol der Pflanz, 277-310.
Kochan, T. J., Somers, M. J., Kaiser, A. M., Shoshiev, M. S., Hagan, A. K., Hastie, J. L., Giordano, N. P., Smith, A. D., Schubert, A. M., Carlson, P. E. Jr., Hanna, P. C., & Carlson, P. E. Jr. (2017). Intestinal calcium and bile salts facilitate germination of Clostridium difficile spores. PLoS Pathogens, 13(7), e1006443. https://doi.org/10.1371/journal.ppat.1006443
Kohler, L. J., Quirk, A. V., Welkos, S. L., & Cote, C. K. (2018). Incorporating germination-induction into decontamination strategies for bacterial spores. Journal of Applied Microbiology, 124(1), 2-14. https://doi.org/10.1111/jam.13600
Kong, L., Doona, C. J., Setlow, P., & Li, Y.-Q. (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., Setlow, P., & Li, Y.-Q. (2010). Characterization of bacterial spore germination using integrated phase contrast microscopy, Raman spectroscopy, and optical tweezers. Analytical Chemistry, 82(9), 3840-3847. https://doi.org/10.1021/ac1003322
Korza, G., Abini-Agbomson, S., Setlow, B., Shen, A., & Setlow, P. (2017). Levels of L-malate and other low molecular weight metabolites in spores of Bacillus species and Clostridium difficile. PLoS One, 12(8), e0182656. https://doi.org/10.1371/journal.pone.0182656
Korza, G., Goulet, M., DeMarco, A., Wicander, J., & Setlow, P. (2023). Role of Bacillus subtilis spore core water content and pH in the accumulation and utilization of spores' large 3-phosphoglyceric acid depot, and the crucial role of this depot in generating ATP early during spore germination. Microorganisms, 11(1), 195. https://doi.org/10.3390/microorganisms11010195
Korza, G., Setlow, B., Rao, L., Li, Q., & Setlow, P. (2016). Changes in Bacillus spore small Molecules, rRNA, germination, and outgrowth after extended sublethal exposure to various temperatures: Evidence that protein synthesis is not essential for spore germination. Journal of Bacteriology, 198(24), 3254-3264. https://doi.org/10.1128/JB.00583-16
Korza, G., & Setlow, P. (2013). Topology and accessibility of germination proteins in the Bacillus subtilis spore inner membrane. Journal of Bacteriology, 195(7), 1484-1491. https://doi.org/10.1128/JB.02262-12
Lawler, A. J., Lambert, P. A., & Worthington, T. (2020). A revised understanding of Clostridioides difficile spore germination. Trends in Microbiology, 28(9), 744-752. https://doi.org/10.1016/j.tim.2020.03.004
Lenz, C. A., Reineke, K., Knorr, D., & Vogel, R. F. (2015). High pressure thermal inactivation of Clostridium botulinum type E endospores-Kinetic modeling and mechanistic insights. Frontiers in Microbiology, 6, 652. https://doi.org/10.3389/fmicb.2015.00652
Li, Y., Butzin, X. Y., Davis, A., Setlow, B., Korza, G., Üstok, F. I., Christie, G., Setlow, P., & Hao, B. (2013). Activity and regulation of various forms of CwlJ, SleB, and YpeB proteins in degrading cortex peptidoglycan of spores of Bacillus Species in vitro and during spore germination. Journal of Bacteriology, 195(11), 2530-2540. https://doi.org/10.1128/JB.00259-13
Li, Y., Davis, A., Korza, G., Zhang, P., Li, Y.-Q., Setlow, B., Setlow, P., & Hao, B. (2012). Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis. Journal of Bacteriology, 194(8), 1875-1884. https://doi.org/10.1128/JB.00062-12
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, Y., Davis, A., Korza, G., Zhang, P., Li, Y.-Q., Setlow, B., Setlow, P., & Hao, B. (2019). Structural and functional analyses of the N-terminal domain of the A subunit of a Bacillus megaterium spore germinant receptor. Proceedings of the National Academy of Sciences, USA, 116(23), 11470-11479. https://doi.org/10.1128/JB.00062-12
Li, Y., Jin, K., Setlow, B., Setlow, P., & Hao, B. (2012). Crystal structure of the catalytic domain of the Bacillus cereus SleB protein, important in cortex peptidoglycan degradation during spore germination. Journal of Bacteriology, 194(17), 4537-4545. https://doi.org/10.1128/JB.00877-12
Ling, B., Tang, J., Kong, F., Mitcham, E. J., & Wang, S. (2015). Kinetics of food quality changes during thermal processing: A review. Food and Bioprocess Technology, 8(2), 343-358. https://doi.org/10.1007/s11947-014-1398-3
Luu, S., & Setlow, P. (2014). Analysis of the loss in heat and acid resistance during germination of spores of Bacillus species. Journal of Bacteriology, 196(9), 1733-1740. https://doi.org/10.1128/JB.01555-14
McCann, K. P., Robinson, C., Sammons, R. L., Smith, D. A., & Corfe, B. M. (1996). Alanine germination receptors of Bacillus subtailis. Letters in Applied Microbiology, 23(5), 290-294. https://doi.org/10.1111/j.1472-765X.1996.tb00192.x
McKenney, P. T., Driks, A., & Eichenberger, P. (2013). The Bacillus subtilis endospore: Assembly and functions of the multilayered coat. Nature Reviews Microbiology, 11(1), 33-44. https://doi.org/10.1038/nrmicro2921
Messens, W., Van Camp, J., & Huyghebaert, A. (1997). The use of high pressure to modify the functionality of food proteins. Trends in Food Science & Technology, 8(4), 107-112. https://doi.org/10.1016/S0924-2244(97)01015-7
Mills, G., Earnshaw, R., & Patterson, M. (1998). Effects of high hydrostatic pressure on Clostridium sporogenes spores. Letters in Applied Microbiology, 26(3), 227-230. https://doi.org/10.1046/j.1472-765X.1998.00329.x
Moir, A., & Cooper, G. (2016). Spore germination. In A. Driks & P. Eichenberger (Eds.), The bacterial spore: From molecules to systems (pp. 217-236). American Society for Microbiology. https://doi.org/10.1128/9781555819323.ch11
Moir, A., Corfe, B., & Behravan, J. (2002). Spore germination. Cellular and Molecular Life Sciences, 59(3), 403-409. https://doi.org/10.1007/s00018-002-8432-8
Moir, A., Kemp, E. H., Robinson, C., & Corfe, B. M. (1994). The genetic analysis of bacterial spore germination. Journal of Applied Bacteriology, 76, 9S-16S. https://doi.org/10.1111/j.1365-2672.1994.tb04353.x
Moir, A., Lafferty, E., & Smith, D. A. (1979). Genetic analysis of spore germination mutants of Bacillus subtilis 168: The correlation of phenotype with map location. Microbiology, 111(1), 165-180. https://doi.org/10.1099/00221287-111-1-165
Mokashi, S., Kanaan, J., Craft, D. L., Byrd, B., Zenick, B., Laue, M., Korza, G., Mok, W. W. K., & Setlow, P. (2020). Killing of bacterial spores by dodecylamine and its effects on spore inner membrane properties. Journal of Applied Microbiology, 129(6), 1511-1522. https://doi.org/10.1111/jam.14732
Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews, 64(3), 548-572. https://doi.org/10.1128/MMBR.64.3.548-572.2000
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
Orsburn, B., Sucre, K., Popham, D. L., & Melville, S. B. (2009). The SpmA/B and DacF proteins of Clostridium perfringens play important roles in spore heat resistance. FEMS Microbiology Letters, 291(2), 188-194. https://doi.org/10.1111/j.1574-6968.2008.01454.x
Paidhungat, M., Ragkousi, K., & Setlow, P. (2001). Genetic requirements for induction of germination of spores of Bacillus subtilis by Ca(2+)-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, 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). Spore germination and outgrowth. In A. L. Sonenshein, J. A. Hoch, & R. Losick (Eds.), Bacillus subtilis and its closest relatives (pp. 537-548). American Society for Microbiology. https://doi.org/10.1128/9781555817992.ch37
Paredes-Sabja, D., Setlow, B., Setlow, P., & Sarker, M. R. (2008). Characterization of Clostridium perfringens spores that lack SpoVA proteins and dipicolinic acid. Journal of Bacteriology, 190(13), 4648-4659. https://doi.org/10.1128/JB.00325-08
Paredes-Sabja, D., Setlow, P., & Sarker, M. R. (2009a). Role of GerKB in germination and outgrowth of Clostridium perfringens spores. Applied and Environmental Microbiology, 75(11), 3813-3817. https://doi.org/10.1128/AEM.00048-09
Paredes-Sabja, D., Setlow, P., & Sarker, M. R. (2009b). SleC is essential for cortex peptidoglycan hydrolysis during germination of spores of the pathogenic bacterium Clostridium perfringens. Journal of Bacteriology, 191(8), 2711-2720. https://doi.org/10.1128/JB.01832-08
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
Paredes-Sabja, D., Torres, J. A., Setlow, P., & Sarker, M. R. (2008). Clostridium perfringens spore germination: Characterization of germinants and their receptors. Journal of Bacteriology, 190(4), 1190-1201. https://doi.org/10.1128/JB.01748-07
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
Popham, D. L., Helin, J., Costello, C. E., & Setlow, P. (1996a). Analysis of the peptidoglycan structure of Bacillus subtilis endospores. Journal of Bacteriology, 178(22), 6451-6458. https://doi.org/10.1128/jb.178.22.6451-6458.1996
Popham, D. L., Helin, J., Costello, C. E., & Setlow, P. (1996b). Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proceedings of the National Academy of Sciences, USA, 93(26), 15405-15410. https://doi.org/10.1073/pnas.93.26.15405
Postollec, F., Mathot, A.-G., Bernard, M., Divanac'h, M.-L., Pavan, S., & Sohier, D. (2012). Tracking spore-forming bacteria in food: From natural biodiversity to selection by processes. International Journal of Food Microbiology, 158(1), 1-8. https://doi.org/10.1016/j.ijfoodmicro.2012.03.004
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
Rao, L., Zhou, B., Serruya, R., Moussaieff, A., Sinai, L., & Ben-Yehuda, S. (2022). Glutamate catabolism during sporulation determines the success of the future spore germination. iScience, 25(10), 105242. https://doi.org/10.1016/j.isci.2022.105242
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 & 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). The impact of high pressure and temperature on bacterial spores: Inactivation mechanisms of Bacillus subtilis above 500 MPa. Journal of Food Science, 76(3), M189-M197. https://doi.org/10.1111/j.1750-3841.2011.02066.x
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
Rosenberg, A., Soufi, B., Ravikumar, V., Soares, N. C., Krug, K., Smith, Y., Macek, B., & Ben-Yehuda, S. (2015). Phosphoproteome dynamics mediate revival of bacterial spores. BMC Biology, 13(1), 76. https://doi.org/10.1186/s12915-015-0184-7
Saif Zaman, M., Goyal, A., Prakash Dubey, G., Gupta, P. K., Chandra, H., Das, T. K., Ganguli, M., & Singh, Y. (2005). Imaging and analysis of Bacillus anthracis spore germination. Microscopy Research and Technique, 66(6), 307-311. https://doi.org/10.1002/jemt.20174
Sanchez-Salas, J.-L., & Setlow, P. (1993). Proteolytic processing of the protease which initiates degradation of small, acid-soluble proteins during germination of Bacillus subtilis spores. Journal of Bacteriology, 175(9), 2568-2577. https://doi.org/10.1128/jb.175.9.2568-2577.1993
Sarker, M. R., Akhtar, S., Torres, J. A., & Paredes-Sabja, D. (2015). High hydrostatic pressure-induced inactivation of bacterial spores. Critical Reviews in Microbiology, 41(1), 18-26. https://doi.org/10.3109/1040841x.2013.788475
Segev, E., Rosenberg, A., Mamou, G., Sinai, L., & Ben-Yehuda, S. (2013). Molecular kinetics of reviving bacterial spores. Journal of Bacteriology, 195(9), 1875-1882. https://doi.org/10.1128/JB.00093-13
Setlow, B., Cowan, A. E., & Setlow, P. (2003). Germination of spores of Bacillus subtilis with dodecylamine. Journal of Applied Microbiology, 95(3), 637-648. https://doi.org/10.1046/j.1365-2672.2003.02015.x
Setlow, P. (1981). Biochemistry of bacterial forespore development and spore germination. Sporulation and germination (pp. 13-28). American Society for Microbiology.
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). 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., Wang, S., & Li, Y.-Q. (2017). Germination of spores of the orders Bacillales and Clostridiales. Annual Review of Microbiology, 71, 459-477. https://doi.org/10.1146/annurev-micro-090816-093558
Shah, I. M., Laaberki, M.-H., Popham, D. L., & Dworkin, J. (2008). A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell, 135(3), 486-496. https://doi.org/10.1016/j.cell.2008.08.039
Shen, A. (2020). Clostridioides difficile spore formation and germination: new insights and opportunities for intervention. Annual Review of Microbiology, 74(1), 545-566. https://doi.org/10.1146/annurev-micro-011320-011321
Shen, A., Edwards, A. N., Sarker, M. R., & Paredes-Sabja, D. (2019). Sporulation and germination in Clostridial pathogens. Microbiology Spectrum, 7(6), 7.6.3. https://doi.org/10.1128/microbiolspec.GPP3-0017-2018
Shimamoto, S., Moriyama, R., Sugimoto, K., Miyata, S., & Makino, S. (2001). Partial characterization of an enzyme fraction with protease activity which converts the spore peptidoglycan hydrolase (SleC) precursor to an active enzyme during germination of Clostridium perfringens S40 spores and analysis of a gene cluster involved in the activity. Journal of Bacteriology, 183(12), 3742-3751. https://doi.org/10.1128/JB.183.12.3742-3751.2001
Shinde, U., & Thomas, G. (2011). Insights from bacterial subtilases into the mechanisms of intramolecular chaperone-mediated activation of furin. In M. Mbikay & N. G. Seidah (Eds.), Proprotein convertases (pp. 59-106). Humana Press. https://doi.org/10.1007/978-1-61779-204-5_4
Shrestha, R., Cochran, A. M., & Sorg, J. A. (2019). The requirement for co-germinants during Clostridium difficile spore germination is influenced by mutations in yabG and cspA. PLoS Pathogens, 15(4), e1007681. https://doi.org/10.1371/journal.ppat.1007681
Shrestha, R., & Sorg, J. A. (2018). Hierarchical recognition of amino acid co-germinants during Clostridioides difficile spore germination. Anaerobe, 49, 41-47. https://doi.org/10.1016/j.anaerobe.2017.12.001
Sinai, L., & Ben-Yehuda, S. (2016). Commentary: Changes in Bacillus spore small molecules, rRNA, germination, and outgrowth after extended sublethal exposure to various temperatures: Evidence that protein synthesis is not essential for spore germination. Frontiers in Microbiology, 7, 2043. https://doi.org/10.3389/fmicb.2016.02043
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
Sorg, J. A., & Sonenshein, A. L. (2008). Bile salts and glycine as cogerminants for Clostridium difficile spores. Journal of Bacteriology, 190(7), 2505-2512. https://doi.org/10.1128/JB.01765-07
Stewart, B. T., & Halvorson, H. O. (1953). Studies on the spores of aerobic bacteria I: The occurrence of alanine racemase. Journal of Bacteriology, 65(2), 160-166. https://doi.org/10.1128/jb.65.2.160-166.1953
Stragier, P., & Losick, R. (1996). Molecular genetics of sporulation in Bacillus subtilis. Annual Review of Genetics, 30, 297-241. https://doi.org/10.1146/annurev.genet.30.1.297
Swarge, B., Abhyankar, W., Jonker, M., Hoefsloot, H., Kramer, G., Setlow, P., Brul, S., & Koning, L. J. D. (2020). Integrative analysis of proteome and transcriptome dynamics during Bacillus subtilis spore revival. mSphere, 5(4), e00463-00420. https://doi.org/10.1128/mSphere.00463-20
Swarge, B., Nafid, C., Vischer, N., Kramer, G., Setlow, P., & Brul, S. (2020). Investigating synthesis of the MalS malic enzyme during Bacillus subtilis spore germination and outgrowth and the influence of spore maturation and sporulation conditions. mSphere, 5(4), e00464-00420. https://doi.org/10.1128/mSphere.00464-20
Talukdar, P. K., & Sarker, M. R. (2020). The serine proteases CspA and CspC are essential for germination of spores of Clostridium perfringens SM101 through activating SleC and cortex hydrolysis. Food Microbiology, 86, 103325. https://doi.org/10.1016/j.fm.2019.103325
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
Venkatasubramanian, P., & Johnstone, K. (1993). Biochemical analysis of germination mutants to characterize germinant receptors of Bacillus subtilis 1604 spores. Microbiology, 139(8), 1921-1926. https://doi.org/10.1099/00221287-139-8-1921</b1ib>
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
Vepachedu, V. R., & Setlow, P. (2007a). Analysis of interactions between nutrient germinant receptors and SpoVA proteins of Bacillus subtilis spores. FEMS Microbiology Letters, 274(1), 42-47. https://doi.org/10.1111/j.1574-6968.2007.00807.x
Vepachedu, V. R., & Setlow, P. (2007b). Role of SpoVA proteins in release of dipicolinic acid during germination of Bacillus subtilis spores triggered by dodecylamine or lysozyme. Journal of Bacteriology, 189(5), 1565-1572. https://doi.org/10.1128/JB.01613-06
Vercammen, A., Vivijs, B., Lurquin, I., & Michiels, C. W. (2012). Germination and inactivation of Bacillus coagulans and Alicyclobacillus acidoterrestris spores by high hydrostatic pressure treatment in buffer and tomato sauce. International Journal of Food Microbiology, 152(3), 162-167. https://doi.org/10.1016/j.ijfoodmicro.2011.02.019
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(6806), 897-900. https://doi.org/10.1038/35038060
Wang, S., Setlow, P., & Li, Y.-Q. (2015). Slow Leakage of Ca-dipicolinic acid from individual Bacillus spores during initiation of spore germination. Journal of Bacteriology, 197(6), 1095-1103. https://doi.org/10.1128/JB.02490-14
Warth, A. D., & Strominger, J. L. (1972). Structure of the peptidoglycan from spores of Bacillus subtilis. Biochemistry, 11(8), 1389-1396. https://doi.org/10.1021/bi00758a010
Wu, X., Grover, N., Paskaleva, E. E., Mundra, R. V., Page, M. A., Kane, R. S., & Dordick, J. S. (2015). Characterization of the activity of the spore cortex lytic enzyme CwlJ1. Biotechnology and Bioengineering, 112(7), 1365-1375. https://doi.org/10.1002/bit.25565
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. https://doi.org/10.1128/AEM.64.9.3220-3224.1998
Xing, Y., & Harper, W. F. Jr. (2020). Bacillus spore awakening: Recent discoveries and technological developments. Current Opinion in Biotechnology, 64, 110-115. https://doi.org/10.1016/j.copbio.2019.12.024
Yang, P., Rao, L., Zhao, L., Wu, X., Wang, Y., & Liao, X. (2021). High pressure processing combined with selected hurdles: Enhancement in the inactivation of vegetative microorganisms. Comprehensive Reviews in Food Science and Food Safety, 20(2), 1800-1828. https://doi.org/10.1111/1541-4337.12724
Yasuda, Y., Kanda, K., Nishioka, S., Tanimoto, Y., Kato, C., Saito, A., Fukuchi, S., Nakanishi, Y., & Tochikubo, K. (1993). Regulation of L-alanine-initiated germination of Bacillus subtilis spores by alanine racemase. Amino Acids, 4(1), 89-99. https://doi.org/10.1007/BF00805804
Yi, X., & Setlow, P. (2010). Studies of the commitment step in the germination of spores of Bacillus species. Journal of Bacteriology, 192(13), 3424-3433. https://doi.org/10.1128/JB.00326-10
Zhang, J.-Q., Griffiths, K. K., Cowan, A., Setlow, P., & Yu, J. (2013). Expression level of Bacillus subtilis germinant receptors determines the average rate but not the heterogeneity of spore germination. Journal of Bacteriology, 195(8), 1735-1740. https://doi.org/10.1128/JB.02212-12
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., 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. (2019). 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
Zhou, B., Alon, S., Rao, L., Sinai, L., & Ben-Yehuda, S. (2022). Reviving the view: Evidence that macromolecule synthesis fuels bacterial spore germination. microLife, 3, uqac004. https://doi.org/10.1093/femsml/uqac004
Zhou, B., Semanjski, M., Orlovetskie, N., Bhattacharya, S., Alon, S., Argaman, L., Jarrous, N., Zhang, Y., Macek, B., Sinai, L., & Ben-Yehuda, S. (2019). Arginine dephosphorylation propels spore germination in bacteria. Proceedings of the National Academy of Sciences, USA, 116(28), 14228-14237. https://doi.org/10.1073/pnas.1817742116