Functional Characterisation of Germinant Receptors in and Presents Novel Insights into Spore Germination Systems

1. Peck MW (2009) Biology and genomic analysis of Clostridium botulinum. In: Poole RK, editor. Advances in Microbial Physiology: Academic Press. pp. 183–265, 320.

2. CarterAT, PaulCJ, MasonDR, TwineSM, AlstonMJ, et al. (2009) Independent evolution of neurotoxin and flagellar genetic loci in proteolytic Clostridium botulinum. BMC Genomics 10: 115.

3. PeckMW, StringerSC, CarterAT (2011) Clostridium botulinum in the post-genomic era. Food Microbiol 28: 183–191.

4. HillKK, SmithTJ (2013) Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr Top Microbiol Immunol 364: 1–20.

5. BarashJR, ArnonSS (2014) A novel strain of Clostridium botulinum that produces type B and type H botulinum toxins. J Infect Dis 209: 183–191.

6. PoulainB, PopoffMR, MolgoJ (2008) How do the Botulinum Neurotoxins block neurotransmitter release: from botulism to the molecular mechanism of action. The Botulinum J 1: 14.

7. Bruggemann H, Wollherr A, Mazuet C, Popoff M (2011) Clostridium botulinum. In: Fratamico P, Liu Y, Kathariou S, editors. Genomes of Foodborne and Waterborne Pathogens: ASM Press. pp. 185–212.

8. Lindström M, Fredriksson-Ahomaa M, and Korkeala H (2009) Molecular epidemiology of group I and group II Clostridium botulinum. In: Brüggemann H, Gottschalk, G., editor. Clostridia, molecular biology in the post-genomic era. Caister Academic Press, Norfolk, United Kingdom. pp. 103–130.

9. HackettR, KamPC (2007) Botulinum toxin: pharmacology and clinical developments: a literature review. Med Chem 3: 333–345.

10. Hatheway C (1988) Botulism. In: Balows A, Hausler WJ, Ohashi M, Turano A, Lennete EH, editors. Laboratory Diagnosis of Infectious Diseases: Springer New York. pp. 111–133.

11. Johnson EA (2007) Food microbiology: fundamentals and frontiers. In: Doyle MP, Beuchat, L. R., editor. Clostridium botulinum. 3rd ed. Food microbiology: fundamentals and frontiers: ASM Press. pp. 401–421.

12. JohnsonEA (1999) Clostridial toxins as therapeutic agents: benefits of nature's most toxic proteins. Annu Rev Microbiol 53: 551–575.

13. RaphaelBH, LuquezC, McCroskeyLM, JosephLA, JacobsonMJ, et al. (2008) Genetic homogeneity of Clostridium botulinum type A1 strains with unique toxin gene clusters. Appl Environ Microbiol 74: 4390–4397.

14. FangPK, RaphaelBH, MaslankaSE, CaiS, SinghBR (2010) Analysis of genomic differences among Clostridium botulinum type A1 strains. BMC Genomics 11: 725.

15. RaphaelBH, JosephLA, McCroskeyLM, LuquezC, MaslankaSE (2010) Detection and differentiation of Clostridium botulinum type A strains using a focused DNA microarray. Mol Cell Probe 24: 146–153.

16. SebaihiaM, PeckMW, MintonNP, ThomsonNR, HoldenMT, et al. (2007) Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res 17: 1082–1092.

17. InksterT, CordinaC, SiegmethA (2011) Septic arthritis following anterior cruciate ligament reconstruction secondary to Clostridium sporogenes; a rare clinical pathogen. J Clin Pathol 64: 820–821.

18. McClure PJ (2006) Spore-forming bacteria. In: Blackburn CdW, editor. Food spoilage microorganisms. No. 122 ed: Woodhead Publishing limited pp. 579–623.

19. BrownJL, Tran-DinhN, ChapmanB (2012) Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum. J Food Prot 75: 779–792.

20. TaylorRH, DunnML, OgdenLV, JefferiesLK, EggettDL, et al. (2013) Conditions associated with Clostridium sporogenes growth as a surrogate for Clostridium botulinum in nonthermally processed canned butter. J Dairy Sci 96: 2754–2764.

21. CollinsMD, LawsonPA, WillemsA, CordobaJJ, Fernandez-GarayzabalJ, et al. (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44: 812–826.

22. JacobsonMJ, LinG, WhittamTS, JohnsonEA (2008) Phylogenetic analysis of Clostridium botulinum type A by multi-locus sequence typing. Microbiology 154: 2408–2415.

23. BradburyM, GreenfieldP, MidgleyD, LiD, Tran-DinhN, et al. (2012) Draft genome sequence of Clostridium sporogenes PA 3679, the common nontoxigenic surrogate for proteolytic Clostridium botulinum. J Bacteriol 194: 1631–1632.

24. SetlowP (2014) Germination of Spores of Bacillus Species: What We Know and Do Not Know. J Bacteriol 196: 1297–1305.

25. StringerSC, WebbMD, PeckMW (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.

26. StringerSC, WebbMD, PeckMW (2011) Lag time variability in individual spores of Clostridium botulinum. Food Microbiol 28: 228–235.

27. WebbMD, StringerSC, Le MarcY, BaranyiJ, PeckMW (2012) Does proximity to neighbours affect germination of spores of non-proteolytic Clostridium botulinum? Food Microbiol 32: 104–109.

28. Christie G (2012) Initiation of germination in Bacillus and Clostridium spores. In: Bacterial Spores: Current Research and Applications. pp 89–106.

29. Paredes-SabjaD, SetlowP, SarkerMR (2011) Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol 19: 85–94.

30. RamirezN, Abel-SantosE (2010) Requirements for germination of Clostridium sordellii spores in vitro. J Bacteriol 192: 418–425.

31. LigginsM, RamirezN, MagnusonN, Abel-SantosE (2011) Progesterone Analogs Influence Germination of Clostridium sordellii and Clostridium difficile Spores In Vitro. J Bacteriol 193: 2776–2783.

32. AdamKH, BruntJ, BrightwellG, FlintSH, PeckMW (2011) Spore germination of the psychrotolerant, red meat spoiler, Clostridium frigidicarnis. Lett Appl Microbiol 53: 92–97.

33. MooreP, KyneL, MartinA, SolomonK (2013) Germination efficiency of clinical Clostridium difficile spores and correlation with ribotype, disease severity and therapy failure. J Med Microbiol 62: 1405–1413.

34. Paredes-SabjaD, ShenA, SorgJA (2014) Clostridium difficile spore biology: sporulation, germination, and spore structural proteins. Trends Microbiol 22: 406–416.

35. BanawasS, Paredes-SabjaD, KorzaG, LiY, HaoB, et al. (2013) The Clostridium perfringens germinant receptor protein GerKC is located in the spore inner membrane and is crucial for spore germination. J Bacteriol 195: 5084–5091.

36. FrancisMB, AllenCA, ShresthaR, SorgJA (2013) Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection. PLoS Pathog 9: e1003356.

37. HeegD, BurnsDA, CartmanST, MintonNP (2012) Spores of Clostridium difficile clinical isolates display a diverse germination response to bile salts. PLoS One 7: e32381.

38. HowertonA, RamirezN, Abel-SantosE (2011) Mapping interactions between germinants and Clostridium difficile spores. J Bacteriol 193: 274–282.

39. Paredes-SabjaD, SetlowP, SarkerMR (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.

40. RamirezN, LigginsM, Abel-SantosE (2010) Kinetic evidence for the presence of putative germination receptors in Clostridium difficile spores. J Bacteriol 192: 4215–4222.

41. SarkerMR, Paredes-SabjaD (2012) Molecular basis of early stages of Clostridium difficile infection: germination and colonization. Future Microbiol 7: 933–943.

42. SorgJA, SonensheinAL (2009) Chenodeoxycholate is an inhibitor of Clostridium difficile spore germination. J Bacteriol 191: 1115–1117.

43. SorgJA, SonensheinAL (2010) Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J Bacteriol 192: 4983–4990.

44. AlbertoF, BroussolleV, MasonDR, CarlinF, PeckMW (2003) Variability in spore germination response by strains of proteolytic Clostridium botulinum types A, B and F. Lett Appl Microbiol 36: 41–45.

45. XiaoY, FranckeC, AbeeT, Wells-BennikMH (2011) Clostridial spore germination versus bacilli: genome mining and current insights. Food Microbiol 28: 266–274.

46. BroussolleV, AlbertoF, ShearmanCA, MasonDR, BotellaL, et al. (2002) Molecular and physiological characterisation of spore germination in Clostridium botulinum and C-sporogenes. Anaerobe 8: 89–100.

47. AndoY (1973) Studies on germination of spores of clostridial species capable of causing food poisoning (I) Factors affecting the germination of spores of Clostridium botulinum type A in a chemically defined medium. J Food Hyg Soc Jpn 14: 457–461.

48. UeharaM, FrankHA (1965) Factors affecting alanine-induced germination of clostridial spores. Spores III: American Society for Microbiology 38–46.

49. IshimoriT, TakahashiK, GotoM, NakagawaS, KasaiY, et al. (2012) Synergistic effects of high hydrostatic pressure, mild heating, and amino acids on germination and inactivation of Clostridium sporogenes spores. Appl Environ Microbiol 78: 8202–8207.

50. RossC, Abel-SantosE (2010) The Ger receptor family from sporulating bacteria. Curr Issues Mol Biol 12: 147–158.

51. ShoesmithJG, HollandKT (1972) The germination of spores of Clostridium tetani. J Gen Microbiol 70: 253–261.

52. WaitesWM, WyattLR (1971) Germination of spores of Clostridium bifermentans by certain amino acids, lactate and pyruvate in the presence of sodium or potassium ions. J Gen Microbiol 67: 215–222.

53. HornstraLM, de VriesYP, Wells-BennikMH, de VosWM, AbeeT (2006) Characterization of germination receptors of Bacillus cereus ATCC 14579. Appl Environ Microbiol 72: 44–53.

54. PlowmanJ, PeckMW (2002) Use of a novel method to characterize the response of spores of non-proteolytic Clostridium botulinum types B, E and F to a wide range of germinants and conditions. J Appl Microbiol 92: 681–694.

55. HornstraLM, de VriesYP, de VosWM, AbeeT (2006) Influence of sporulation medium composition on transcription of ger operons and the germination response of spores of Bacillus cereus ATCC 14579. Appl Environ Microbiol 72: 3746–3749.

56. Ramirez-PeraltaA, ZhangP, LiYQ, SetlowP (2012) Effects of sporulation conditions on the germination and germination protein levels of Bacillus subtilis spores. Appl Environ Microbiol 78: 2689–2697.

57. Nguyen Thi MinhH, DurandA, LoisonP, Perrier-CornetJM, GervaisP (2011) Effect of sporulation conditions on the resistance of Bacillus subtilis spores to heat and high pressure. Appl Microbiol Biotechnol 90: 1409–1417.

58. RoseR, SetlowB, MonroeA, MallozziM, DriksA, et al. (2007) Comparison of the properties of Bacillus subtilis spores made in liquid or on agar plates. J Appl Microbiol 103: 691–699.

59. SetlowB, CowanAE, SetlowP (2003) Germination of spores of Bacillus subtilis with dodecylamine. J Appl Microbiol 95: 637–648.

60. PeckMW, EvansRI, FairbairnDA, HartleyMG, RussellNJ (1995) Effect of sporulation temperature on some properties of spores of non-proteolytic Clostridium botulinum. Int J Food Microbiol 28: 289–297.

61. MellyE, GenestPC, GilmoreME, LittleS, PophamDL, et al. (2002) Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J Appl Microbiol 92: 1105–1115.

62. JohnstoneK (1994) The trigger mechanism of spore germination: current concepts. J Appl Bacteriol 76: 17S–24S.

63. RowleyDB, FeeherryF (1970) Conditions affecting germination of Clostridium botulinum 62A spores in a chemically defined medium. J Bacteriol 104: 1151–1157.

64. MontvilleTJ, JonesSB, ConwayLK, SapersGM (1985) Germination of spores from Clostridium botulinum B-aphis and Ba410. Appl Environ Microbiol 50: 795–800.

65. ChristieG, LoweCR (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.

66. MoirA, CorfeBM, BehravanJ (2002) Spore germination. Cell Mol Life Sci 59: 403–409.

67. DodatkoT, AkoachereM, MuehlbauerSM, HelfrichF, HowertonA, et al. (2009) Bacillus cereus spores release alanine that synergizes with inosine to promote germination. PLoS ONE 4: e6398.

68. YiX, LiuJ, FaederJR, SetlowP (2011) Synergism between different germinant receptors in the germination of Bacillus subtilis spores. J Bacteriol 193: 4664–4671.

69. FisherN, HannaP (2005) Characterization of Bacillus anthracis germinant receptors in vitro. J Bacteriol 187: 8055–8062.

70. LiJ, ChenJ, VidalJE, McClaneBA (2011) The Agr-Like quorum-sensing system regulates sporulation and production of enterotoxin and Beta2 toxin by Clostridium perfringens type A non-food-borne human gastrointestinal disease strain F5603. Infection and Immunity 79: 2451–2459.

71. NgYK, EhsaanM, PhilipS, ColleryMM, JanoirC, et al. (2013) Expanding the repertoire of gene tools for precise manipulation of the Clostridium difficile genome: allelic exchange using pyrE alleles. PLoS ONE 8: e56051.

72. GriffithsKK, ZhangJ, CowanAE, YuJ, SetlowP (2011) Germination proteins in the inner membrane of dormant Bacillus subtilis spores colocalize in a discrete cluster. Mol Microbiol 81: 1061–1077.

73. Cabrera-MartinezRM, Tovar-RojoF, VepacheduVR, SetlowP (2003) Effects of overexpression of nutrient receptors on germination of spores of Bacillus subtilis. J Bacteriol 185: 2457–2464.

74. PaidhungatM, SetlowP (2000) Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. J Bacteriol 182: 2513–2519.

75. SieversF, WilmA, DineenD, GibsonTJ, KarplusK, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.

76. WaterhouseAM, ProcterJB, MartinDMA, ClampM, BartonGJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191.

77. PuntaM, CoggillPC, EberhardtRY, MistryJ, TateJ, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–301.

78. KroghA, LarssonB, von HeijneG, SonnhammerEL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580.

79. PurdyD, O'KeeffeTAT, ElmoreM, HerbertM, McLeodA, et al. (2002) Conjugative transfer of clostridial shuttle vectors from Escherichia coli to Clostridium difficile through circumvention of the restriction barrier. Mol Microbiol 46: 439–452.

80. PerutkaJ, WangWJ, GoerlitzD, LambowitzAM (2004) Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. J Mol Biol 336: 421–439.

81. HeapJT, KuehneSA, EhsaanM, CartmanST, CooksleyCM, et al. (2010) The ClosTron: Mutagenesis in Clostridium refined and streamlined. J Microbiol Methods 80: 49–55.

82. HeapJT, PenningtonOJ, CartmanST, MintonNP (2009) A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78: 79–85.