A comparative genomic view of clostridial sporulation and physiology

Clostridia are anaerobic, endospore-forming prokaryotes that include strains of importance to human and animal health and physiology, cellulose degradation, solvent production and bioremediation. Their differentiation and related developmental programmes are not well understood at the molecular level. Recent genome sequencing and transcriptional-profiling studies have offered a glimpse of their inner workings and indicate that a better understanding of the orchestration of the molecular events that underlie their unique physiology, capabilities and diversity will pay major dividends.

[1]  I. Mandic-Mulec,et al.  Copyright � 1995, American Society for Microbiology The Bacillus subtilis SinR Protein Is a Repressor of , 1995 .

[2]  Yuh Nung Jan,et al.  Asymmetric cell division , 1998, Nature.

[3]  Robert D. Finn,et al.  The Pfam protein families database , 2004, Nucleic Acids Res..

[4]  J. Engasser,et al.  The role of acids on the production of acetone and butanol by Clostridium acetobutylicum , 1985, Applied Microbiology and Biotechnology.

[5]  M. Mavrovouniotis.  Group contributions for estimating standard gibbs energies of formation of biochemical compounds in aqueous solution , 1990, Biotechnology and bioengineering.

[6]  R. Losick,et al.  Bacillus subtilis and Its Closest Relatives , 2002 .

[7]  R. Portalier,et al.  Involvement of Carbon Source and Acetyl Phosphate in the External-pH-Dependent Expression of Porin Genes inEscherichia coli , 2000, Journal of bacteriology.

[8]  G. Gottschalk,et al.  The internal pH of Clostridium acetobutylicum and its effect on the shift from acid to solvent formation , 1985, Archives of Microbiology.

[9]  Rainer Merkl,et al.  The genome sequence of Clostridium tetani, the causative agent of tetanus disease , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Eleftherios T. Papoutsakis,et al.  DNA Array-Based Transcriptional Analysis of Asporogenous, Nonsolventogenic Clostridium acetobutylicum Strains SKO1 and M5 , 2003, Journal of bacteriology.

[11]  H. Bahl,et al.  Expression of heat shock genes in Clostridium acetobutylicum. , 1995, FEMS microbiology reviews.

[12]  M. Hecker,et al.  Regulation and Function of Heat‐lnducible Genes in Bacillus subtilis , 2002 .

[13]  Shane T. Jensen,et al.  The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. , 2003, Journal of molecular biology.

[14]  Hanno Steen,et al.  Proteomics goes quantitative: measuring protein abundance. , 2002, Trends in biotechnology.

[15]  J. Wiegel,et al.  Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes) , 2004, Archives of Microbiology.

[16]  Eleftherios T. Papoutsakis,et al.  Northern, Morphological, and Fermentation Analysis of spo0A Inactivation and Overexpression in Clostridium acetobutylicum ATCC 824 , 2002, Journal of bacteriology.

[17]  J. Stock,et al.  Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Cecil W. Forsberg,et al.  Influence of External pH and Fermentation Products on Clostridium acetobutylicum Intracellular pH and Cellular Distribution of Fermentation Products , 1986, Applied and environmental microbiology.

[19]  J. Hoch,et al.  Evolution of signalling in the sporulation phosphorelay , 2002, Molecular microbiology.

[20]  G. Bennett,et al.  Isolation and Characterization of Mutants of Clostridium acetobutylicum ATCC 824 Deficient in Acetoacetyl-Coenzyme A:Acetate/Butyrate:Coenzyme A-Transferase (EC 2.8.3.9) and in Other Solvent Pathway Enzymes , 1989, Applied and environmental microbiology.

[21]  P. Stragier.  A Gene Odyssey: Exploring the Genomes of Endospore-Forming Bacteria , 2002 .

[22]  C. Tomas,et al.  Overexpression of groESL in Clostridium acetobutylicum Results in Increased Solvent Production and Tolerance, Prolonged Metabolism, and Changes in the Cell's Transcriptional Program , 2003, Applied and Environmental Microbiology.

[23]  N. Sugimoto,et al.  Rapid, simplified method for production and purification of tetanus toxin , 1985, Applied and environmental microbiology.

[24]  E Terry Papoutsakis,et al.  Transcriptional organization of the Clostridium acetobutylicum genome. , 2004, Nucleic acids research.

[25]  R. Losick,et al.  Asymmetric Cell Division in B. subtilis Involves a Spiral-like Intermediate of the Cytokinetic Protein FtsZ , 2002, Cell.

[26]  H. A. George,et al.  Acidic Conditions Are Not Obligatory for Onset of Butanol Formation by Clostridium beijerinckii (Synonym, C. butylicum) , 1983, Applied and environmental microbiology.

[27]  D. Hilbert,et al.  Sporulation of Bacillus subtilis. , 2004, Current opinion in microbiology.

[28]  J. Hoch.  Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. , 1993, Annual review of microbiology.

[29]  Sporulation and time course expression of sigma-factor homologous genes in Clostridium acetobutylicum. , 1998, FEMS microbiology letters.

[30]  J. Hoch,et al.  Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway , 1993, Molecular microbiology.

[31]  U. Völker,et al.  Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis. , 2005, Microbiology.

[32]  E. Papoutsakis,et al.  Transcriptional Analysis of spo0A Overexpression in Clostridium acetobutylicum and Its Effect on the Cell's Response to Butanol Stress , 2004, Journal of bacteriology.

[33]  J. Hoch,et al.  Transition‐state regulators: sentinels of Bacillus subtilis post‐exponential gene expression , 1993, Molecular microbiology.

[34]  E. Rapaport,et al.  Stress- and Growth Phase-Associated Proteins of Clostridium acetobutylicum , 1988, Applied and environmental microbiology.

[35]  E. Papoutsakis,et al.  Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. , 1996, Microbiology.

[36]  E. Papoutsakis,et al.  Analysis of Degenerate Variants ofClostridium acetobutylicumATCC 824: BIOTECHNOLOGY/FOOD MICROBIOLOGY , 1996 .

[37]  Host-plasmid interactions in recombinant strains of Clostridium acetobutylicum ATCC 824 , 1994 .

[38]  G. Bennett,et al.  Cloning, Sequencing, and Characterization of the Gene Encoding Flagellin, flaC, and the Post-translational Modification of Flagellin, FlaC, from Clostridium acetobutylicum ATCC824 , 2000 .

[39]  N. A. Gutierrez,et al.  Isolation and partial characterization of a non-motile mutant ofClostridium acetobutylicum , 1990, Biotechnology Letters.

[40]  R. Losick,et al.  Developmental Commitment in a Bacterium , 2005, Cell.

[41]  A. Sonenshein,et al.  Efficient sporulation in Clostridium difficile requires disruption of the σK gene , 2003, Molecular microbiology.

[42]  H. Hayashi,et al.  The luxS gene is involved in cell–cell signalling for toxin production in Clostridium perfringens , 2002, Molecular microbiology.

[43]  in chief George M. Garrity.  Bergey’s Manual® of Systematic Bacteriology , 1989, Springer New York.

[44]  D R Woods,et al.  The genetic engineering of microbial solvent production. , 1995, Trends in biotechnology.

[45]  H. Flint,et al.  The microbiology of butyrate formation in the human colon. , 2002, FEMS microbiology letters.

[46]  I. Zhulin,et al.  Chemotaxis and Motility , 2002 .

[47]  P. Lawson,et al.  The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. , 1994, International journal of systematic bacteriology.

[48]  E. Papoutsakis,et al.  Solventogenesis in Clostridium acetobutylicum fermentations related to carboxylic acid and proton concentrations , 1988, Biotechnology and bioengineering.

[49]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[50]  G. Gottschalk,et al.  Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani. , 2004, Anaerobe.

[51]  A. Grossman,et al.  Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis , 1995, Journal of bacteriology.

[52]  R. Losick,et al.  Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis , 1987, Journal of bacteriology.

[53]  R. Z. Vêncio,et al.  DNA microarrays for comparative genomics and analysis of gene expression in Trypanosoma cruzi. , 2004, Molecular and biochemical parasitology.

[54]  D. Hilbert,et al.  Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation , 2004, Microbiology and Molecular Biology Reviews.

[55]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[56]  M. Young,et al.  Molecular genetics and the initiation of solventogenesis in Clostridium beijerinckii (formerly Clostridium acetobutylicum) NCIMB 8052. , 1995, FEMS microbiology reviews.

[57]  L. Márquez-Magaña,et al.  Dual Promoters Are Responsible for Transcription Initiation of the fla/che Operon in Bacillus subtilis , 1998, Journal of bacteriology.

[58]  P. Dürre,et al.  Initiation of endospore formation in Clostridium acetobutylicum. , 2004, Anaerobe.

[59]  Shane T. Jensen,et al.  The Spo0A regulon of Bacillus subtilis , 2003, Molecular microbiology.

[60]  M. Hattori,et al.  Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Victoria A. Feher,et al.  Two-Component Signal Transduction in Bacillus subtilis: How One Organism Sees Its World , 1999, Journal of bacteriology.

[62]  E. Papoutsakis,et al.  Increased levels of ATP and NADH are associated with increased solvent production in continuous cultures of Clostridium acetobutylicum , 1989, Applied Microbiology and Biotechnology.

[63]  P. Youngman,et al.  Spo0A directly controls the switch from acid to solvent production in solvent‐forming clostridia , 2000, Molecular microbiology.

[64]  E. Papoutsakis,et al.  Characterization of recombinant strains of the Clostridium acetobutylicum butyrate kinase inactivation mutant: need for new phenomenological models for solventogenesis and butanol inhibition? , 2000, Biotechnology and bioengineering.

[65]  M. Mavrovouniotis.  Estimation of standard Gibbs energy changes of biotransformations. , 1991, The Journal of biological chemistry.

[66]  J. Errington.  Regulation of endospore formation in Bacillus subtilis , 2003, Nature Reviews Microbiology.

[67]  J Schultz,et al.  SMART, a simple modular architecture research tool: identification of signaling domains. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[68]  R. Lewis,et al.  Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon. , 2005, FEMS microbiology reviews.

[69]  Shane T. Jensen,et al.  The Program of Gene Transcription for a Single Differentiating Cell Type during Sporulation in Bacillus subtilis , 2004, PLoS biology.

[70]  I. Smith,et al.  Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor , 1991, Journal of bacteriology.

[71]  M. Smeltzer,et al.  Comparative Genomics of Staphylococcus aureus Musculoskeletal Isolates , 2005, Journal of bacteriology.

[72]  A. Ninfa,et al.  Is acetyl phosphate a global signal in Escherichia coli? , 1993, Journal of bacteriology.

[73]  Alan J Wolfe,et al.  Evidence that acetyl phosphate functions as a global signal during biofilm development , 2003, Molecular microbiology.

[74]  N. Fairweather,et al.  Revised nomenclature of Clostridium difficile toxins and associated genes. , 2005, Journal of medical microbiology.

[75]  J. Rood.  Virulence genes of Clostridium perfringens. , 1998, Annual review of microbiology.

[76]  J. Hoch,et al.  Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis , 2000, Molecular microbiology.

[77]  Eva R. Kashket,et al.  Intracellular Conditions Required for Initiation of Solvent Production by Clostridium acetobutylicum , 1986, Applied and environmental microbiology.

[78]  T. Nyström.  The glucose‐starvation stimulon of Escherichia coli: induced and repressed synthesis of enzymes of central metabolic pathways and role of acetyl phosphate in gene expression and starvation survival , 1994, Molecular microbiology.

[79]  E. Papoutsakis,et al.  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 , 1997, Journal of bacteriology.

[80]  R. Losick,et al.  Identification and characterization of sporulation gene spoVS from Bacillus subtilis , 1995, Journal of bacteriology.

[81]  David T. Jones,et al.  Initiation of solvent production, clostridial stage and endospore formation in Clostridium acetobutylicum P262 , 1984, Applied Microbiology and Biotechnology.

[82]  Patrick Eichenberger,et al.  Genome-Wide Analysis of the Stationary-Phase Sigma Factor (Sigma-H) Regulon of Bacillus subtilis , 2002, Journal of bacteriology.

[83]  P Youngman,et al.  Spo0A controls the sigma A-dependent activation of Bacillus subtilis sporulation-specific transcription unit spoIIE , 1992, Journal of bacteriology.

[84]  R. Losick,et al.  Sporulation Genes and Intercompartmental Regulation , 2002 .

[85]  John R Yates,et al.  Large-scale protein identification using mass spectrometry. , 2003, Biochimica et biophysica acta.

[86]  A. Wolfe,et al.  Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli , 1994, Molecular microbiology.

[87]  George N. Bennett,et al.  Intracellular Butyryl Phosphate and Acetyl Phosphate Concentrations in Clostridium acetobutylicum and Their Implications for Solvent Formation , 2005, Applied and Environmental Microbiology.

[88]  J. Hoch,et al.  Identification of a membrane protein involved in activation of the KinB pathway to sporulation in Bacillus subtilis , 1996, Journal of bacteriology.

[89]  Philippe Soucaille,et al.  Regulation of solvent production in Clostridium acetobutylicum , 1998 .

[90]  J. Hoch,et al.  Two-Component Systems, Phosphorelays, and Regulation of Their Activities by Phosphatases , 2002 .

[91]  P. Dürre,et al.  Changes in protein synthesis and identification of proteins specifically induced during solventogenesis in Clostridium acetobutylicum , 2002, Electrophoresis.

[92]  A. Sonenshein,et al.  Control of sporulation initiation in Bacillus subtilis. , 2000, Current opinion in microbiology.

[93]  M. Sarker,et al.  Disruption of the gene (spo0A) encoding sporulation transcription factor blocks endospore formation and enterotoxin production in enterotoxigenic Clostridium perfringens type A. , 2004, FEMS microbiology letters.

[94]  L. Petit,et al.  Clostridium perfringens: toxinotype and genotype. , 1999, Trends in microbiology.

[95]  C. Tomas,et al.  Transcriptional Analysis of Butanol Stress and Tolerance in Clostridium acetobutylicum , 2004, Journal of bacteriology.

[96]  B. Dupuy,et al.  BotR/A and TetR are alternative RNA polymerase sigma factors controlling the expression of the neurotoxin and associated protein genes in Clostridium botulinum type A and Clostridium tetani , 2004, Molecular microbiology.

[97]  G. Bennett,et al.  Enzymatic characterization of a nonmotile, nonsolventogenicClostridium acetobutylicum ATCC 824 mutant , 1991, Current Microbiology.

[98]  H. Bahl,et al.  Induction of heat shock proteins during initiation of solvent formation inClostridium acetobutylicum , 1990, Applied Microbiology and Biotechnology.

[99]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[100]  D. T. Jones,et al.  Acetone-butanol fermentation revisited. , 1986, Microbiological reviews.

[101]  Ronald W. Davis,et al.  Replication dynamics of the yeast genome. , 2001, Science.

[102]  D. T. Jones,et al.  Solvent Production and Morphological Changes in Clostridium acetobutylicum , 1982, Applied and environmental microbiology.

[103]  Cathy H. Wu,et al.  InterPro, progress and status in 2005 , 2004, Nucleic Acids Res..

[104]  E. Papoutsakis,et al.  Effects of propionate and acetate additions on solvent production in batch cultures of Clostridium acetobutylicum , 1990, Applied and environmental microbiology.

[105]  A. Wolfe.  The Acetate Switch , 2005, Microbiology and Molecular Biology Reviews.

[106]  Peer Bork,et al.  SMART 4.0: towards genomic data integration , 2004, Nucleic Acids Res..

[107]  M. Scotcher,et al.  SpoIIE Regulates Sporulation but Does Not Directly Affect Solventogenesis in Clostridium acetobutylicum ATCC 824 , 2005, Journal of bacteriology.

[108]  S. Melville,et al.  The CcpA Protein Is Necessary for Efficient Sporulation and Enterotoxin Gene (cpe) Regulation in Clostridium perfringens , 2004, Journal of bacteriology.

[109]  M. Scotcher,et al.  Expression of abrB310 and sinR, and Effects of Decreased abrB310 Expression on the Transition from Acidogenesis to Solventogenesis, in Clostridium acetobutylicum ATCC 824 , 2005, Applied and Environmental Microbiology.

[110]  R. Losick,et al.  Chromosomal rearrangement generating a composite gene for a developmental transcription factor. , 1989, Science.

[111]  Differential induction of genes related to solvent formation during the shift from acidogenesis to solventogenesis in continuous culture of Clostridium acetobutylicum , 1995 .

[112]  Eleftherios T. Papoutsakis,et al.  Transcriptional Program of Early Sporulation and Stationary-Phase Events in Clostridium acetobutylicum , 2005, Journal of bacteriology.

[113]  U. Bai,et al.  SinI modulates the activity of SinR, a developmental switch protein of Bacillus subtilis, by protein-protein interaction. , 1993, Genes & development.

[114]  George N. Bennett,et al.  Genome Sequence and Comparative Analysis of the Solvent-Producing Bacterium Clostridium acetobutylicum , 2001, Journal of bacteriology.