Spore germination

The Bacterial Spore: From Molecules to Systems

Volumn , Issue , 2016, Pages 217-236

  Moir, Anne ^a   Cooper, Gareth ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

B. cereus sensu lato; B. subtilis; Clostridia; Germinant receptor; Lipid environment; Spore germination

Indexed keywords

EID: 85049957384     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1128/9781555819323.ch11     Document Type: Chapter

References (202)

1. Setlow P. 2006. Spores of Bacillus subtilis:their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101:514-525.
2. Moir A, Corfe BM, Behravan J. 2002. Spore germination. Cell Mol Life Sci 59:403-409.
3. Paidhungat M, Setlow P. 2002. Spore germination and outgrowth, p 537-548. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and Its Closest Relatives:From Genes to Cells. ASM Press, Washington, DC.
4. Setlow P. 2013. Summer meeting 201-when the sleepers wake:the germination of spores of Bacillus species. J Appl Microbiol 115:1251-1268.
5. Setlow P. 2014. Germination of spores of Bacillus species:what we know and do not know. J Bacteriol 196:1297-1305.
6. Woese CR, Morowitz HJ, Hutchison CA III. 1958. Analysis of action of L-alanine analogues in spore germination. J Bacteriol 76:578-588.
7. Foerster HF, Foster JW. 1966. Response of Bacillus spores to combinations of germinative compounds. J Bacteriol 91:1168-1177.
8. Gould GW. 1969. Germination, p 397-444. In Gould GW, Hurst A (ed), The Bacterial Spore. Academic Press Inc, London, United Kingdom.
9. Setlow P. 1983. Germination and outgrowth, p 211254. In Hurst A, Gould GW (ed), The Bacterial Spore, vol 2. Academic Press, London, United Kingdom.
10. Moir A, Smith DA. 1990. The genetics of bacterial spore germination. Annu Rev Microbiol 44:531-553.
11. Setlow P. 2003. Spore germination. Curr Opin Microbiol 6:550-556.
12. Carr KA, Lybarger SR, Anderson EC, Janes BK, Hanna PC. 2010. The role of Bacillus anthracis germinant receptors in germination and virulence. Mol Microbiol 75:365-375.
13. Ross C, Abel-Santos E. 2010. The Ger receptor family from sporulating bacteria. Curr Issues Mol Biol 12:147-158.
14. Paredes-Sabja D, Setlow P, Sarker MR. 2011. Germination of spores of Bacillales and Clostridiales species:mechanisms and proteins involved. Trends Microbiol 19:85-94.
15. Peck MW, Stringer SC, Carter AT. 2011. Clostridium botulinum in the post-genomic era. Food Microbiol 28:183-191.
16. Abee T, Groot MN, Tempelaars M, Zwietering M, Moezelaar R, van der Voort M. 2011. Germination and outgrowth of spores of Bacillus cereus group members:diversity and role of germinant receptors. Food Microbiol 28:199-208.
17. Xiao Y, Francke C, Abee T, Wells-Bennik MH. 2011. Clostridial spore germination versus bacilli:genome mining and current insights. Food Microbiol 28:266-274.
18. Paredes-Sabja D, Torres JA, Setlow P, Sarker MR. 2008. Clostridium perfringens spore germination:characterization of germinants and their receptors. J Bacteriol 190:1190-1201.
19. Paidhungat M, Ragkousi K, Setlow P. 2001. Genetic requirements for induction of germination of spores of Bacillus subtilis by Ca(2+)-dipicolinate. J Bacteriol 183:4886-4893.
20. Popham DL, Meador-Parton J, Costello CE, Setlow P. 1999. Spore peptidoglycan structure in a cwlD dacB double mutant of Bacillus subtilis. J Bacteriol 181:6205-6209.
21. Setlow B, Cowan AE, Setlow P. 2003. Germination of spores of Bacillus subtilis with dodecylamine. J Appl Microbiol 95:637-648.
22. Paidhungat M, Setlow B, Daniels WB, Hoover D, Papafragkou E, Setlow P. 2002. Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. Appl Environ Microbiol 68:3172-3175.
23. Dworkin J, Shah IM. 2010. Exit from dormancy in microbial organisms. Nat Rev Microbiol 8:890-896.
24. Shah IM, Laaberki MH, Popham DL, Dworkin J. 2008. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486-496.
25. Vary JC, Halvorson HO. 1965. Kinetics of germination of Bacillus spores. J Bacteriol 89:1340-1347.
26. Hashimoto T, Frieben WR, Conti SF. 1969. Microgermination of Bacillus cereus spores. J Bacteriol 100:1385-1392.
27. Kong L, Zhang P, Wang G, Yu J, Setlow P, Li YQ. 2011. Characterization of bacterial spore germination using phase-contrast and fluorescence microscopy, Raman spectroscopy and optical tweezers. Nat Protoc 6:625-639.
28. Zhang P, Kong L, Wang G, Scotland M, Ghosh S, Setlow B, Setlow P, Li YQ. 2012. Analysis of the slow germination of multiple individual superdormant Bacillus subtilis spores using multifocus Raman microspectroscopy and differential interference contrast microscopy. J Appl Microbiol 112:526-536.
29. Zhang P, Garner W, Yi X, Yu J, Li YQ, 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. J Bacteriol 192:3608-3619.
30. Ghosh S, Setlow P. 2009. Isolation and characterization of superdormant spores of Bacillus species. J Bacteriol 191:1787-1797.
31. Ghosh S, Setlow P. 2010. The preparation, germination properties and stability of superdormant spores of Bacillus cereus. J Appl Microbiol 108:582-590.
32. Ghosh S, Zhang P, Li YQ, Setlow P. 2009. Superdormant spores of Bacillus species have elevated wet-heat resistance and temperature requirements for heat activation. J Bacteriol 191:5584-5591.
33. Ghosh S, Scotland M, Setlow P. 2012. Levels of germination proteins in dormant and superdormant spores of Bacillus subtilis. J Bacteriol 194:2221-2227.
34. Setlow P, Liu G, Faeder JR. 2012. Heterogeneity in bacterial spore populations, p 119-214. In Abel-Santos E (ed), Bacterial Spores:Current Research and Applications. Caister Academic Press, Poole, United Kingdom.
35. Eijlander RT, Abee T, Kuipers OP. 2011. Bacterial spores in food:how phenotypic variability complicates prediction of spore properties and bacterial behavior. Curr Opin Biotechnol 22:180-186.
36. Stringer SC, Webb MD, Peck MW. 2009. Contrasting effects of heat treatment and incubation temperature on germination and outgrowth of individual spores of nonproteolytic Clostridium botulinum bacteria. Appl Environ Microbiol 75:2712-2719.
37. Stringer SC, Webb MD, Peck MW. 2011. Lag time variability in individual spores of Clostridium botulinum. Food Microbiol 28:228-235.
38. Planchon S, Dargaignaratz C, Levy C, Ginies C, Broussolle V, Carlin F. 2011. Spores of Bacillus cereus strain KBAB4 produced at 10 °C and 30 °C display variations in their properties. Food Microbiol 28:291-297.
39. Melly E, Genest PC, Gilmore ME, Little S, Popham DL, Driks A, Setlow P. 2002. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J Appl Microbiol 92:1105-1115.
40. Rose R, Setlow B, Monroe A, Mallozzi M, Driks A, Setlow P. 2007. Comparison of the properties of Bacillus subtilis spores made in liquid or on agar plates. J Appl Microbiol 103:691-699.
41. Sanchez-Salas JL, Setlow B, Zhang P, Li YQ, Setlow P. 2011. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl Environ Microbiol 77:67466754.
42. Alzahrani OM, Moir A. 2014. Spore germination and germinant receptor genes in wild strains of Bacillus subtilis. J Appl Microbiol 117:741-749.
43. Okugawa S, Moayeri M, Pomerantsev AP, Sastalla I, Crown D, Gupta PK, Leppla SH. 2012. Lipoprotein biosynthesis by prolipoprotein diacylglyceryl transferase is required for efficient spore germination and full virulence of Bacillus anthracis. Mol Microbiol 83:96-109.
44. Sastalla I, Rosovitz MJ, Leppla SH. 2010. Accidental selection and intentional restoration of sporulation-deficient Bacillus anthracis mutants. Appl Environ Microbiol 76:6318-6321.
45. Moir A, Lafferty E, Smith DA. 1979. Genetics analysis of spore germination mutants of Bacillus subtilis 168:the correlation of phenotype with map location. J Gen Microbiol 111:165-180.
46. Keynan A, Evenchick Z. 1969. Activation, p 359-396. In Gould GW, Hurst A (ed), The Bacterial Spore. Academic Press, London, United Kingdom.
47. Busta FF, Ordal ZJ. 1964. Heat-activation kinetics of endospores of Bacillus subtilis. J Food Sci 29:345-353.
48. Foerster HF. 1983. Activation and germination characteristics observed in endospores of thermophilic strains of Bacillus. Arch Microbiol 134:175-181.
49. Foerster HF. 1985. The effects of alterations in the suspending medium on low-temperature activation of spores of Bacillus stearothermophilus-NGB101. Arch Microbiol 142:185-189.
50. Luu S, Cruz-Mora J, Setlow B, Feeherry FE, Doona CJ, Setlow P. 2015. The effects of heat activation on Bacillus spore germination, with nutrients or under high pressure, with or without various germination proteins. Appl Environ Microbiol 81:2927-2938.
51. 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. J Bacteriol 182:1987-1994.
52. Popham DL, Illades-Aguiar B, Setlow P. 1995. The Bacillus subtilis dacB gene, encoding penicillin-binding protein 5, is part of a three-gene operon required for proper spore cortex synthesis and spore core dehydration. J Bacteriol 177:4721-4729.
53. Orsburn B, Sucre K, Popham DL, Melville SB. 2009. The SpmA/B and DacF proteins of Clostridium per-fringens play important roles in spore heat resistance. FEMS Microbiol Lett 291:188-194.
54. Scott IR, Ellar DJ. 1978. Metabolism and the triggering of germination of Bacillus megaterium. Use of L-[3H] alanine and tritiated water to detect metabolism. Bio-chem J 174:635-640.
55. Sinai L, Rosenberg A, Smith Y, Segev E, Ben-Yehuda S. 2015. The molecular timeline of a reviving bacterial spore. Mol Cell 57:695-707.
56. Carr KA, Janes BK, Hanna PC. 2010. Role of the gerP operon in germination and outgrowth of Bacillus anthracis spores. PLoS One 5:e9128. doi:10.1371/jour-nal.pone.0009128.
57. 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 4:89-99.
58. Chesnokova ON, McPherson SA, Steichen CT, Turnbough CL Jr. 2009. The spore-specific alanine rac-emase of Bacillus anthracis and its role in suppressing germination during spore development. J Bacteriol 191:1303-1310.
59. Doona CJ, Ghosh S, Feeherry FF, 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. J Appl Microbiol 117:711-720.
60. Yi X, Setlow P. 2010. Studies of the commitment step in the germination of spores of bacillus species. J Bacteriol 192:3424-3433.
61. Swerdlow BM, Setlow B, Setlow P. 1981. Levels of H+ and other monovalent cations in dormant and germinating spores of Bacillus megaterium. J Bacteriol 148:20-29.
62. Magill NG, Cowan AE, Leyva-Vazquez MA, Brown M, Koppel DE, Setlow P. 1996. Analysis of the relationship between the decrease in pH and accumulation of 3-phosphoglyceric acid in developing forespores of Bacillus species. J Bacteriol 178:2204-2210.
63. Popham DL, Helin J, Costello CE, Setlow P. 1996. Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proc Natl Acad Sci USA 93:15405-15410.
64. Li Y, Davis A, Korza G, Zhang P, Li YQ, Setlow B, Setlow P, Hao B. 2012. Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 194:1875-1884.
65. Tovar-Rojo F, Chander M, Setlow B, Setlow P. 2002. The products of the spoVA operon are involved in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 184:584-587.
66. Perez-Valdespino A, Li Y, Setlow B, Ghosh S, Pan D, Korza G, Feeherry FE, Doona CJ, Li Y-Q, Hao B, Setlow P. 2014. Function of the SpoVAEa and SpoVAF proteins of Bacillus subtilis spores. J Bacteriol 196:2077-2088.
67. Velasquez J, Schuurman-Wolters G, Birkner JP, Abee T, Poolman B. 2014. Bacillus subtilis spore protein SpoVAC functions as a mechanosensitive channel. Mol Microbiol 92:813-823.
68. Setlow B, Wahome PG, Setlow P. 2008. Release of small molecules during germination of spores of Bacillus species. J Bacteriol 190:4759-4763.
69. Cowan AE, Koppel DE, Setlow B, Setlow P. 2003. A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores:implications for spore dormancy. Proc Natl Acad Sci USA 100:4209-4214.
70. Cowan AE, Olivastro EM, Koppel DE, Loshon CA, Setlow B, Setlow P. 2004. Lipids in the inner membrane of dormant spores of Bacillus species are largely immobile. Proc Natl Acad Sci USA 101:7733-7738.
71. Boland FM, Atrih A, Chirakkal H, Foster SJ, Moir A. 2000. Complete spore-cortex hydrolysis during germination of Bacillus subtilis 168 requires SleB and YpeB. Microbiology 146:57-64.
72. Chirakkal H, O'Rourke M, Atrih A, Foster SJ, Moir A. 2002. Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology 148:2383-2392.
73. Fukushima T, Yamamoto H, Atrih A, Foster SJ, Sekiguchi J. 2002. A polysaccharide deacetylase gene (pdaA) is required for germination and for production of muramic delta-lactam residues in the spore cortex of Bacillus subtilis. J Bacteriol 184:6007-6015.
74. Zhang P, Thomas S, Li YQ, Setlow P. 2012. Effects of cortex peptidoglycan structure and cortex hydrolysis on the kinetics of Ca(2+)-dipicolinic acid release during Bacillus subtilis spore germination. J Bacteriol 194:646-652.
75. Moriyama R, Fukuoka H, Miyata S, Kudoh S, Hattori A, Kozuka S, Yasuda Y, Tochikubo K, Makino S. 1999. Expression of a germination-specific amidase, SleB, of bacilli in the forespore compartment of sporulating cells and its localization on the exterior side of the cortex in dormant spores. J Bacteriol 181:2373-2378.
76. Atrih A, Foster SJ. 2001. In vivo roles of the germination-specific lytic enzymes of Bacillus subtilis 168. Microbiology 147:2925-2932.
77. Heffron JD, Lambert EA, Sherry N, Popham DL. 2010. Contributions of four cortex lytic enzymes to germination of Bacillus anthracis spores. J Bacteriol 192:763-770.
78. Heffron JD, Orsburn B, Popham DL. 2009. Roles of germination-specific lytic enzymes CwlJ and SleB in Bacillus anthracis. J Bacteriol 191:2237-2247.
79. Giebel JD, Carr KA, Anderson EC, Hanna PC. 2009. The germination-specific lytic enzymes SleB, CwlJ1, and CwlJ2 each contribute to Bacillus anthracis spore germination and virulence. J Bacteriol 191:5569-5576.
80. Setlow B, Peng L, Loshon CA, Li YQ, Christie G, Setlow P. 2009. Characterization of the germination of Bacillus megaterium spores lacking enzymes that degrade the spore cortex. J Appl Microbiol 107:318-328.
81. Christie G, Ustok FI, Lu Q, Packman LC, Lowe CR. 2010. Mutational analysis of Bacillus megaterium QM B1551 cortex-lytic enzymes. J Bacteriol 192:53785389.
82. Ragkousi K, Eichenberger P, van Ooij C, Setlow P. 2003. Identification of a new gene essential for germination of Bacillus subtilis spores with Ca2+-dipicolinate. J Bacteriol 185:2315-2329.
83. Bernhards CB, Popham DL. 2014. Role of YpeB in cortex hydrolysis during germination of Bacillus anthracis spores. J Bacteriol 196:3399-3409.
84. Li Y, Butzin XY, Davis A, Setlow B, Korza G, Ustok FI, 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. J Bacteriol 195:2530-2540.
85. Ustok FI, Packman LC, Lowe CR, Christie G. 2014. Spore germination mediated by Bacillus megaterium QM B1551 SleL and YpeB. J Bacteriol 196:1045-1054.
86. Heffron JD, Sherry N, Popham DL. 2011. In vitro studies of peptidoglycan binding and hydrolysis by the Bacillus anthracis germination-specific lytic enzyme SleB. J Bacteriol 193:125-131.
87. 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. J Bacteriol 194:45374545.
88. Jing X, Robinson HR, Heffron JD, Popham DL, Schubot FD. 2012. The catalytic domain of the germination-specific lytic transglycosylase SleB from Bacillus anthracis displays a unique active site topology. Proteins 80:2469-2475.
89. Kodama T, Takamatsu H, Asai K, Kobayashi K, Ogasawara N, Watabe K. 1999. The Bacillus subtilis yaaH gene is transcribed by SigE RNA polymerase during sporulation, and its product is involved in germination of spores. J Bacteriol 181:4584-4591.
90. Lambert EA, Popham DL. 2008. The Bacillus anthracis SleL (YaaH) protein is an N-acetylglucosaminidase involved in spore cortex depolymerization. J Bacteriol 190:7601-7607.
91. Sanchez-Salas JL, Santiago-Lara ML, Setlow B, Sussman MD, Setlow P. 1992. Properties of Bacillus megaterium and Bacillus subtilis mutants which lack the protease that degrades small, acid-soluble proteins during spore germination. J Bacteriol 174:807-814.
92. Ibarra JR, Orozco AD, Rojas JA, Lopez K, Setlow P, Yasbin RE, Pedraza-Reyes M. 2008. Role of the Nfo and ExoA apurinic/apyrimidinic endonucleases in repair of DNA damage during outgrowth of Bacillus subtilis spores. J Bacteriol 190:2031-2038.
93. Setlow P. 2007. I will survive:DNA protection in bacterial spores. Trends Microbiol 15:172-180.
94. Santo LY, Doi RH. 1974. Ultrastructural analysis during germination and outgrowth of Bacillus subtilis spores. J Bacteriol 120:475-481.
95. Plomp M, Leighton TJ, Wheeler KE, Hill HD, Malkin AJ. 2007. in vitro high-resolution structural dynamics of single germinating bacterial spores. Proc Natl Acad Sci USA 104:9644-9649.
96. Jagtap P, Michailidis G, Zielke R, Walker AK, Patel N, Strahler JR, Driks A, Andrews PC, Maddock JR. 2006. Early events of Bacillus anthracis germination identified by time-course quantitative proteomics. Proteomics 6:5199-5211.
97. Nessi C, Albertini AM, Speranza ML, Galizzi A. 1995. The outB gene of Bacillus subtilis codes for NAD synthetase. J Biol Chem 270:6181-6185.
98. Murray T, Popham DL, Pearson CB, Hand AR, Setlow P. 1998. Analysis of outgrowth of Bacillus subtilis spores lacking penicillin-binding protein 2a. J Bacteriol 180:6493-6502.
99. Keijser BJF, Ter Beek A, Rauwerda H, Schuren F, Montijn R, van der Spek H, Brul S. 2007. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J Bacteriol 189:3624-3634.
100. Bettegowda C, Huang X, Lin J, Cheong I, Kohli M, Szabo SA, Zhang X, Diaz LA Jr, Velculescu VE, Parmigiani G, Kinzler KW, Vogelstein B, Zhou S. 2006. The genome and transcriptomes of the anti-tumor agent Clostridium novyi-NT. Nat Biotechnol 24:1573-1580.
101. Segev E, Smith Y, Ben-Yehuda S. 2012. RNA dynamics in aging bacterial spores. Cell 148:139-149.
102. Zuberi AR, Moir A, Feavers IM. 1987. The nucleotide sequence and gene organization of the gerA spore germination operon of Bacillus subtilis 168. Gene 51:1-11.
103. Ramirez-Peralta A, Gupta S, Butzin XY, 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. J Bacteriol 195:3009-3021.
104. Paidhungat M, Setlow P. 2000. Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. J Bacteriol 182:2513-2519.
105. Stewart K-AV, Setlow P. 2013. Numbers of individual nutrient germinant receptors and other germination proteins in spores of Bacillus subtilis. J Bacteriol 195:3575-3582.
106. Bagyan I, Hobot J, Cutting S. 1996. A compartmentalized regulator of developmental gene expression in Bacillus subtilis. J Bacteriol 178:4500-4507.
107. Traag BA, Ramirez-Peralta A, Wang Erickson AF, Setlow P, Losick R. 2013. A novel RNA polymerasebinding protein controlling genes involved in spore germination in Bacillus subtilis. Mol Microbiol 89:113-122.
108. Hinc K, Nagorska K, Iwanicki A, Wegrzyn G, Seror SJ, Obuchowski M. 2006. Expression of genes coding for GerA and GerK spore germination receptors is dependent on the protein phosphatase PrpE. J Bacteriol 188:4373-4383.
109. Ross CA, Abel-Santos E. 2010. Guidelines for nomenclature assignment of Ger receptors. Res Microbiol 161:830-837.
110. Abdoarrahem MM, Gammon K, Dancer BN, Berry C. 2009. Genetic basis for alkaline activation of germination in Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 75:6410-6413.
111. Guidi-Rontani C, Pereira Y, Ruffie S, Sirard JC, Weber-Levy M, Mock M. 1999. Identification and characterization of a germination operon on the virulence plasmid pXO1 of Bacillus anthracis. Mol Microbiol 33:407-414.
112. Van der Auwera G, Mahillon J. 2005. TnXO1, a germination-associated class II transposon from Bacillus anthracis. Plasmid 53:251-257.
113. Christie G, Lowe CR. 2007. Role of chromosomal and plasmid-borne receptor homologues in the response of Bacillus megaterium QM B1551 spores to germinants. J Bacteriol 189:4375-4383.
114. Griffiths KK, Zhang J, Cowan AE, Yu J, Setlow P. 2011. Germination proteins in the inner membrane of dormant Bacillus subtilis spores colocalize in a discrete cluster. Mol Microbiol 81:1061-1077.
115. Ghosh S, Setlow B, Wahome PG, Cowan AE, Plomp M, Malkin AJ, Setlow P. 2008. Characterization of spores of Bacillus subtilis that lack most coat layers. J Bac-teriol 190:6741-6748.
116. Hudson KD, Corfe BM, Kemp EH, Feavers IM, Coote PJ, Moir A. 2001. Localization of GerAA and GerAC germination proteins in the Bacillus subtilis spore. J Bacteriol 183:4317-4322.
117. Paidhungat M, Setlow P. 2001. Localization of a germinant receptor protein (GerBA) to the inner membrane of Bacillus subtilis spores. J Bacteriol 183:3982-3990.
118. Pelczar PL, Igarashi T, Setlow B, Setlow P. 2007. Role of GerD in germination of Bacillus subtilis spores. J Bacteriol 189:1090-1098.
119. Pelczar PL, Setlow P. 2008. Localization of the germination protein GerD to the inner membrane in Bacillus subtilis spores. J Bacteriol 190:5635-5641.
120. Mongkolthanaruk W, Robinson C, Moir A. 2009. Localization of the GerD spore germination protein in the Bacillus subtilis spore. Microbiology 155:1146-1151.
121. Li Y, Jin K, Ghosh S, Devarakonda P, Carlson K, Davis A, Stewart K-AV, Cammett E, Pelczar Rossi P, Setlow B, Lu M, Setlow P, Hao B. 2014. Structural and functional analysis of the GerD spore germination protein of Bacillus species. J Mol Biol 426:1995-2008.
122. Yi X, Liu J, Faeder JR, Setlow P. 2011. Synergism between different germinant receptors in the germination of Bacillus subtilis spores. J Bacteriol 193:46644671.
123. Luu H, Akoachere M, Patra M, Abel-Santos E. 2011. Cooperativity and interference of germination pathways in Bacillus anthracis spores. J Bacteriol 193:4192-4198.
124. Cooper GR, 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. J Bacteriol 193:2261-2267.
125. Mongkolthanaruk W, Cooper GR, Mawer JSP, Allan RN, Moir A. 2011. Effect of amino acid substitutions in the GerAA protein on the function of the alanine-responsive germinant receptor of Bacillus subtilis spores. J Bacteriol 193:2268-2275.
126. Gupta S, Ustok FI, Johnson CL, Bailey DMD, Lowe CR, Christie G. 2013. Investigating the functional hierarchy of Bacillus megaterium PV361 spore germinant receptors. J Bacteriol 195:3045-3053.
127. Stewart KAV, Yi X, Ghosh S, Setlow P. 2012. Germination protein levels and rates of germination of spores of Bacillus subtilis with overexpressed or deleted genes encoding germination proteins. J Bacteriol 194:3156-3164.
128. Jack DL, Paulsen IT, Saier MH. 2000. The amino acid/polyamine/organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microbiology 146:1797-1814.
129. Wilson MJ, Carlson PE, Janes BK, Hanna PC. 2012. Membrane topology of the Bacillus anthracis GerH germinant receptor proteins. J Bacteriol 194:13691377.
130. Paidhungat M, Setlow P. 1999. Isolation and characterization of mutations in Bacillus subtilis that allow spore germination in the novel germinant D-alanine. J Bacteriol 181:3341-3350.
131. Atluri S, Ragkousi K, Cortezzo DE, Setlow P. 2006. Cooperativity between different nutrient receptors in germination of spores of Bacillus subtilis and reduction of this cooperativity by alterations in the GerB receptor. J Bacteriol 188:28-36.
132. Christie G, Gotzke H, Lowe CR. 2010. Identification of a receptor subunit and putative ligand-binding residues involved in the Bacillus megaterium QM B1551 spore germination response to glucose. J Bacteriol 192:43174326.
133. Christie G, Lazarevska M, Lowe CR. 2008. Functional consequences of amino acid substitutions to GerVB, a component of the Bacillus megaterium spore germinant receptor. J Bacteriol 190:2014-2022.
134. Sammons RL, Moir A, Smith DA. 1981. Isolation and properties of spore germination mutants of Bacillus subtilis 168 deficient in the initiation of germination. J Gen Microbiol 124:229-241.
135. Gao X, Zhou L, Jiao X, Lu F, Yan C, Zeng X, Wang J, Shi Y. 2010. Mechanism of substrate recognition and transport by an amino acid antiporter. Nature 463:828-832.
136. Shaffer PL, Goehring A, Shankaranarayanan A, Gouaux E. 2009. Structure and mechanism of a Na+-independent amino acid transporter. science 325:10101014.
137. Li Y, Setlow B, Setlow P, Hao B. 2010. Crystal structure of the GerBC component of a Bacillus subtilis spore germinant receptor. J Mol Biol 402:8-16.
138. Li Y, Catta P, Stewart KAV, Dufner M, Setlow P, Hao B. 2011. Structure-based functional studies of the effects of amino acid substitutions in GerBC, the C subunit of the Bacillus subtilis GerB spore germinant receptor. J Bacteriol 193:4143-4152.
139. Korza G, Setlow P. 2013. Topology and accessibility of germination proteins in the Bacillus subtilis spore inner membrane. J Bacteriol 195:1484-1491.
140. Priest FG, Barker M, Baillie LWJ, Holmes EC, Maiden MCJ. 2004. Population structure and evolution of the Bacillus cereus group. J Bacteriol 186:7959-7970.
141. Clements MO, Moir A. 1998. Role of the gerl operon of Bacillus cereus 569 in the response of spores to germinants. J Bacteriol 180:6729-6735.
142. Barlass PJ, Houston CW, Clements MO, Moir A. 2002. Germination of Bacillus cereus spores in response to L-alanine and to inosine:the roles of gerL and gerQ operons. Microbiology 148:2089-2095.
143. Dodatko T, Akoachere M, Jimenez N, Alyarez Z, Abel-Santos E. 2010. Dissecting interactions between nucleosides and germination receptors in Bacillus cereus 569 spores. Microbiology 156:1244-1255.
144. Dodatko T, Akoachere M, Muehlbauer SM, Helfrich F, Howerton A, Ross C, Wysocki V, Brojatsch J, Abel-Santos E. 2009. Bacillus cereus spores release alanine that synergizes with inosine to promote germination. PLos One 4:e6398. doi:10.1371/journal.pone.0006398.
145. Thackray PD, Behravan J, Southworth TW, Moir A. 2001. GerN, an antiporter homologue important in germination of Bacillus cereus endospores. J Bacteriol 183:476-482.
146. Southworth TW, Guffanti AA, Moir A, Krulwich TA. 2001. GerN, an endospore germination protein of Bacillus cereus, is an Na(+)/H(+)-K(+) antiporter. J Bacteriol 183:5896-5903.
147. Senior A, Moir A. 2008. The Bacillus cereus GerN and GerT protein homologs have distinct roles in spore germination and outgrowth, respectively. J Bacteriol 190:6148-6152.
148. Tani K, Watanabe T, Matsuda H, Nasu M, Kondo M. 1996. Cloning and sequencing of the spore germination gene of Bacillus megaterium ATCC 12872:similarities to the NaH-antiporter gene of Enterococcus hirae. Microbiol Immunol 40:99-105.
149. Paredes-Sabja D, Setlow P, Sarker MR. 2009. GerO, a putative Na+/H+-K+ antiporter, is essential for normal germination of spores of the pathogenic bacterium Clostridium perfringens. J Bacteriol 191:3822-3831.
150. Hornstra LM, de Vries YP, de Vos WM, Abee T, Wells-Bennik MHJ. 2005. gerR, a novel ger operon involved in L-alanine- and inosine-initiated germination of Bacillus cereus ATCC 14579. Appl Environ Microbiol 71:774-781.
151. Hornstra LM, de Vries YP, Wells-Bennik MHJ, de Vos WM, Abee T. 2006. Characterization of germination receptors of Bacillus cereus ATCC 14579. Appl Environ Microbiol 72:44-53.
152. Weiner MA, Read TD, Hanna PC. 2003. Identification and characterization of the gerH operon of Bacillus anthracis endospores:a differential role for purine nucleosides in germination. J Bacteriol 185:1462-1464.
153. Fisher N, Hanna P. 2005. Characterization of Bacillus anthracis germinant receptors in vitro. J Bacteriol 187:8055-8062.
154. Hu H, Emerson J, Aronson AI. 2007. Factors involved in the germination and inactivation of Bacillus anthra-cis spores in murine primary macrophages. FEMS Microbiol Lett 272:245-250.
155. Barua S, McKevitt M, DeGiusti K, Hamm EE, Larabee J, Shakir S, Bryant K, Koehler TM, Blanke SR, Dyer D, Gillaspy A, Ballard JD. 2009. The mechanism of Bacillus anthracis intracellular germination requires multiple and highly diverse genetic loci. Infect Immun 77:23-31.
156. Ramirez N, Abel-Santos E. 2010. Requirements for germination of Clostridium sordellii spores in vitro. J Bacteriol 192:418-425.
157. Waites WM, Wyatt LR. 1974. The effect of pH, germin-ants and temperature on the germination of spores of Clostridium bifermentans. J Gen Microbiol 80:253-258.
158. Adam KH, Brunt J, Brightwell G, Flint SH, Peck MW. 2011. Spore germination of the psychrotolerant, red meat spoiler, Clostridium frigidicarnis. Lett Appl Microbiol 53:92-97.
159. Brunt J, Plowman J, Gaskin DJH, Itchner M, Carter AT, Peck MW. 2014. Functional characterisation of germinant receptors in Clostridium botulinum and Clostridium sporogenes presents novel insights into spore germination systems. PLoS Pathog 10:e1004382. doi:10.1371/journal.ppat.1004382.
160. Paredes-Sabja D, Setlow P, Sarker MR. 2009. Role of GerKB in germination and outgrowth of Clostridium perfringens spores. Appl Environ Microbiol 75:38133817.
161. Olguin-Araneda V, Banawas S, Sarker MR, Paredes-Sabja D. 2015. Recent advances in germination of Clostridium spores. Res Microbiol 166:236-243.
162. Urakami K, Miyata S, Moriyama R, Sugimoto K, Makino S. 1999. Germination-specific cortex-lytic enzymes from Clostridium perfringens S40 spores:time of synthesis, precursor structure and regulation of enzymatic activity. FEMS Microbiol Lett 173:467-473.
163. Makino S, Moriyama R. 2002. Hydrolysis of cortex peptidoglycan during bacterial spore germination. Med Sci Monit 8:RA119-RA127.
164. Okamura S, Urakami K, Kimata M, Aoshima T, Shimamoto S, Moriyama R, Makino S. 2000. The N-terminal prepeptide is required for the production of spore cortex-lytic enzyme from its inactive precursor during germination of Clostridium perfringens S40 spores. Mol Microbiol 37:821-827.
165. Banawas S, Korza G, Paredes-Sabja D, Li Y, Hao B, Setlow P, Sarker MR. 2015. Location and stoichiometry of the protease CspB and the cortex-lytic enzyme SleC in Clostridium perfringens spores. Food Microbiol 50:83-87.
166. Paredes-Sabja D, Setlow P, Sarker MR. 2009. SleC is essential for cortex peptidoglycan hydrolysis during germination of spores of the pathogenic bacterium Clostridium perfringens. J Bacteriol 191:2711-2720.
167. Paredes-Sabja D, Setlow P, Sarker MR. 2009. The protease CspB is essential for initiation of cortex hydrolysis and dipicolinic acid (DPA) release during germination of spores of Clostridium perfringens type A food poisoning isolates. Microbiology 155:3464-3472.
168. Sorg JA, Sonenshein AL. 2008. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacte-riol 190:2505-2512.
169. Howerton A, Ramirez N, Abel-Santos E. 2011. Mapping interactions between germinants and Clostridium difficile spores. J Bacteriol 193:274-282.
170. Wheeldon LJ, Worthington T, Lambert PA. 2011. Histidine acts as a co-germinant with glycine and taurocholate for Clostridium difficile spores. J Appl Microbiol 110:987-994.
171. Francis MB, Allen CA, Shrestha R, Sorg JA. 2013. Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection. PLoS Pathog 9:e1003356. doi:10.1371/journal.ppat. 1003356.
172. Paredes-Sabja D, Shen A, Sorg JA. 2014. Clostridium difficile spore biology:sporulation, germination, and spore structural proteins. Trends Microbiol 22:406-416.
173. Burns DA, Heap JT, Minton NP. 2010. SleC is essential for germination of Clostridium difficile spores in nutrient-rich medium supplemented with the bile salt taurocholate. J Bacteriol 192:657-664.
174. Burns DA, Heap JT, Minton NP. 2010. Clostridium difficile spore germination:an update. Res Microbiol 161:730-734.
175. Francis MB, Allen CA, Sorg JA. 2015. Spore cortex hydrolysis precedes dipicolinic acid release during Clostridium difficile spore germination. J Bacteriol 197:2276-2283.
176. Igarashi T, Setlow B, Paidhungat M, Setlow P. 2004. Effects of a gerF (lgt) mutation on the germination of spores of Bacillus subtilis. J Bacteriol 186:2984-2991.
177. Kawai F, Hara H, Takamatsu H, Watabe K, Matsumoto K. 2006. Cardiolipin enrichment in spore membranes and its involvement in germination of Bacillus subtilis Marburg. Genes Genet Syst 81:69-76.
178. Griffiths KK, Setlow P. 2009. Effects of modification of membrane lipid composition on Bacillus subtilis sporulation and spore properties. J Appl Microbiol 106:2064-2078.
179. Henriques AO, Moran CP. 2007. Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61:555-588.
180. Moir A. 1981. Germination properties of a spore coat-defective mutant of Bacillus subtilis. J Bacteriol 146:1106-1116.
181. Ferguson CC, Camp AH, Losick R. 2007. gerT, a newly discovered germination gene under the control of the sporulation transcription factor sigmaK in Bacillus subtilis. J Bacteriol 189:7681-7689.
182. Kodama T, Matsubayashi T, Yanagihara T, Komoto H, Ara K, Ozaki K, Kuwana R, Imamura D, Takamatsu H, Watabe K, Sekiguchi J. 2011. A novel small protein of Bacillus subtilis involved in spore germination and spore coat assembly. Biosci Biotechnol Biochem 75:1119-1128.
183. Naclerio G, Baccigalupi L, Zilhao R, De Felice M, Ricca E. 1996. Bacillus subtilis spore coat assembly requires cotH gene expression. J Bacteriol 178:4375-4380.
184. Little S, Driks A. 2001. Functional analysis of the Bacillus subtilis morphogenetic spore coat protein CotE. Mol Microbiol 42:1107-1120.
185. Zheng LB, Donovan WP, Fitz-James PC, Losick R. 1988. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev 2:1047-1054.
186. Bourne N, FitzJames PC, Aronson AI. 1991. Structural and germination defects of Bacillus subtilis spores with altered contents of a spore coat protein. J Bacteriol 173:6618-6625.
187. Stewart BT, Halvorson HO. 1953. Studies on the spores of aerobic bacteria. I. The occurrence of alanine racemase. J Bacteriol 65:160-166.
188. Todd SJ, Moir AJG, Johnson MJ, Moir A. 2003. Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J Bacteriol 185:3373-3378.
189. Liang L, He XH, Liu G, Tan HR. 2008. The role of a purine-specific nucleoside hydrolase in spore germination of Bacillus thuringiensis. Microbiology 154:1333-1340.
190. Wuytack EY, Boven S, Michiels CW. 1998. Comparative study of pressure-induced germination of Bacillus subtilis spores at low and high pressures. Appl Environ Microbiol 64:3220-3224.
191. Wuytack EY, Soons J, Poschet F, Michiels CW. 2000. Comparative study of pressure- and nutrient-induced germination of Bacillus subtilis spores. Appl Environ Microbiol 66:257-261.
192. Black EP, Koziol-Dube K, Guan D, Wei J, Setlow B, Cortezzo DE, Hoover DG, Setlow P. 2005. Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Appl Environ Microbiol 71:5879-5887.
193. Black EP, Wei J, Atluri S, Cortezzo DE, Koziol-Dube K, Hoover DG, Setlow P. 2007. Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. J Appl Microbiol 102:65-76.
194. Rode LJ, Foster JW. 1961. Germination of bacterial spores with alkyl primary amines. J Bacteriol 81:768-779.
195. Vepachedu VR, Setlow P. 2007. Role of SpoVA proteins in release of dipicolinic acid during germination of Bacillus subtilis spores triggered by dodecylamine or lysozyme. J Bacteriol 189:1565-1572.
196. Peck MW, Fairbairn DA, Lund BM. 1992. Factors affecting growth from heat-treated spores of nonproteolytic Clostridium botulinum. Lett Appl Microbiol 15:152-155.
197. Peck MW, Fairbairn DA, Lund BM. 1993. Heat-resistance of spores of nonproteolytic Clostridium botulinum estimated on medium containing lysozyme. Lett Appl Microbiol 16:126-131.
198. Wei J, Shah IM, Ghosh S, Dworkin J, Hoover DG, Setlow P. 2010. Superdormant spores of bacillus species germinate normally with high pressure, peptido-glycan fragments, and bryostatin. J Bacteriol 192:1455-1458.
199. van Melis CCJ, Nierop Groot MN, Abee T. 2011. Impact of sorbic acid on germinant receptor-dependent and -independent germination pathways in Bacillus cereus. Appl Environ Microbiol 77:2552-2554.
200. Shah IM, Dworkin J. 2010. Induction and regulation of a secreted peptidoglycan hydrolase by a membrane Ser/Thr kinase that detects muropeptides. Mol Microbiol 75:1232-1243.
201. Setlow P. 2014. Spore resistance properties. Microbiol Spectrum 2(4):TBS-0003-2012. doi:10.1128/microbiolspec. TBS-0003-2012.
202. Galperin MY. 2013. Genomic diversity of sporeforming Firmicutes. Microbiol Spectrum 1(2):TBS-0015-2012.