The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Al-Hinai, Mohab A.; Jones, Shawn W.; Papoutsakis, Eleftherios T.

doi:10.1128/MMBR.00025-14

Title: The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Journal Article · Wed Jan 28 00:00:00 EST 2015 · Microbiology and Molecular Biology Reviews

DOI:https://doi.org/10.1128/MMBR.00025-14· OSTI ID:1454688

Al-Hinai, Mohab A. ^[1]; Jones, Shawn W. ^[2]; Papoutsakis, Eleftherios T. ^[3]

Univ. of Delaware, Newark, DE (United States); Sultan Qaboos Univ., Muscat (Oman)
Elcriton Inc., New Castle, DE (United States)
Elcriton Inc., New Castle, DE (United States); Univ. of Delaware, Newark, DE (United States)

Bacillus and Clostridium organisms initiate the sporulation process when unfavorable conditions are detected. The sporulation process is a carefully orchestrated cascade of events at both the transcriptional and posttranslational levels involving a multitude of sigma factors, transcription factors, proteases, and phosphatases. Like Bacillus genomes, sequenced Clostridium genomes contain genes for all major sporulation-specific transcription and sigma factors (spo0A, sigH, sigF, sigE, sigG, and sigK) that orchestrate the sporulation program. However, recent studies have shown that there are substantial differences in the sporulation programs between the two genera as well as among different Clostridium species. First, in the absence of a Bacillus-like phosphorelay system, activation of Spo0A in Clostridium organisms is carried out by a number of orphan histidine kinases. Second, downstream of Spo0A, the transcriptional and posttranslational regulation of the canonical set of four sporulation-specific sigma factors (σF, σE, σG, and σK) display different patterns, not only compared to Bacillus but also among Clostridium organisms. Finally, recent studies demonstrated that σK, the last sigma factor to be activated according to the Bacillus subtilis model, is involved in the very early stages of sporulation in Clostridium acetobutylicum, C. perfringens, and C. botulinum as well as in the very late stages of spore maturation in C. acetobutylicum. Despite profound differences in initiation, propagation, and orchestration of expression of spore morphogenetic components, these findings demonstrate not only the robustness of the endospore sporulation program but also the plasticity of the program to generate different complex phenotypes, some apparently regulated at the epigenetic level.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Delaware, Newark, DE (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: sc0007092

OSTI ID:: 1454688

Journal Information:: Microbiology and Molecular Biology Reviews, Vol. 79, Issue 1; ISSN 1092-2172

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 114 works

Citation information provided by
Web of Science

References (116)

The identification of four histidine kinases that influence sporulation in Clostridium thermocellum Mearls, Elizabeth B.; Lynd, Lee R. Anaerobe, Vol. 28 https://doi.org/10.1016/j.anaerobe.2014.06.004	journal	August 2014
Control of the Expression and Compartmentalization of G Activity during Sporulation of Bacillus subtilis by Regulators of F and E Chary, V. K.; Meloni, M.; Hilbert, D. W. Journal of Bacteriology, Vol. 187, Issue 19 https://doi.org/10.1128/JB.187.19.6832-6840.2005	journal	September 2005
Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications Tracy, Bryan P.; Jones, Shawn W.; Fast, Alan G. Current Opinion in Biotechnology, Vol. 23, Issue 3 https://doi.org/10.1016/j.copbio.2011.10.008	journal	June 2012
Localization of a second SigH promoter in the Bacillus subtilis sigA operon and regulation of dnaE expression by the promoter. Qi, F. X.; Doi, R. H. Journal of Bacteriology, Vol. 172, Issue 10 https://doi.org/10.1128/jb.172.10.5631-5636.1990	journal	October 1990
Fermentative production of butanol—the industrial perspective Green, Edward M. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2011.02.004	journal	June 2011
Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum: Sporulation initiation in clostridia Steiner, Elisabeth; Dago, Angel E.; Young, Danielle I. Molecular Microbiology, Vol. 80, Issue 3 https://doi.org/10.1111/j.1365-2958.2011.07608.x	journal	March 2011
Sigma factor and sporulation genes in Clostridium Sauer, Uwe; Santangelo, Joseph D.; Treuner, Anke FEMS Microbiology Reviews, Vol. 17, Issue 3 https://doi.org/10.1111/j.1574-6976.1995.tb00216.x	journal	October 1995
The genome sequence of Clostridium tetani, the causative agent of tetanus disease Bruggemann, H.; Baumer, S.; Fricke, W. F. Proceedings of the National Academy of Sciences, Vol. 100, Issue 3 https://doi.org/10.1073/pnas.0335853100	journal	January 2003
Involvement of Clostridium botulinum ATCC 3502 Sigma Factor K in Early-Stage Sporulation Kirk, David G.; Dahlsten, Elias; Zhang, Zhen Applied and Environmental Microbiology, Vol. 78, Issue 13 https://doi.org/10.1128/AEM.00304-12	journal	April 2012
Expression of abrB310 and sinR, and Effects of Decreased abrB310 Expression on the Transition from Acidogenesis to Solventogenesis, in Clostridium acetobutylicum ATCC 824 Scotcher, M. C.; Rudolph, F. B.; Bennett, G. N. Applied and Environmental Microbiology, Vol. 71, Issue 4 https://doi.org/10.1128/AEM.71.4.1987-1995.2005	journal	April 2005
A Life with Acetogens, Thermophiles, and Cellulolytic Anaerobes Ljungdahl, Lars G. Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073617	journal	October 2009
Development and Characterization of a Gene Expression Reporter System for Clostridium acetobutylicumATCC 824 Tummala, Seshu B.; Welker, Neil E.; Papoutsakis, Eleftherios T. Applied and Environmental Microbiology, Vol. 65, Issue 9 https://doi.org/10.1128/AEM.65.9.3793-3799.1999	journal	September 1999
Sporulation and Enterotoxin (CPE) Synthesis Are Controlled by the Sporulation-Specific Sigma Factors SigE and SigK in Clostridium perfringens Harry, K. H.; Zhou, R.; Kroos, L. Journal of Bacteriology, Vol. 191, Issue 8 https://doi.org/10.1128/JB.01839-08	journal	February 2009
Bet-hedging and epigenetic inheritance in bacterial cell development Veening, J. -W.; Stewart, E. J.; Berngruber, T. W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 11 https://doi.org/10.1073/pnas.0700463105	journal	March 2008
The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. Strauch, M. A.; Spiegelman, G. B.; Perego, M. The EMBO Journal, Vol. 8, Issue 5 https://doi.org/10.1002/j.1460-2075.1989.tb03546.x	journal	May 1989
Bistability, Epigenetics, and Bet-Hedging in Bacteria Veening, Jan-Willem; Smits, Wiep Klaas; Kuipers, Oscar P. Annual Review of Microbiology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.163002	journal	October 2008
Expression of kinA and kinB of Bacillus subtilis, Necessary for Sporulation Initiation, Is under Positive Stringent Transcription Control Tojo, S.; Hirooka, K.; Fujita, Y. Journal of Bacteriology, Vol. 195, Issue 8 https://doi.org/10.1128/JB.02131-12	journal	February 2013
Regulation of transcription of the Bacillus subtilis spoIIA locus. Wu, J. J.; Howard, M. G.; Piggot, P. J. Journal of Bacteriology, Vol. 171, Issue 2 https://doi.org/10.1128/jb.171.2.692-698.1989	journal	February 1989
Promoter specificity of sigma G-containing RNA polymerase from sporulating cells of Bacillus subtilis: identification of a group of forespore-specific promoters. Nicholson, W. L.; Sun, D. X.; Setlow, B. Journal of Bacteriology, Vol. 171, Issue 5 https://doi.org/10.1128/jb.171.5.2708-2718.1989	journal	May 1989
Deciding fate in adverse times: Sporulation and competence in Bacillus subtilis Schultz, Daniel; Wolynes, Peter G.; Jacob, Eshel Ben Proceedings of the National Academy of Sciences, Vol. 106, Issue 50 https://doi.org/10.1073/pnas.0912185106	journal	December 2009
Role of the Anti-Sigma Factor SpoIIAB in Regulation of G during Bacillus subtilis Sporulation Serrano, M.; Neves, A.; Soares, C. M. Journal of Bacteriology, Vol. 186, Issue 12 https://doi.org/10.1128/JB.186.12.4000-4013.2004	journal	June 2004
Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Schmidt, R.; Margolis, P.; Duncan, L. Proceedings of the National Academy of Sciences, Vol. 87, Issue 23 https://doi.org/10.1073/pnas.87.23.9221	journal	December 1990
Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay Trach, K.; Burbulys, D.; Strauch, M. Research in Microbiology, Vol. 142, Issue 7-8 https://doi.org/10.1016/0923-2508(91)90060-N	journal	January 1991
Bile Salts and Glycine as Cogerminants for Clostridium difficile Spores Sorg, J. A.; Sonenshein, A. L. Journal of Bacteriology, Vol. 190, Issue 7 https://doi.org/10.1128/JB.01765-07	journal	February 2008
Binding of the Bacillus subtilis spoIVCA product to the recombination sites of the element interrupting the sigma K-encoding gene. Popham, D. L.; Stragier, P. Proceedings of the National Academy of Sciences, Vol. 89, Issue 13 https://doi.org/10.1073/pnas.89.13.5991	journal	July 1992
Regulation of the Phosphorelay and the Initiation of Sporulation in Bacillus Subtilis Hoch, J. A. Annual Review of Microbiology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.mi.47.100193.002301	journal	October 1993
Genome Sequence and Comparative Analysis of the Solvent-Producing Bacterium Clostridium acetobutylicum Nolling, J.; Breton, G.; Omelchenko, M. V. Journal of Bacteriology, Vol. 183, Issue 16 https://doi.org/10.1128/JB.183.16.4823-4838.2001	journal	August 2001
Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis. Londono-Vallejo, J. A.; Stragier, P. Genes & Development, Vol. 9, Issue 4 https://doi.org/10.1101/gad.9.4.503	journal	February 1995
The transcriptional program underlying the physiology of clostridial sporulation Jones, Shawn W.; Paredes, Carlos J.; Tracy, Bryan Genome Biology, Vol. 9, Issue 7 https://doi.org/10.1186/gb-2008-9-7-r114	journal	January 2008
K of Clostridium acetobutylicum Is the First Known Sporulation-Specific Sigma Factor with Two Developmentally Separated Roles, One Early and One Late in Sporulation Al-Hinai, M. A.; Jones, S. W.; Papoutsakis, E. T. Journal of Bacteriology, Vol. 196, Issue 2 https://doi.org/10.1128/JB.01103-13	journal	November 2013
Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor Kroos, L.; Kunkel, B.; Losick, R. Science, Vol. 243, Issue 4890 https://doi.org/10.1126/science.2492118	journal	January 1989
Sporulation Regulatory Protein SpoIIID from Bacillus subtilis Activates and Represses Transcription by Both Mother-cell-specific Forms of RNA Polymerase Halberg, Richard; Kroos, Lee Journal of Molecular Biology, Vol. 243, Issue 3 https://doi.org/10.1006/jmbi.1994.1670	journal	October 1994
Timing of spoII gene expression relative to septum formation during sporulation of Bacillus subtilis. Gholamhoseinian, A.; Piggot, P. J. Journal of Bacteriology, Vol. 171, Issue 10 https://doi.org/10.1128/jb.171.10.5747-5749.1989	journal	October 1989
Colonisation ofClostridiumin the body is restricted to hypoxic and necrotic areas of tumours Lambin, P.; Theys, J.; Landuyt, W. Anaerobe, Vol. 4, Issue 4 https://doi.org/10.1006/anae.1998.0161	journal	August 1998
A comparative genomic view of clostridial sporulation and physiology Paredes, Carlos J.; Alsaker, Keith V.; Papoutsakis, Eleftherios T. Nature Reviews Microbiology, Vol. 3, Issue 12 https://doi.org/10.1038/nrmicro1288	journal	October 2005
Bacillus sporulation gene spo0H codes for sigma 30 (sigma H). Dubnau, E.; Weir, J.; Nair, G. Journal of Bacteriology, Vol. 170, Issue 3 https://doi.org/10.1128/jb.170.3.1054-1062.1988	journal	March 1988
The relationship between sporulation and solvent production in clostridium acetobutylicum P262 Long, Susan; Jones, David T.; Woods, David R. Biotechnology Letters, Vol. 6, Issue 8 https://doi.org/10.1007/BF00139997	journal	August 1984
Novel System for Efficient Isolation of Clostridium Double-Crossover Allelic Exchange Mutants Enabling Markerless Chromosomal Gene Deletions and DNA Integration Al-Hinai, Mohab A.; Fast, Alan G.; Papoutsakis, Eleftherios T. Applied and Environmental Microbiology, Vol. 78, Issue 22 https://doi.org/10.1128/AEM.02214-12	journal	September 2012
RNA Polymerase and Alternative σ Factors Dupuy, Bruno; Sonenshein, Abraham; Haraldsen, Jeralyn Handbook on Clostridia https://doi.org/10.1201/9780203489819.ch26	book	March 2005
Chromosomal rearrangement generating a composite gene for a developmental transcription factor Stragier, P.; Kunkel, B.; Kroos, L. Science, Vol. 243, Issue 4890 https://doi.org/10.1126/science.2536191	journal	January 1989
Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater Shimizu, T.; Ohtani, K.; Hirakawa, H. Proceedings of the National Academy of Sciences, Vol. 99, Issue 2 https://doi.org/10.1073/pnas.022493799	journal	January 2002
Chemotherapeutic tumour targeting using clostridial spores Minton, Nigel P.; Mauchline, Margaret L.; Lemmon, Marylin J. FEMS Microbiology Reviews, Vol. 17, Issue 3 https://doi.org/10.1111/j.1574-6976.1995.tb00219.x	journal	October 1995
Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by the RNA polymerase containing sigma H. Predich, M.; Nair, G.; Smith, I. Journal of Bacteriology, Vol. 174, Issue 9 https://doi.org/10.1128/jb.174.9.2771-2778.1992	journal	May 1992
Evaluating the Involvement of Alternative Sigma Factors SigF and SigG in Clostridium perfringens Sporulation and Enterotoxin Synthesis Li, J.; McClane, B. A. Infection and Immunity, Vol. 78, Issue 10 https://doi.org/10.1128/IAI.00528-10	journal	July 2010
Genome-Wide Analysis of Cell Type-Specific Gene Transcription during Spore Formation in Clostridium difficile Saujet, Laure; Pereira, Fátima C.; Serrano, Monica PLoS Genetics, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pgen.1003756	journal	October 2013
Bacterial sporulation: A question of commitment? Stephens, Craig Current Biology, Vol. 8, Issue 2 https://doi.org/10.1016/S0960-9822(98)70031-4	journal	January 1998
The ClosTron: A universal gene knock-out system for the genus Clostridium Heap, John T.; Pennington, Oliver J.; Cartman, Stephen T. Journal of Microbiological Methods, Vol. 70, Issue 3 https://doi.org/10.1016/j.mimet.2007.05.021	journal	September 2007
MOLECULAR GENETICS OF SPORULATION IN BACILLUS SUBTILIS Stragier, Patrick; Losick, Richard Annual Review of Genetics, Vol. 30, Issue 1 https://doi.org/10.1146/annurev.genet.30.1.297	journal	December 1996
Sporulation-specific sigma factor sigma 29 of Bacillus subtilis is synthesized from a precursor protein, P31. LaBell, T. L.; Trempy, J. E.; Haldenwang, W. G. Proceedings of the National Academy of Sciences, Vol. 84, Issue 7 https://doi.org/10.1073/pnas.84.7.1784	journal	April 1987
Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis Lopez, D.; Fischbach, M. A.; Chu, F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 1 https://doi.org/10.1073/pnas.0810940106	journal	December 2008
Activation of spo0A transcription by sigma H is necessary for sporulation but not for competence in Bacillus subtilis. Siranosian, K. J.; Grossman, A. D. Journal of Bacteriology, Vol. 176, Issue 12 https://doi.org/10.1128/jb.176.12.3812-3815.1994	journal	June 1994
Prespore-specific gene expression in Bacillus subtilis is driven by sequestration of SpoIIE phosphatase to the prespore side of the asymmetric septum Wu, L. J.; Feucht, A.; Errington, J. Genes & Development, Vol. 12, Issue 9 https://doi.org/10.1101/gad.12.9.1371	journal	May 1998
Septation, dephosphorylation, and the activation of sigma F during sporulation in Bacillus subtilis King, N.; Dreesen, O.; Stragier, P. Genes & Development, Vol. 13, Issue 9 https://doi.org/10.1101/gad.13.9.1156	journal	May 1999
Hierarchical Evolution of the Bacterial Sporulation Network de Hoon, Michiel J. L.; Eichenberger, Patrick; Vitkup, Dennis Current Biology, Vol. 20, Issue 17 https://doi.org/10.1016/j.cub.2010.06.031	journal	September 2010
Delineation of AbrB-binding sites on the Bacillus subtilis spo0H, kinB, ftsAZ, and pbpE promoters and use of a derived homology to identify a previously unsuspected binding site in the bsuB1 methylase promote. Strauch, M. A. Journal of Bacteriology, Vol. 177, Issue 23 https://doi.org/10.1128/jb.177.23.6999-7002.1995	journal	December 1995
Regulation of Bacillus subtilis sigmaH (spo0H) and AbrB in response to changes in external pH. Cosby, W. M.; Zuber, P. Journal of Bacteriology, Vol. 179, Issue 21 https://doi.org/10.1128/jb.179.21.6778-6787.1997	journal	November 1997
The promoter for a sporulation gene in the spoIVC locus of Bacillus subtilis and its use in studies of temporal and spatial control of gene expression. Kunkel, B.; Sandman, K.; Panzer, S. Journal of Bacteriology, Vol. 170, Issue 8 https://doi.org/10.1128/jb.170.8.3513-3522.1988	journal	August 1988
Complete nucleotide sequence of a skin element excised by DNA rearrangement during sporulation in Bacillus subtilis Takemaru, K. -i.; Mizuno, M.; Sato, T. Microbiology, Vol. 141, Issue 2 https://doi.org/10.1099/13500872-141-2-323	journal	February 1995
Northern, Morphological, and Fermentation Analysis of spo0A Inactivation and Overexpression in Clostridium acetobutylicum ATCC 824 Harris, L. M.; Welker, N. E.; Papoutsakis, E. T. Journal of Bacteriology, Vol. 184, Issue 13 https://doi.org/10.1128/JB.184.13.3586-3597.2002	journal	July 2002
Efficient sporulation in Clostridium difficile requires disruption of the σK gene: Gene disruption essential for sporulation Haraldsen, Jeralyn D.; Sonenshein, Abraham L. Molecular Microbiology, Vol. 48, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03471.x	journal	April 2003
Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis. Kenney, T. J.; York, K.; Youngman, P. Proceedings of the National Academy of Sciences, Vol. 86, Issue 23 https://doi.org/10.1073/pnas.86.23.9109	journal	December 1989
The Forespore Line of Gene Expression in Bacillus subtilis Wang, Stephanie T.; Setlow, Barbara; Conlon, Erin M. Journal of Molecular Biology, Vol. 358, Issue 1 https://doi.org/10.1016/j.jmb.2006.01.059	journal	April 2006
Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor. Weir, J.; Predich, M.; Dubnau, E. Journal of Bacteriology, Vol. 173, Issue 2 https://doi.org/10.1128/jb.173.2.521-529.1991	journal	January 1991
Alternative Sigma Factors SigF, SigE, and SigG Are Essential for Sporulation in Clostridium botulinum ATCC 3502 Kirk, David G.; Zhang, Zhen; Korkeala, Hannu Applied and Environmental Microbiology, Vol. 80, Issue 16 https://doi.org/10.1128/AEM.01015-14	journal	June 2014
Expression of spoIIIJ in the Prespore Is Sufficient for Activation of G and for Sporulation in Bacillus subtilis Serrano, M.; Corte, L.; Opdyke, J. Journal of Bacteriology, Vol. 185, Issue 13 https://doi.org/10.1128/JB.185.13.3905-3917.2003	journal	July 2003
Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Errington, J. Microbiological Reviews, Vol. 57, Issue 1 https://doi.org/10.1128/MMBR.57.1.1-33.1993	journal	January 1993
Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes Sebaihia, M.; Peck, M. W.; Minton, N. P. Genome Research, Vol. 17, Issue 7 https://doi.org/10.1101/gr.6282807	journal	June 2007
Transcriptional organization of the Clostridium acetobutylicum genome Paredes, C. J. Nucleic Acids Research, Vol. 32, Issue 6 https://doi.org/10.1093/nar/gkh509	journal	March 2004
Sporulation of Bacillus subtilis Piggot, Patrick J.; Hilbert, David W. Current Opinion in Microbiology, Vol. 7, Issue 6 https://doi.org/10.1016/j.mib.2004.10.001	journal	December 2004
Inactivation of E and G in Clostridium acetobutylicum Illuminates Their Roles in Clostridial-Cell-Form Biogenesis, Granulose Synthesis, Solventogenesis, and Spore Morphogenesis Tracy, B. P.; Jones, S. W.; Papoutsakis, E. T. Journal of Bacteriology, Vol. 193, Issue 6 https://doi.org/10.1128/JB.01380-10	journal	January 2011
Genetic Networks Controlling the Initiation of Sporulation and the Development of Genetic Competence in Bacillus subtilis Grossman, Alan D. Annual Review of Genetics, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.ge.29.120195.002401	journal	December 1995
The mechanism of cell differentiation in Bacillus subtilis Iber, Dagmar; Clarkson, Joanna; Yudkin, Michael D. Nature, Vol. 441, Issue 7091 https://doi.org/10.1038/nature04666	journal	May 2006
Development and Application of Flow-Cytometric Techniques for Analyzing and Sorting Endospore-Forming Clostridia Tracy, B. P.; Gaida, S. M.; Papoutsakis, E. T. Applied and Environmental Microbiology, Vol. 74, Issue 24 https://doi.org/10.1128/AEM.01626-08	journal	October 2008
SpoIIE governs the phosphorylation state of a protein regulating transcription factor sigma F during sporulation in Bacillus subtilis. Arigoni, F.; Duncan, L.; Alper, S. Proceedings of the National Academy of Sciences, Vol. 93, Issue 8 https://doi.org/10.1073/pnas.93.8.3238	journal	April 1996
The sigma factors of Bacillus subtilis. Haldenwang, W. G. Microbiological reviews, Vol. 59, Issue 1 https://doi.org/10.1128/MMBR.59.1.1-30.1995	journal	January 1995
The genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 reside on a large plasmid whose loss leads to degeneration of the strain. Cornillot, E.; Nair, R. V.; Papoutsakis, E. T. Journal of Bacteriology, Vol. 179, Issue 17 https://doi.org/10.1128/jb.179.17.5442-5447.1997	journal	September 1997
Identification of a new sigma-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. Sun, D. X.; Stragier, P.; Setlow, P. Genes & Development, Vol. 3, Issue 2 https://doi.org/10.1101/gad.3.2.141	journal	February 1989
Analysis of a suppressor mutation ssb (kinC) of sur0B20 (spo0A) mutation in Bacillus subtilis reveals that kinC encodes a histidine protein kinase. Kobayashi, K.; Shoji, K.; Shimizu, T. Journal of Bacteriology, Vol. 177, Issue 1 https://doi.org/10.1128/jb.177.1.176-182.1995	journal	January 1995
Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis Perego, M.; Spiegelman, G. B.; Hoch, J. A. Molecular Microbiology, Vol. 2, Issue 6 https://doi.org/10.1111/j.1365-2958.1988.tb00079.x	journal	November 1988
rpoD operon promoter used by sigma H-RNA polymerase in Bacillus subtilis. Carter, H. L.; Wang, L. F.; Doi, R. H. Journal of Bacteriology, Vol. 170, Issue 4 https://doi.org/10.1128/jb.170.4.1617-1621.1988	journal	April 1988
Cloning, nucleotide sequencing, and expression of the Clostridium perfringens enterotoxin gene in Escherichia coli. Czeczulin, J. R.; Hanna, P. C.; McClane, B. A. Infection and Immunity, Vol. 61, Issue 8 https://doi.org/10.1128/IAI.61.8.3429-3439.1993	journal	January 1993
The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Kunkel, B.; Losick, R.; Stragier, P. Genes & Development, Vol. 4, Issue 4 https://doi.org/10.1101/gad.4.4.525	journal	April 1990
Features of Pro- K Important for Cleavage by SpoIVFB, an Intramembrane Metalloprotease Zhou, R.; Chen, K.; Xiang, X. Journal of Bacteriology, Vol. 195, Issue 12 https://doi.org/10.1128/JB.00229-13	journal	April 2013
Genetic regulation of morphogenesis in Bacillus subtilis: roles of sigma E and sigma F in prespore engulfment. Illing, N.; Errington, J. Journal of Bacteriology, Vol. 173, Issue 10 https://doi.org/10.1128/jb.173.10.3159-3169.1991	journal	May 1991
SpoIIE Is Necessary for Asymmetric Division, Sporulation, and Expression of F, E, and G but Does Not Control Solvent Production in Clostridium acetobutylicum ATCC 824 Bi, C.; Jones, S. W.; Hess, D. R. Journal of Bacteriology, Vol. 193, Issue 19 https://doi.org/10.1128/JB.05474-11	journal	July 2011
Inactivation of F in Clostridium acetobutylicum ATCC 824 Blocks Sporulation Prior to Asymmetric Division and Abolishes E and G Protein Expression but Does Not Block Solvent Formation Jones, S. W.; Tracy, B. P.; Gaida, S. M. Journal of Bacteriology, Vol. 193, Issue 10 https://doi.org/10.1128/JB.00088-11	journal	March 2011
Targeted gene disruption by use of a group II intron (targetron) vector in Clostridium acetobutylicum Shao, Lijun; Hu, Shiyuan; Yang, Yi Cell Research, Vol. 17, Issue 11 https://doi.org/10.1038/cr.2007.91	journal	November 2007
The Biocide Chlorine Dioxide Stimulates Biofilm Formation in Bacillus subtilis by Activation of the Histidine Kinase KinC Shemesh, M.; Kolter, R.; Losick, R. Journal of Bacteriology, Vol. 192, Issue 24 https://doi.org/10.1128/JB.01025-10	journal	October 2010
Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis. Karmazyn-Campelli, C.; Bonamy, C.; Savelli, B. Genes & Development, Vol. 3, Issue 2 https://doi.org/10.1101/gad.3.2.150	journal	February 1989
Sporulation protein SpoIVFB from Bacillus subtilis enhances processing of the sigma factor precursor Pro-sigma K in the absence of other sporulation gene products. Lu, S.; Cutting, S.; Kroos, L. Journal of Bacteriology, Vol. 177, Issue 4 https://doi.org/10.1128/jb.177.4.1082-1085.1995	journal	February 1995
Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis. Karow, M. L.; Glaser, P.; Piggot, P. J. Proceedings of the National Academy of Sciences, Vol. 92, Issue 6 https://doi.org/10.1073/pnas.92.6.2012	journal	March 1995
The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome Sebaihia, Mohammed; Wren, Brendan W.; Mullany, Peter Nature Genetics, Vol. 38, Issue 7 https://doi.org/10.1038/ng1830	journal	June 2006
A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia: Genomics update Yutin, Natalya; Galperin, Michael Y. Environmental Microbiology https://doi.org/10.1111/1462-2920.12173	journal	July 2013
Gut Microbiota in Health and Disease Sekirov, Inna; Russell, Shannon L.; Antunes, L. Caetano M. Physiological Reviews, Vol. 90, Issue 3 https://doi.org/10.1152/physrev.00045.2009	journal	July 2010
The biosynthesis of granulose by Clostridium pasteurianum Robson, R. L.; Robson, R. M.; Morris, J. G. Biochemical Journal, Vol. 144, Issue 3 https://doi.org/10.1042/bj1440503	journal	December 1974
Activation of Cell-Specific Transcription by a Serine Phosphatase at the Site of Asymmetric Division Duncan, L.; Alper, S.; Arigoni, F. Science, Vol. 270, Issue 5236 https://doi.org/10.1126/science.270.5236.641	journal	October 1995
Recent progress in Bacillus subtilis sporulation Higgins, Douglas; Dworkin, Jonathan FEMS Microbiology Reviews, Vol. 36, Issue 1 https://doi.org/10.1111/j.1574-6976.2011.00310.x	journal	January 2012
Direct Analysis of Genes Encoding 16S rRNA from Complex Communities Reveals Many Novel Molecular Species within the Human Gut Suau, Antonia; Bonnet, Régis; Sutren, Malène Applied and Environmental Microbiology, Vol. 65, Issue 11 https://doi.org/10.1128/AEM.65.11.4799-4807.1999	journal	November 1999
Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum Worner, Kristina; Szurmant, Hendrik; Chiang, Christina Molecular Microbiology, Vol. 59, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.04988.x	journal	February 2006
AbrB and Spo0E Control the Proper Timing of Sporulation in Bacillus subtilis Shafikhani, Sasha H.; Leighton, Terrance Current Microbiology, Vol. 48, Issue 4 https://doi.org/10.1007/s00284-003-4186-2	journal	April 2004
Regulation of endospore formation in Bacillus subtilis Errington, Jeff Nature Reviews Microbiology, Vol. 1, Issue 2 https://doi.org/10.1038/nrmicro750	journal	November 2003
The Spore Differentiation Pathway in the Enteric Pathogen Clostridium difficile Pereira, Fátima C.; Saujet, Laure; Tomé, Ana R. PLoS Genetics, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pgen.1003782	journal	October 2013
Global Analysis of the Sporulation Pathway of Clostridium difficile Fimlaid, Kelly A.; Bond, Jeffrey P.; Schutz, Kristin C. PLoS Genetics, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pgen.1003660	journal	August 2013
Compartmentalized expression of a gene under the control of sporulation transcription factor sigma E in Bacillus subtilis. Driks, A.; Losick, R. Proceedings of the National Academy of Sciences, Vol. 88, Issue 22 https://doi.org/10.1073/pnas.88.22.9934	journal	November 1991
The SpoIIE phosphatase, the sporulation septum and the establishment of forespore-specific transcription in Bacillus subtilis: a reassessment Arigoni, Fabrizio; Guerout-Fleury, Anne-Marie; Barak, Imrich Molecular Microbiology, Vol. 31, Issue 5 https://doi.org/10.1046/j.1365-2958.1999.01282.x	journal	March 1999
Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. Perego, M.; Cole, S. P.; Burbulys, D. Journal of Bacteriology, Vol. 171, Issue 11 https://doi.org/10.1128/jb.171.11.6187-6196.1989	journal	November 1989
The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age Mariat, D.; Firmesse, O.; Levenez, F. BMC Microbiology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2180-9-123	journal	January 2009
The Spo0A regulon of Bacillus subtilis: The Spo0A regulon Molle, Virginie; Fujita, Masaya; Jensen, Shane T. Molecular Microbiology, Vol. 50, Issue 5 https://doi.org/10.1046/j.1365-2958.2003.03818.x	journal	November 2003
A forespore checkpoint for mother cell gene expression during development in B. subtilis Cutting, Simon; Oke, Valerie; Driks, Adam Cell, Vol. 62, Issue 2 https://doi.org/10.1016/0092-8674(90)90362-I	journal	July 1990
Solvent Production and Morphological Changes in Clostridium acetobutylicum Jones, D. T.; van der Westhuizen, A.; Long, S. Applied and Environmental Microbiology, Vol. 43, Issue 6 https://doi.org/10.1128/AEM.43.6.1434-1439.1982	journal	January 1982
Binding of Spo0A stimulates spoIIG promoter activity in Bacillus subtilis. Satola, S. W.; Baldus, J. M.; Moran, C. P. Journal of Bacteriology, Vol. 174, Issue 5 https://doi.org/10.1128/jb.174.5.1448-1453.1992	journal	March 1992
The sigma factors of Bacillus subtilis Haldenwang, W. G. Microbiological Reviews, Vol. 59, Issue 1 https://doi.org/10.1128/mr.59.1.1-30.1995	journal	March 1995
Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis Errington, J. Microbiological Reviews, Vol. 57, Issue 1 https://doi.org/10.1128/mr.57.1.1-33.1993	journal	March 1993
RNA Polymerase and Alternative σ Factors Duerre, Peter Handbook on Clostridia https://doi.org/10.1201/9780203489819-37	book	March 2005
The genome sequence of Clostridium tetani, the causative agent of tetanus disease Brüggemann, Holger; Baumer, Sebastian; Fricke, Wolfgang Florian Universität Regensburg https://doi.org/10.5283/epub.10903	text	January 2003
Sporulation in Clostridia (Genetics) Duerre, Peter Handbook on Clostridia https://doi.org/10.1201/9780203489819-41	book	March 2005

Cited By (23)

Capturing One of the Human Gut Microbiome’s Most Wanted: Reconstructing the Genome of a Novel Butyrate-Producing, Clostridial Scavenger from Metagenomic Sequence Data Jeraldo, Patricio; Hernandez, Alvaro; Nielsen, Henrik B. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00783	journal	May 2016
RNAseq-based transcriptome assembly of Clostridium acetobutylicum for functional genome annotation and discovery Ralston, Matthew T.; Papoutsakis, Eleftherios T. AIChE Journal, Vol. 64, Issue 12 https://doi.org/10.1002/aic.16396	journal	October 2018
Microbial solvent formation revisited by comparative genome analysis Poehlein, Anja; Solano, José David Montoya; Flitsch, Stefanie K. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0742-z	journal	March 2017
Effect of fermentation system on the physicochemical and microbial community dynamics during enset ( Ensete ventricosum ) fermentation Andeta, A. F.; Vandeweyer, D.; Teffera, E. F. Journal of Applied Microbiology, Vol. 126, Issue 3 https://doi.org/10.1111/jam.14173	journal	January 2019
Whole-genome sequence of an evolved Clostridium pasteurianum strain reveals Spo0A deficiency responsible for increased butanol production and superior growth Sandoval, Nicholas R.; Venkataramanan, Keerthi P.; Groth, Theodore S. Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0408-7	journal	December 2015
Genomics of Clostridium taeniosporum, an organism which forms endospores with ribbon-like appendages Cambridge, Joshua M.; Blinkova, Alexandra L.; Salvador Rocha, Erick I. PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0189673	journal	January 2018
A Strongly Fluorescing Anaerobic Reporter and Protein-Tagging System for Clostridium Organisms Based on the Fluorescence-Activating and Absorption-Shifting Tag Protein (FAST) Streett, Hannah E.; Kalis, Katie M.; Papoutsakis, Eleftherios T. Applied and Environmental Microbiology, Vol. 85, Issue 14 https://doi.org/10.1128/aem.00622-19	journal	May 2019
The industrial anaerobe Clostridium acetobutylicum uses polyketides to regulate cellular differentiation Herman, Nicolaus A.; Kim, Seong Jong; Li, Jeffrey S. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01809-5	journal	November 2017
The characteristics of Clostridium difficile ST81, a new PCR ribotype of toxin A- B+ strain with high-level fluoroquinolones resistance and higher sporulation ability than ST37/PCR ribotype 017 Wang, Baoya; Peng, Wenwen; Zhang, Pingping FEMS Microbiology Letters, Vol. 365, Issue 17 https://doi.org/10.1093/femsle/fny168	journal	July 2018
Differential requirements for conserved peptidoglycan remodeling enzymes during Clostridioides difficile spore formation: Regulation of Clostridium difficile Engulfment Ribis, John W.; Fimlaid, Kelly A.; Shen, Aimee Molecular Microbiology, Vol. 110, Issue 3 https://doi.org/10.1111/mmi.14090	journal	October 2018
Transcription profiling of butanol producer Clostridium beijerinckii NRRL B-598 using RNA-Seq Sedlar, Karel; Koscova, Pavlina; Vasylkivska, Maryna BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4805-8	journal	May 2018
Clostridium butyricum maximizes growth while minimizing enzyme usage and ATP production: metabolic flux distribution of a strain cultured in glycerol Serrano-Bermúdez, Luis Miguel; González Barrios, Andrés Fernando; Maranas, Costas D. BMC Systems Biology, Vol. 11, Issue 1 https://doi.org/10.1186/s12918-017-0434-0	journal	June 2017
Optimization of alkaline protease production by rational deletion of sporulation related genes in Bacillus licheniformis Zhou, Cuixia; Zhou, Huiying; Zhang, Huitu Microbial Cell Factories, Vol. 18, Issue 1 https://doi.org/10.1186/s12934-019-1174-1	journal	July 2019
Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes Davidson, Philip; Eutsey, Rory; Redler, Brendan PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007470	journal	September 2018
Characterization of Clostridium novyi isolated from a sow in a sudden death case in Korea Kim, Won-II; Jeong, Chang-Gi; Seo, Byoung-Joo Research Square [preprints] https://doi.org/10.21203/rs.2.21648/v1	posted_content	May 2020
Linking Microbial Community Structure and Function During the Acidified Anaerobic Digestion of Grass Joyce, Aoife; Ijaz, Umer Z.; Nzeteu, Corine Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00540	journal	March 2018
Comparison of expression of key sporulation, solventogenic and acetogenic genes in C. beijerinckii NRRL B-598 and its mutant strain overexpressing spo0A Kolek, J.; Diallo, M.; Vasylkivska, M. Applied Microbiology and Biotechnology, Vol. 101, Issue 22 https://doi.org/10.1007/s00253-017-8555-3	journal	October 2017
Acidogenesis, solventogenesis, metabolic stress response and life cycle changes in Clostridium beijerinckii NRRL B-598 at the transcriptomic level Patakova, Petra; Branska, Barbora; Sedlar, Karel Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37679-0	journal	February 2019
Comparative genomics identifies potential virulence factors in Clostridium tertium and C. paraputrificum Muñoz, Marina; Restrepo-Montoya, Daniel; Kumar, Nitin Virulence, Vol. 10, Issue 1 https://doi.org/10.1080/21505594.2019.1637699	journal	January 2019
System-level modeling of acetone–butanol–ethanol fermentation Liao, Chen; Seo, Seung-Oh; Lu, Ting FEMS Microbiology Letters, Vol. 363, Issue 9 https://doi.org/10.1093/femsle/fnw074	journal	March 2016
Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes Davidson, Phillip; Eutsey, Rory; Redler, Brendan Carnegie Mellon University https://doi.org/10.1184/r1/7264163.v1	text	January 2018
Characterization of Clostridium novyi isolated from a sow in a sudden death case in Korea Jeong, Chang-Gi; Seo, Byoung-Joo; Nazki, Salik Research Square [preprints] https://doi.org/10.21203/rs.2.21648/v2	posted_content	May 2020
Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes Davidson, Phillip; Eutsey, Rory; Redler, Brendan Carnegie Mellon University https://doi.org/10.1184/r1/7264163	text	January 2018

Similar Records

Steam explosion pretreatment coupling high-temperature short-time sterilization facilitating cellulose degradation and sporulation-regulatory gene expression in high-solid fermentation

Journal Article · Sat Jan 28 00:00:00 EST 2023 · International Journal of Biological Macromolecules · OSTI ID:1454688

Li, Chonglei; Du, Xiaoyu; Liu, Zhi-Hua; +5 more

Phosphorylation of the Bacillus subtilis Replication Controller YabA Plays a Role in Regulation of Sporulation and Biofilm Formation

Journal Article · Wed Mar 21 00:00:00 EDT 2018 · Frontiers in Microbiology · OSTI ID:1454688

García García, Tránsito; Ventroux, Magali; Derouiche, Abderahmane; +6 more

Sporulation Phosporelay Proteins And Their Complexes: Crystallographic Characterization

Journal Article · Thu Jun 04 00:00:00 EDT 2009 · Methods Enzymol 422:102,2007 · OSTI ID:1454688

Varughese, K I; Zhao, H; Veldore, V H; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Citation Formats

References (116)

Cited By (23)

Similar Records

Related Subjects