Chapter 15 : Physiology and Sporulation in

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Physiology and Sporulation in , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819323/9781555816759_Chap15-1.gif /docserver/preview/fulltext/10.1128/9781555819323/9781555816759_Chap15-2.gif


Clostridia are anaerobic bacteria, although many species can tolerate oxygen to various extents. They are able to form endospores and are not capable of dissimilatory sulfate reduction. Most of them show a positive Gram reaction. These criteria have been used in the past for classification. However, phylogenetic analyses based on 16S rRNA sequences led to reattribution of many former clostridia to numerous other and also novel genera, such as , , , , , , , , , , , , , , , , , , and (J. P.Euzéby, List of prokaryotic names with standing in nomenclature – genus , http://www.bacterio.cict.fr/c/clostridium.html). For the genus , approximately 180 species have been validly described, rendering it one of the largest bacterial genera. Only a few of these species are pathogenic, however, involving microbes producing very dangerous toxins. On the other hand, a large number of species are used in biotechnological applications (enzyme, bulk chemicals, and biofuels production) and tested for use in cancer therapy. This is due to the enormous metabolic diversity within the clostridia, rendering them the avant-garde of biotechnologically exploited microorganisms. During past years, techniques have been developed that allowed establishment of genetic systems for many clostridia. Thus, the tools are at hand for further elucidation and exploitation. Due to the limited space of this article, many aspects cannot be presented in detail. Thus, the interested reader is referred to recent references for additional information ( ).

Citation: Dürre P. 2016. Physiology and Sporulation in , p 315-329. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0010-2012
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Vegetative growth and sporulation/germination cycle in clostridia. During normal growth, cells (shown is ) divide and multiply (left). During this period, acids, carbon dioxide, and hydrogen are formed. Upon signals not yet determined, cells start to differentiate into "clostridial forms" with granulose as a storage material (solventogenic species produce at this time acetone, butanol, or isopropanol), then form endospores, which finally will germinate into vegetative cells again.

Citation: Dürre P. 2016. Physiology and Sporulation in , p 315-329. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Signal transduction in and leading to the onset of sporulation. (A) In , three sensor kinases autophosphorylate at a histidine residue and transfer the phosphoryl group to an aspartate residue of the response regulator Spo0A. Cac0323 acts alone, while Cac0903 and Cac3319 act in concert. Cac0437 is a protein masquerading as a kinase, but acting as a phosphatase. (B) In , five different kinases channel the phosphoryl group to Spo0A via a phosphorelay consisting of Spo0F and Spo0B.

Citation: Dürre P. 2016. Physiology and Sporulation in , p 315-329. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Bahl H,, Dürre P . 2001. Clostridia: Biotechnology and Medical Applications. Wiley-VCH, Weinheim, Germany. [CrossRef]
2. Dürre P . 2005. Handbook on Clostridia. CRC Press-Taylor and Francis Group, Boca Raton, FL. [CrossRef]
3. Dürre P . 2007. Clostridia . Encyclopedia of Life Sciences. doi:10.1002/9780470015902.a0020370. [CrossRef]
4. Dürre P, . 2009. The genus Clostridium , p 339 353. In Goldman E,, Green LH (ed), Practical Handbook of Microbiology, 2nd ed. CRC Press-Taylor and Francis Group, Boca Raton, FL.
5. Rood JI,, McClane BA,, Songer JG,, Titball RW . 1997. The Clostridia: Molecular Biology and Pathogenesis. Academic Press, San Diego, CA.
6. Schiel B,, Dürre P, . 2010. Clostridium , p 1701 1715. In Flickinger MC (ed), Encyclopedia of Industrial Biotechnology, Bioprocess, Bioseparation, and Cell Technology, vol. 3. John Wiley & Sons, Hoboken, NJ. doi:10.1002/9780470054581.eib236 [CrossRef]
7. Wilde E,, Hippe H,, Tosunoglu N,, Schallehn G,, Herwig K,, Gottschalk G . 1989. Clostridium tetanomorphum sp. nov., nom. rev. Int J Syst Bacteriol 39 : 127 134.[CrossRef]
8. Brüggemann H,, Gottschalk G . 2004. Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani . Anaerobe 10 : 53 68.[PubMed] [CrossRef]
9. Wieringa KT . 1936. Over het verdwijnen van waterstof en koolzuur onder anaerobe voorwaarden. Antonie van Leeuwenhoek 3 : 263 273.[CrossRef]
10. Braun M,, Mayer F,, Gottschalk G . 1981. Clostridium aceticum (Wieringa), a microorganism producing acetic acid from molecular hydrogen and carbon dioxide. Arch Microbiol 128 : 288 293.[PubMed] [CrossRef]
11. Braun M . 1981. Charakterisierung von anaeroben autotrophen Essigsäurebildnern and Untersuchungen zur Essigsäurebildung aus Wasserstoff and Kohlendioxid durch Clostridium aceticum. Ph.D. dissertation. University of Göttingen, Germany.
12. Das A,, Ljungdahl LG, . 2003. Electron-transport system in acetogens, p 191 204. In Ljungdahl LG,, Adams MW,, Barton LL,, Ferry JG (ed), Biochemistry and Physiology of Anaerobic Bacteria. Springer, New York, NY. [CrossRef]
13. Huang H,, Wang S,, Moll J,, Thauer RK . 2012. Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H 2 plus CO 2 . J Bacteriol 194 : 3689 3699.[PubMed] [CrossRef]
14. Balch WE,, Schoberth S,, Tanner RS,, Wolfe RS . 1977. Acetobacterium, a new genus of hydrogen-oxidizing, carbon dioxide-reducing anaerobic bacteria. Int J Syst Bacteriol 27 : 355 361.[CrossRef]
15. Schmehl M,, Jahn A,, Meyer zu Vilsendorf A,, Hennecke S,, Masepohl B,, Schuppler M,, Marxer M,, Oelze J,, Klipp W . 1993. Identification of a new class of nitrogen fixation genes in Rhodobacter capsulatus: a putative membrane complex involved in electron transport to nitrogenase. Mol Gen Genet 241 : 602 615.[PubMed] [CrossRef]
16. Biegel E,, Müller V . 2010. Bacterial Na +-translocating ferredoxin: NAD + oxidoreductase. Proc Natl Acad Sci USA 107 : 18138 18142.[PubMed] [CrossRef]
17. Poehlein A,, Schmidt S,, Kaster A-K,, Goenreich M,, Vollmers J,, Thürmer A,, Bertsch J,, Schuchmann K,, Voigt B,, Hecker M,, Daniel R,, Thauer RK,, Gottschalk G,, Müller V . 2012. An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS One. 7( 3) : e33439. doi:10.1371/journal.pone.0033439 [CrossRef]
18. Müller V . 2003. Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69 : 6345 6353.[PubMed] [CrossRef]
19. Köpke M,, Held C,, Hujer S,, Liesegang H,, Wiezer A,, Wollherr A,, Ehrenreich A,, Liebl W,, Gottschalk G,, Dürre P . 2010. Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci USA 107 : 13087 13092.[PubMed] [CrossRef]
20. Köpke M,, Mihalcea C,, Bromley JC,, Simpson SD . 2011. Fermentative production of ethanol from carbon monoxide. Curr Opin Biotechnol 22 : 320 325.[PubMed] [CrossRef]
21. Schiel-Bengelsdorf B,, Dürre P . 2012. Pathway engineering and synthetic biology using acetogenic clostridia. FEBS Lett 586 : 2191 2198.[PubMed] [CrossRef]
22. Hilpert W,, Schink B,, Dimroth P . 1984. Life by a new decarboxylation-dependent energy conservation mechanism with Na + as coupling ion. EMBO J 3 : 1665 1670.[PubMed]
23. Kane MB,, Brauman A,, Breznak JA . 1991. Clostridium mayombei sp. nov., an H 2/CO 2 acetogenic bacterium from the gut of the African soil-feeding termite, Cubitermes speciosus . Arch Microbiol 156 : 99 104.[CrossRef]
24. Charrier C,, Duncan GJ,, Reid MD,, Rucklidge GJ,, Henderson D,, Young P,, Russell VJ,, Aminov RI,, Flint HJ,, Louis P . 2006. A novel class of CoA-transferase involved in shortchain fatty acid metabolism in butyrate-producing human colonic bacteria. Microbiology 152 : 179 182.[PubMed] [CrossRef]
25. Louis P,, Duncan SH,, McCrae SI,, Millar J,, Jackson MS,, Flint HJ . 2004. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186 : 2099 2106.[PubMed] [CrossRef]
26. Herrmann G,, Jayamani E,, Mai G,, Buckel W . 2008. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190 : 784 791.[PubMed] [CrossRef]
27. Dürre P,, Bahl H,, Gottschalk G, .. 1988. Membrane processes and product formation in anaerobes, p 187 220. In Erickson LE,, Fung DY-C (ed), Handbook on Anaerobic Fermentations. Marcel Dekker Inc., New York, NY.
28. Dürre P, . 2005. Formation of solvents in clostridia, p 671 693. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
29. Dürre P, . 2009. Metabolic networks in Clostridium acetobutylicum: interaction of sporulation, solventogenesis and toxin formation, p 215 227. In Brüggemann H,, Gottschalk G (ed), Clostridia. Molecular Biology in the Post-genomic Era. Caister Academic Press, Norfolk, United Kingdom.
30. Dürre P . 2007. Biobutanol: an attractive biofuel. Biotechnol J 2 : 1525 1534.[PubMed] [CrossRef]
31. Dürre P . 2011. Fermentative production of butanol – the academic perspective. Curr Opin Biotechnol 22 : 331 336.[PubMed] [CrossRef]
32. Green EM . 2011. Fermentative production of butanol – the industrial perspective. Curr Opin Biotechnol 22 : 337 343.[PubMed] [CrossRef]
33. Lütke-Eversloh T,, Bahl H . 2011. Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr Opin Biotechnol 22 : 634 647.[PubMed] [CrossRef]
34. Kenealy WR,, Waselefsky DM . 1985. Studies on the substrate range of Clostridium kluyveri: the use of propanol and succinate. Arch Microbiol 141 : 187 194.[CrossRef]
35. Gaston LW,, Stadtman ER . 1963. Fermentation of ethylene glycol by Clostridium glycolicum, sp. n. J Bacteriol 85 : 356 362.[PubMed]
36. Schink B . 1984. Clostridium magnum sp. nov., a non-autotrophic homoacetogenic bacterium. Arch Microbiol 137 : 250 255.[CrossRef]
37. Forsberg CW . 1987. Production of 1,3-propanediol from glycerol by Clostridium acetobutylicum and other Clostridium species. Appl Environ Microbiol 53 : 639 643.[PubMed]
38. Li F,, Hinderberger J,, Seedorf H,, Zhang J,, Buckel W,, Thauer RK . 2008. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri . J Bacteriol 190 : 843 850.[PubMed] [CrossRef]
39. Seedorf H,, Fricke WF,, Veith B,, Brüggemann H,, Liesegang H,, Strittmatter A,, Miethke M,, Buckel W,, Hinderberger J,, Li F,, Hagemeier C,, Thauer RK,, Gottschalk G . 2008. The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci USA 105 : 2128 2133.[PubMed] [CrossRef]
40. Buckel W, . 1990. Amino acid fermentations: coenzyme B 12-dependent and –independent pathways, p 21 30. In Hauska G,, Thauer RK (ed), The Molecular Basis of Bacterial Metabolism. Springer-Verlag, Heidelberg, Germany. [CrossRef]
41. Buckel W . 1991. Ungewöhnliche Chemie bei der Fermentation von Aminosäuren durch anaerobe Bakterien. Bioforum 14 : 7 19.
42. Buckel W, . 2005. Special clostridial enzymes and fermentation pathways, p 177 220. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
43. Dürre P,, Andersch W,, Andreesen JR . 1981. Isolation and characterization of an adenine-utilizing, anaerobic sporeformer, Clostridium purinolyticum sp. nov. Int J Syst Bacteriol 31 : 184 194.[CrossRef]
44. Dürre P,, Andreesen JR . 1982. Selenium-dependent growth and glycine fermentation by Clostridium purinolyticum . J Gen Microbiol 128 : 1457 1466.[PubMed]
45. Dürre P,, Andreesen JR . 1983. Purine and glycine metabolism by purinolytic clostridia. J Bacteriol 154 : 192 199.[PubMed]
46. Dürre P,, Andreesen JR . 1982. Anaerobic degradation of uric acid via pyrimidine derivatives by selenium-starved cells of Clostridium purinolyticum . Arch Microbiol 131 : 255 260.[PubMed] [CrossRef]
47. Andreesen JR, . 2005. Degradation of heterocyclic compounds, p 221 237. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
48. Vogels GD,, van der Drift C . 1976. Degradation of purines and pyrimidines by microorganisms. Bacteriol Rev 40 : 403 468.[PubMed]
49. Minton NP,, Clarke DJ . 1989. Clostridia. Plenum Press, New York, NY. [CrossRef]
50. Bahl H,, Dürre P, . 1993. Clostridia , p 285 323. In Rehm H-J,, Reed G,, Pühler A,, Stadler P, (ed), Biotechnology, vol 1. Sahm H (ed), Biological Fundamentals. VCH Verlagsgesellschaft mbH, Weinheim, Germany.
51. Labbé RG, . 2005. Sporulation (morphology) of clostridia, p 647 658. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
52. Reysenbach AL,, Ravenscroft N,, Long S,, Jones DT,, Woods DR . 1986. Characterization, biosynthesis, and regulation of granulose in Clostridium acetobutylicum . Appl Environ Microbiol 52 : 185 190.[PubMed]
53. Bergère JL,, Rousseau M,, Mercier C . 1975. Polyoside intracellulaire impliqué dans la sporulation de Clostridium butyricum. I. Cytologie, production et analyse enzymatique préliminaire. Ann Inst Pasteur Microbiol 126 : 295 314.
54. Brown RG,, Lindberg B,, Laishley EJ . 1975. Characterization of two reserve glucans from Clostridium pasteurianum . Can J Microbiol 21 : 1136 1138.[PubMed] [CrossRef]
55. Darvill AG,, Hall MA,, Fish JP,, Morris JG . 1977. The intracellular reserve polysaccharide of Clostridium pasteurianum . Can J Microbiol 23 : 947 953.[PubMed] [CrossRef]
56. Hobson PN,, Nasr H . 1951. An amylopectin-type polysaccharide synthesized from sucrose by C. butyricum . J Chem Soc 1951 : 1855 1857.[CrossRef]
57. Whyte JNC,, Strasdine GA . 1972. An intracellular α-D-glucan from Clostridium botulinum, type E. Carbohydr Res 25 : 435 441.[PubMed] [CrossRef]
58. McCoy E,, Fred EB,, Peterson WH,, Hastings EG . 1926. A cultural study of the acetone butyl alcohol organism. J Infect Dis 39 : 457 483.[CrossRef]
59. Spray RS . 1948. The granulose reaction of certain anaerobes of the “butyric” group. J Bacteriol 55 : 79 84.[PubMed]
60. Orsburn BC,, Melville SB,, Popham DL . 2010. EtfA catalyses the formation of dipicolinic acid in Clostridium perfringens . Mol Microbiol 75 : 178 186.[PubMed] [CrossRef]
61. Cabrera-Martinez RM,, Mason JM,, Setlow B,, Waites WM,, Setlow P . 1989. Purification and amino acid sequence of two small, acid-soluble proteins from Clostridium bifermentans spores. FEMS Microbiol Lett 52 : 139 143.[PubMed] [CrossRef]
62. Cabrera-Martinez RM,, Setlow P . 1991. Cloning and nucleotide sequence of three genes coding for small, acid-soluble proteins of Clostridium perfringens spores. FEMS Microbiol Lett 61 : 127 131.[PubMed] [CrossRef]
63. Huang I-H,, Raju D,, Paredes-Sabja D,, Sarker MR . 2007. Clostridium perfringens: sporulation, spore resistance and germination. Bangladesh J Microbiol 24 : 1 8.
64. Paredes-Sabja D,, Raju D,, Torres JA,, Sarker MR . 2008. Role of small, acid-soluble spore proteins in the resistance of Clostridium perfringens spores to chemicals. Int J Food Microbiol 122 : 333 335.[PubMed] [CrossRef]
65. Raju D,, Waters M,, Setlow P,, Sarker MR . 2006. Investigating the role of small, acid-soluble spore proteins (SASPs) in the resistance of Clostridium perfringens spores to heat. BMC Microbiol 6 : 50. doi:10.1186/1471-2180-6-50 [CrossRef]
66. Raju D,, Setlow P,, Sarker MR . 2007. Antisense-RNA-mediated decreased synthesis of small, acid-soluble spore proteins leads to decreased resistance of Clostridium perfringens spores to moist heat and UV radiation. Appl Environ Microbiol 73 : 2048 2053.[PubMed] [CrossRef]
67. Carpenter CE,, Reddy DSA,, Cornforth DP . 1987. Inactivation of clostridial ferredoxin and pyruvate-ferredoxin oxidoreductase by sodium nitrite. Appl Environ Microbiol 53 : 549 552.[PubMed]
68. Reddy D,, Lancaster LR Jr,, Cornforth DP . 1983. Nitrite inhibition of Clostridium botulinum: electron spin resonance detection of iron-nitric oxide complexes. Science 221 : 769 770.[PubMed] [CrossRef]
69. Scheeff ED,, Axelrod HL,, Miller MD,, Chiu H-J,, Deacon AM,, Wilson IA,, Manning G . 2010. Genomics, evolution, and crystal structure of a new family of bacterial spore kinases. Proteins 78 : 1470 1482.[PubMed] [CrossRef]
70. Dalla Vecchia E,, Veeramani H,, Suvorova EI,, Wigginton NS,, Bargar JR,, Bernier-Latmani R . 2010. U(VI) reduction by spores of Clostridium acetobutylicum . Res Microbiol 161 : 765 771.[PubMed] [CrossRef]
71. Permpoonpattana P,, Tolls EH,, Nadem R,, Tan S,, Brisson A,, Cutting SM . 2011. Surface layers of Clostridium difficile endospores. J Bacteriol 193 : 6461 6470.[PubMed] [CrossRef]
72. Dürre P,, Hollergschwandner C . 2004. Initiation of endospore formation in Clostridium acetobutylicum . Anaerobe 10 : 69 74.[PubMed] [CrossRef]
73. Dürre P, . 2005. Sporulation in clostridia (genetics), p 659 669. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
74. Stragier P, . 2002. A gene odyssey: exploring the genomes of endospore-forming bacteria, p 519 525. In Sonenshein AL,, Hoch JA,, Losick R (ed), Bacillus subtilis and its closest relatives: From Genes to Cells. American Society for Microbiology, Washington, DC. [CrossRef]
75. Paredes CJ,, Alsaker KV,, Papoutsakis ET . 2005. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 3 : 969 978.[PubMed] [CrossRef]
76. Stephenson K,, Lewis RJ . 2005. Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon. FEMS Microbiol Lett 29 : 281 301.[PubMed] [CrossRef]
77. Brown DP,, Ganova-Raeva L,, Green BD,, Wilkinson SR,, Young M,, Youngman P . 1994. Characterization of spo0A homologs in diverse Bacillus and Clostridium species reveals regions of high conservation within the effector domain. Mol Microbiol 14 : 411 426.[PubMed] [CrossRef]
78. Gutierrez Escobar AJ,, Montoya Castaño D . 2009. Evolutionary analysis for the functional divergence of the Spo0A protein: the key sporulation control element. In Silico Biol 9 : 149 162.[PubMed]
79. Hilbert DW,, Piggot PJ . 2004. Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 68 : 234 262.[PubMed] [CrossRef]
80. Nölling J,, Breton G,, Omelchenko MV,, Makarova KS,, Zeng Q,, Gibson R,, Lee HM,, Dubois J,, Qiu D,, Hitti J,, GTC Sequencing Center Production, Finishing, and Bioinformatics Teams, Wolf YI,, Tatusov RL,, Sabathe F,, Doucette-Stamm L,, Soucaille P,, Daly MJ,, Bennett GN,, Koonin EV,, Smith DR . 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum . J Bacteriol 183 : 4823 4838.[PubMed] [CrossRef]
81. Sauer U,, Treuner A,, Buchholz M,, Santangelo JD,, Dürre P . 1994. Sporulation and primary sigma factor homologous genes in Clostridium acetobutylicum . J Bacteriol 176 : 6572 6582.[PubMed]
82. Santangelo JD,, Kuhn A,, Treuner-Lange A,, Dürre P . 1998. Sporulation and time course expression of sigma-factor homologous genes in Clostridium acetobutylicum . FEMS Microbiol Lett 161 : 157 164.[PubMed] [CrossRef]
83. Jones SW,, Tracy BP,, Gaida SM,, Papoutsakis ET . 2011. Inactivation of σ F in Clostridium acetobutylicum ATCC 824 blocks sporulation prior to asymmetric division and abolishes σ E and σ G protein expression but does not block solvent formation. J Bacteriol 193 : 242 2440.[PubMed] [CrossRef]
84. Li J,, McClane BA . 2010. Evaluating the involvement of alternative sigma factors SigF and SigG in Clostridium perfringens sporulation and enterotoxin synthesis. Infect Immun 78 : 4286 4293.[PubMed] [CrossRef]
85. Scotcher MC,, Bennett GN . 2005. SpoIIE regulates sporulation but does not directly affect solventogenesis in Clostridium acetobutylicum ATCC 824. J Bacteriol 187 : 1930 1936.[PubMed] [CrossRef]
86. Bi C,, Jones SW,, Hess DR,, Tracy BP,, Papoutsakis ET . 2011. SpoIIE is necessary for asymmetric division, sporulation, and expression of σ F, σ E, and σ G but does not control solvent production in Clostridium acetobutylicum ATCC 824. J Bacteriol 193 : 5130 5137.[PubMed] [CrossRef]
87. Tracy BP,, Jones AW,, Papoutsakis ET . 2011. Inactivation of σ E and σ G in Clostridium acetobutylicum illuminates their roles in clostridial-cell-form biogenesis, granulose synthesis, solventogenesis, and spore morphogenesis. J Bacteriol 193 : 1414 1426.[PubMed] [CrossRef]
88. Harry KH,, Zhou R,, Kroos L,, Melville SB . 2009. Sporulation and enterotoxin (CPE) synthesis are controlled by the sporulation-specific sigma factors SigE and SigK in Clostridium perfringens . J Bacteriol 191 : 2728 2742.[PubMed] [CrossRef]
89. Jones SW,, Paredes CJ,, Tracy B,, Cheng N,, Sillers R,, Senger RS,, Papoutsakis ET . 2008. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol 9 : R114. doi:10.1186/gb-2008-9-7-r114. [PubMed] [CrossRef]
90. Haraldsen JD,, Sonenshein AL . 2003. Efficient sporulation in Clostridium difficile requires disruption of the σ K gene. Mol Microbiol 48 : 811 821.[PubMed] [CrossRef]
91. Kirk DG,, Dahlsten E,, Zhang Z,, Korkeala H,, Lindström M . 2012. Clostridium botulinum ATCC 3502 sigma factor K is involved with early stage sporulation. Appl Environ Microbiol 78 : 4590 4596.[PubMed] [CrossRef]
92. Saujet L,, Monot M,, Dupuy B,, Soutourina O,, Martin-Verstraete I . 2011. The key sigma factor of transition phase, SigH, controls sporulation, metabolism, and virulence factor expression in Clostridium difficile . J Bacteriol 193 : 3186 3196.[PubMed] [CrossRef]
93. Burns DA,, Minton NP . 2011. Sporulation studies in Clostridium difficile . J Microbiol Methods 87 : 133 138.[PubMed] [CrossRef]
94. Burns DA,, Heeg D,, Cartman ST,, Minton NP . 2011. Reconsidering the sporulation characteristics of hypervirulent Clostridium difficile BI/NAP1/027. PLoS One. 6( 9) : e24894. doi:10.1371/journal.pone.0024894. [PubMed] [CrossRef]
95. Doß S,, Gröger C,, Knauber T,, Whitworth DE,, Treuner-Lange A, . 2005. Comparative genomic analysis of signal transduction proteins in clostridia, p 561 582. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
96. Steiner E,, Dago AE,, Young DI,, Heap JT,, Minton NP,, Hoch JA,, Young M . 2011. Multiple orphan histidine kinases interact directly with Spo0A to control initiation of endospore formation in Clostridium acetobutylicum . Mol Microbiol 80 : 641 654.[PubMed] [CrossRef]
97. Dürre P . 2011. Ancestral sporulation initiation. Mol Microbiol 80 : 584 587.[PubMed] [CrossRef]
98. Harris LM,, Welker NE,, Papoutsakis ET . 2002. Northern, morphological, and fermentation analysis of spo0A inactivation and overexpression in Clostridium acetobutylicum ATCC 824. J Bacteriol 184 : 3586 3597.[PubMed] [CrossRef]
99. Köpke M,, Dürre P, .. 2010. Biochemical production of biobutanol, p 221 257. In Luque R,, Campelo J,, Clark J (ed), Handbook of Biofuels Production. Woodhead Publishing Ltd, Abington, Cambridge, UK.
100. Ravagnani A,, Jennert KCB,, Steiner E,, Grünberg R,, Jefferies JR,, Wilkinson SR,, Young DI,, Tidswell EC,, Brown DP,, Youngman P,, Morris JG,, Young M . 2000. Spo0A directly controls the switch from acid to solvent production in solvent-forming clostridia. Mol Microbiol 37 : 1172 1185.[PubMed] [CrossRef]
101. Paredes-Sabja D,, Sarker N,, Sarker MR . 2011. Clostridium perfringen stpeL is expressed during sporulation. Microbial Pathogen 51 : 384 388.[PubMed] [CrossRef]
102. Popoff MR,, Stiles BG, . 2005. Clostridial toxins vs. other bacterial toxins, p 323 383. In Dürre P (ed), Handbook on Clostridia. CRC Press, Taylor & Francis Group, Boca Raton, FL.
103. Carter GP,, Douce GR,, Govind R,, Howarth PM,, Mackin KE,, Spencer J,, Buckley AM,, Antunes A,, Kotsanas D,, Jenkin GA,, Dupuy B,, Rood JI,, Lyras D . 2011. The anti-sigma factor TcdC modulates hypervirulence in an epidemic BI/NAP1/027 clinical isolate of Clostridium difficile . PLoS Pathog 7( 10) : e1002317. doi:10.1371/journal.ppat.1002317. [PubMed] [CrossRef]
104. Underwood S,, Guan S,, Vijayasubhash V,, Baines SD,, Graham L,, Lewis RJ,, Wilcox MH,, Stephenson K . 2009. Characterization of the sporulation initiation pathway of Clostridium difficile and its role in toxin production. J Bacteriol 191 : 7296 7305.[PubMed] [CrossRef]
105. Deakin LJ,, Clare S,, Fagan RP,, Dawson LF,, Pickard DJ,, West MR,, Wren BW,, Fairweather NF,, Dougan G,, Lawley TD . 2012. Clostridium difficile spo0A gene is a persistence and transmission factor. Infect Immun 80 : 2704 2711.[PubMed] [CrossRef]
106. Lyras D,, O’Connor JR,, Howarth PM,, Sambol SP,, Carter GP,, Phumoonna T,, Poon R,, Adams V,, Vedantam G,, Johnson S,, Gerding DN,, Rood JI . 2009. Toxin B is essential for virulence of Clostridium difficile . Nature 458 : 1176 1179.[PubMed] [CrossRef]
107. Kuehne SA,, Cartman ST,, Heap JT,, Kelly ML,, Cockayne A,, Minton NP . 2010. The role of toxin A and toxin B in Clostridium difficile infection. Nature 467 : 711 713.[PubMed] [CrossRef]
108. Nakamura S,, Serikawa T,, Yamakawa K,, Nishida S,, Kozaki S,, Sakaguchi G . 1978. Sporulation and C2 toxin production by Clostridium botulinum type C strains producing no C1 toxin. Microbiol Immunol 22 : 591 596.[PubMed] [CrossRef]
109. Cooksley CM,, Davis IJ,, Winzer K,, Chan WC,, Peck MW,, Minton NP . 2010. Regulation of neurotoxin production and sporulation by a putative agrBD signaling system in proteolytic Clostridium botulinum . Appl Environ Microbiol 76 : 4448 4460.[CrossRef]
110. Li J,, Chen J,, Vidal JE,, McClane BA . 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. Infect Immun 79 : 2451 2459.[PubMed] [CrossRef]
111. Steiner E,, Scott J,, Minton NP,, Winzer K . 2012. An agr quorum sensing system that regulates granulose formation and sporulation in Clostridium acetobutylicum . Appl Environ Microbiol 78 : 1113 1122.[PubMed] [CrossRef]
112. Marchais A,, Duperrier S,, Durand S,, Gautheret D,, Stragier P . 2011. CsfG, a sporulation-specific, small non-coding RNA highly conserved in endospore formers. RNA Biol 8 : 358 364.[PubMed] [CrossRef]
113. Brousolle V,, Alberto F,, Shearman CA,, Mason DR,, Botella L,, Nguyen-The C,, Peck MW,, Carlin F . 2002. Molecular and physiological characterization of spore germination in Clostridium botulinum and C. sporogenes . Anaerobe 8 : 89 100.[CrossRef]
114. 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.[PubMed] [CrossRef]
115. Paredes-Sabja D,, Udompijitkul P,, Sarker MR . 2009. Inorganic phosphate and sodium ions are cogerminants for spores of Clostridium perfringens type A food poisoning-related isolates. Appl Environ Microbiol 75 : 6299 6305.[PubMed] [CrossRef]
116. Heeg D,, Burns DA,, Cartman ST,, Minton NP . 2012. Spores of Clostridium difficile clinical isolates display a diverse germination response to bile salts. PLoS One 7( 2) : e32381. doi:10.1371/journal.pone.0032381. [PubMed] [CrossRef]
117. Paredes-Sabja D,, Bond C,, Carman RJ,, Setlow P,, Sarker MR . 2008. Germination of spores of Clostridium difficile strains, including isolates from a hospital outbreak of Clostridium difficile-associated disease (CDAD). Microbiology 154 : 2241 2250.[PubMed] [CrossRef]
118. Sorg JA,, Sonenshein AL . 2008. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol 190 : 2505 2512.[PubMed] [CrossRef]
119. Paredes-Sabja D,, Setlow P,, Sarker MR . 2009. Role of GerKB in germination and outgrowth of Clostridium perfringens spores. Appl Environ Microbiol 75 : 3813 3817.[PubMed] [CrossRef]
120. 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.[PubMed] [CrossRef]
121. Makino S,, Moriyama R . 2002. Hydrolysis of cortex peptidoglycan during bacterial spore germination. Med Sci Monit 8 : RA119 127.[PubMed]
122. Miyata S,, Kozuka S,, Yasuda Y,, Chen Y,, Moriyama R,, Tochikubo K,, Makino S . 1997. Localization of germination-specific spore-lytic enzymes in Clostridium perfringens S40 spores detected by immunoelectron microscopy. FEMS Microbiol Lett 152 : 243 247.[PubMed] [CrossRef]
123. Kumazawa T,, Masayama A,, Fukuoka S,, Makino S,, Yoshimura T,, Moriyama R . 2007. Mode of action of a germination-specific cortex-lytic enzyme, SleC, of Clostridium perfringens S40. Biosci Biotechnol Biochem 71 : 884 892.[PubMed] [CrossRef]
124. 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.[PubMed] [CrossRef]
125. 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.[PubMed] [CrossRef]
126. Xiao Y,, Francke C,, Abee T,, Wells-Bennik MHJ . 2011. Clostridial spore germination versus bacilli: genome mining and current insights. Food Microbiol 28 : 266 274.[PubMed] [CrossRef]
127. Bader J,, Albin A,, Stahl U . 2012. Spore-forming bacteria and their utilisation as probiotics. Benef Microbes 3 : 67 75.[PubMed] [CrossRef]
128. Okamoto T,, Sasaki M,, Tsujikawa T,, Fujiyama Y,, Bamba T,, Kusunoki M . 2000. Preventive efficacy of butyrate enemas and oral administration of Clostridium butyricum M588 in dextran sodium sulfate-induced colitis in rats. J Gastroenterol 35 : 341 346.[PubMed] [CrossRef]
129. Takahashi M,, Taguchi H,, Yamaguchi H,, Osaki T,, Komatsu A,, Kamiya S . 2004. The effect of probiotic treatment with Clostridium butyricum on enterohemorrhagic Escherichia coli O157:H7 infection in mice. FEMS Immunol Med Microbiol 41 : 219 226.[PubMed] [CrossRef]
130. Mengesha A,, Wie JZ,, Zhou S-F,, Wie MQ . 2010. Clostridial spores to treat solid tumours – potential for a new therapeutic model. Curr Gene Ther 10 : 15 26.[PubMed]
131. Minton NP,, Mauchline ML,, Lemmon MJ,, Brehm JK,, Fox M,, Michael NP,, Giaccia A,, Brown JM . 1995. Chemotherapeutic tumour targeting using clostridial spores. FEMS Microbiol Rev 17 : 357 364.[PubMed] [CrossRef]
132. Minton NP . 2003. Clostridia in cancer therapy. Nat Rev Microbiol 1 : 237 242.[PubMed] [CrossRef]
133. Brown JM,, Liu S-C, . 2004. Use of anaerobic bacteria for cancer therapy, p 211 219. In Nakano MM,, Zuber P (ed), Strict and Facultative Anaerobes. Medical and Environmental Aspects. Horizon Bioscience, Wymondham, UK.
134. Lambin P,, Theys J,, Landuyt W,, Rijken P,, van der Kogel A,, van der Schueren E,, Hodgkiss R,, Fowler J,, Nuyts S,, de Bruijn E,, van Mellaert L,, Anné J . 1998. Colonization of Clostridium in the body is restricted to hypoxic and necrotic areas of tumours. Anaerobe 4 : 183 188.[PubMed] [CrossRef]
135. Barbé S,, van Mellaert L,, Theys J,, Geukens N,, Lammertyn E,, Lambin P,, Anné J . 2005. Secretory production of biologically active rat interleukin-2 by Clostridium acetobutylicum DSM792 as a tool for anti-tumor treatment. FEMS Microbiol Lett 246 : 67 73.[PubMed] [CrossRef]
136. Theys J,, Nuyts S,, Landuyt W,, van Mellaert L,, Dillen C,, Böhringer M,, Dürre P,, Lambin P,, Anné J . 1999. Stable Escherichia coli-Clostridium acetobutylicum shuttle vector for secretion of murine tumor necrosis factor alpha. Appl Environ Microbiol 65 : 4295 4300.[PubMed]
137. Dang LH,, Bettegowda C,, Huso DL,, Kinzler KW,, Vogelstein B . 2001. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci USA 98 : 15155 15160.[PubMed] [CrossRef]


Generic image for table
Table 1

Major metabolic features of

Citation: Dürre P. 2016. Physiology and Sporulation in , p 315-329. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0010-2012

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error