Towards a comprehensive understanding of Bacillus subtilis cell physiology by physiological proteomics

Using Bacillus subtilis as a model system for functional genomics, this review will provide insights how proteomics can be used to bring the virtual life of genes to the real life of proteins. Physiological proteomics will generate a new and broad understanding of cellular physiology because the majority of proteins synthesized in the cell can be visualized. From a physiological point of view two major proteome fractions can be distinguished: proteomes of growing cells and proteomes of nongrowing cells. In the main analytical window almost 50% of the vegetative proteome expressed in growing cells of B. subtilis were identified. This proteomic view of growing cells can be employed for analyzing the regulation of entire metabolic pathways and thus opens the chance for a comprehensive understanding of metabolism and growth processes of bacteria. Proteomics, on the other hand, is also a useful tool for analyzing the adaptational network of nongrowing cells that consists of several partially overlapping regulation groups induced by stress/starvation stimuli. Furthermore, proteomic signatures for environmental stimuli can not only be applied to predict the physiological state of cells, but also offer various industrial applications from fermentation monitoring up to the analysis of the mode of action of drugs. Even if DNA array technologies currently provide a better overview of the gene expression profile than proteome approaches, the latter address biological problems in which they can not be replaced by mRNA profiling procedures. This proteomics of the second generation is a powerful tool for analyzing global control of protein stability, the protein interaction network, protein secretion or post‐translational modifications of proteins on the way towards the elucidation of the mystery of life.

[1]  Uwe Völker,et al.  A comprehensive proteome map of growing Bacillus subtilis cells , 2004, Proteomics.

[2]  Hiroyuki Kaji,et al.  Only a Small Subset of the Horizontally Transferred Chromosomal Genes in Escherichia coli Are Translated into Proteins*S , 2004, Molecular & Cellular Proteomics.

[3]  Nasreen S Jessani,et al.  Activity-based probes for the proteomic profiling of metalloproteases. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Errington,et al.  Coordination of Cell Division and Chromosome Segregation by a Nucleoid Occlusion Protein in Bacillus subtilis , 2004, Cell.

[5]  R. Aebersold,et al.  Absolute quantification of specific proteins in complex mixtures using visible isotope-coded affinity tags. , 2004, Analytical chemistry.

[6]  Oscar P. Kuipers,et al.  Proteomics of Protein Secretion by Bacillus subtilis: Separating the “Secrets” of the Secretome , 2004, Microbiology and Molecular Biology Reviews.

[7]  Michael Hecker,et al.  A proteomic view of cell physiology of Bacillus licheniformis , 2004, Proteomics.

[8]  P. Bork Sequences and topology: Genes and structures in context , 2004 .

[9]  S. Engelmann,et al.  Oxidative stress triggers thiol oxidation in the glyceraldehyde‐3‐phosphate dehydrogenase of Staphylococcus aureus , 2004, Molecular microbiology.

[10]  J. Helmann,et al.  The Bacillus subtilis Extracytoplasmic-Function σX Factor Regulates Modification of the Cell Envelope and Resistance to Cationic Antimicrobial Peptides , 2004, Journal of bacteriology.

[11]  K. Ziegelbauer,et al.  New Class of Bacterial Phenylalanyl-tRNA Synthetase Inhibitors with High Potency and Broad-Spectrum Activity , 2004, Antimicrobial Agents and Chemotherapy.

[12]  M. Hecker,et al.  Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. , 2004, Microbiology.

[13]  M. Hecker,et al.  MurAA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp‐dependent proteolysis in Bacillus subtilis , 2004, Molecular microbiology.

[14]  Nasreen S Jessani,et al.  The development and application of methods for activity-based protein profiling. , 2004, Current opinion in chemical biology.

[15]  Folker Meyer,et al.  Comparing expression level‐dependent features in codon usage with protein abundance: An analysis of ‘predictive proteomics’ , 2004, Proteomics.

[16]  Jacob D. Jaffe,et al.  Proteogenomic mapping as a complementary method to perform genome annotation , 2004, Proteomics.

[17]  P. Bork,et al.  Genome evolution reveals biochemical networks and functional modules , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Tao Wang,et al.  Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon , 2003, Molecular microbiology.

[19]  J. Collado-Vides,et al.  Identifying global regulators in transcriptional regulatory networks in bacteria. , 2003, Current opinion in microbiology.

[20]  U. Völker,et al.  Chill Induction of the SigB-Dependent General Stress Response in Bacillus subtilis and Its Contribution to Low-Temperature Adaptation , 2003, Journal of bacteriology.

[21]  S. Séror,et al.  Mass spectrometry and site-directed mutagenesis identify several autophosphorylated residues required for the activity of PrkC, a Ser/Thr kinase from Bacillus subtilis. , 2003, Journal of molecular biology.

[22]  M. Hecker,et al.  Patterns of protein carbonylation following oxidative stress in wild-type and sigB Bacillus subtilis cells , 2003, Molecular Genetics and Genomics.

[23]  J. Bernhardt,et al.  Using standard positions and image fusion to create proteome maps from collections of two‐dimensional gel electrophoresis images , 2003, Proteomics.

[24]  M. Hecker,et al.  The extracellular proteome of Bacillus subtilis under secretion stress conditions , 2003, Molecular microbiology.

[25]  S. Ehrlich,et al.  Essential Bacillus subtilis genes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[26]  U. Jenal,et al.  Regulation by proteolysis in bacterial cells. , 2003, Current opinion in microbiology.

[27]  M. Hecker,et al.  Global Characterization of Disulfide Stress in Bacillus subtilis , 2003, Journal of bacteriology.

[28]  R. Losick,et al.  Additional Targets of the Bacillus subtilis Global Regulator CodY Identified by Chromatin Immunoprecipitation and Genome-Wide Transcript Analysis , 2003, Journal of bacteriology.

[29]  Harald Labischinski,et al.  Proteomic Approach to Understanding Antibiotic Action , 2003, Antimicrobial Agents and Chemotherapy.

[30]  M. Hecker,et al.  The role of peptide deformylase in protein biosynthesis: A proteomic study , 2003, Proteomics.

[31]  J. Errington,et al.  Cytokinesis in Bacteria , 2003, Microbiology and Molecular Biology Reviews.

[32]  J. Errington Dynamic proteins and a cytoskeleton in bacteria , 2003, Nature Cell Biology.

[33]  Jörg Bernhardt,et al.  Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. , 2003, Genome research.

[34]  K. Ochi,et al.  Guanine Nucleotides Guanosine 5′-Diphosphate 3′-Diphosphate and GTP Co-operatively Regulate the Production of an Antibiotic Bacilysin in Bacillus subtilis * , 2003, The Journal of Biological Chemistry.

[35]  R. Losick,et al.  RacA, a Bacterial Protein That Anchors Chromosomes to the Cell Poles , 2002, Science.

[36]  Harley H. McAdams,et al.  Generating and Exploiting Polarity in Bacteria , 2002, Science.

[37]  A. Link Multidimensional peptide separations in proteomics. , 2002, Trends in biotechnology.

[38]  M. Hecker,et al.  Bacillus subtilis functional genomics: genome-wide analysis of the DegS-DegU regulon by transcriptomics and proteomics , 2002, Molecular Genetics and Genomics.

[39]  M. Marahiel,et al.  Genomewide Transcriptional Analysis of the Cold Shock Response in Bacillus subtilis , 2002, Journal of bacteriology.

[40]  Lennart Martens,et al.  Chromatographic Isolation of Methionine-containing Peptides for Gel-free Proteome Analysis , 2002, Molecular & Cellular Proteomics.

[41]  Sue Goo Rhee,et al.  Inactivation of Human Peroxiredoxin I during Catalysis as the Result of the Oxidation of the Catalytic Site Cysteine to Cysteine-sulfinic Acid* , 2002, The Journal of Biological Chemistry.

[42]  Agnieszka Laszkiewicz,et al.  Characterization of a membrane‐linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes , 2002, Molecular microbiology.

[43]  Frederico J. Gueiros-Filho,et al.  A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. , 2002, Genes & development.

[44]  M. Hecker,et al.  Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion. , 2002, Journal of biotechnology.

[45]  A. van Dorsselaer,et al.  A method for detection of overoxidation of cysteines: peroxiredoxins are oxidized in vivo at the active-site cysteine during oxidative stress. , 2002, The Biochemical journal.

[46]  J. Helmann,et al.  Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilisσW and σM regulons , 2002 .

[47]  Ronald J Moore,et al.  Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Michael Hecker,et al.  Transcriptome and Proteome Analysis of Bacillus subtilis Gene Expression Modulated by Amino Acid Availability , 2002, Journal of bacteriology.

[49]  K. Ochi,et al.  RelA Protein Is Involved in Induction of Genetic Competence in Certain Bacillus subtilis Strains by Moderating the Level of Intracellular GTP , 2002, Journal of bacteriology.

[50]  J. Stülke,et al.  Control of the glycolytic gapA operon by the catabolite control protein A in Bacillus subtilis: a novel mechanism of CcpA‐mediated regulation , 2002, Molecular microbiology.

[51]  A. Strunnikov,et al.  Cell cycle‐dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein , 2002, The EMBO journal.

[52]  S. Ehrlich,et al.  An expanded view of bacterial DNA replication , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  R. Aebersold,et al.  Proteomics Analysis of Cellular Response to Oxidative Stress , 2002, The Journal of Biological Chemistry.

[54]  C. Harwood,et al.  Regulatory interactions between the Pho and sigma(B)-dependent general stress regulons of Bacillus subtilis. , 2002, Microbiology.

[55]  M. Hecker,et al.  Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis , 2002, Journal of bacteriology.

[56]  M. Hecker,et al.  Stabilization of cell wall proteins in Bacillus subtilis: A proteomic approach , 2002, Proteomics.

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

[58]  P. Bork,et al.  Functional organization of the yeast proteome by systematic analysis of protein complexes , 2002, Nature.

[59]  F. Gamo,et al.  Global Transcriptional Response of Bacillus subtilis to Heat Shock , 2001, Journal of bacteriology.

[60]  J. Hoheisel,et al.  Global Analysis of the General Stress Response ofBacillus subtilis , 2001, Journal of bacteriology.

[61]  Jan Maarten van Dijl,et al.  A proteomic view on genome-based signal peptide predictions. , 2001, Genome research.

[62]  P Youngman,et al.  Genome‐wide analysis of the general stress response in Bacillus subtilis , 2001, Molecular microbiology.

[63]  G. Homuth,et al.  Alkaline shock induces the Bacillus subtilisσW regulon , 2001 .

[64]  M. Hecker,et al.  Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon , 2001, Molecular microbiology.

[65]  A. Sonenshein,et al.  Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. , 2001, Genes & development.

[66]  M. Hecker,et al.  Proteome and transcriptome based analysis of Bacillus subtilis cells overproducing an insoluble heterologous protein , 2001, Applied Microbiology and Biotechnology.

[67]  S. Ehrlich,et al.  Functional Analysis of Bacterial Genes: A Practical Manual , 2001 .

[68]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[69]  D. Zühlke,et al.  Clp‐mediated proteolysis in Gram‐positive bacteria is autoregulated by the stability of a repressor , 2001, The EMBO journal.

[70]  K. Kobayashi,et al.  Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. , 2001, Nucleic acids research.

[71]  M. Hecker,et al.  The Clp Proteases of Bacillus subtilisAre Directly Involved in Degradation of Misfolded Proteins , 2000, Journal of bacteriology.

[72]  T. Nyström,et al.  Protein oxidation in response to increased transcriptional or translational errors. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Michael Hecker,et al.  Role of CcpA in Regulation of the Central Pathways of Carbon Catabolism in Bacillus subtilis , 1999, Journal of bacteriology.

[74]  S. Gygi,et al.  Quantitative analysis of complex protein mixtures using isotope-coded affinity tags , 1999, Nature Biotechnology.

[75]  J. Bernhardt,et al.  Identification of ςB-Dependent Genes in Bacillus subtilis Using a Promoter Consensus-Directed Search and Oligonucleotide Hybridization , 1999, Journal of bacteriology.

[76]  J. Bernhardt,et al.  Dual channel imaging of two‐dimensional electropherograms in Bacillus subtilis , 1999, Electrophoresis.

[77]  F. Neidhardt,et al.  Diagnosis of cellular states of microbial organisms using proteomics , 1999, Electrophoresis.

[78]  M. Hecker,et al.  Expression of the ςB-Dependent General Stress Regulon Confers Multiple Stress Resistance inBacillus subtilis , 1999 .

[79]  M. Hecker,et al.  The yvyD Gene of Bacillus subtilis Is under Dual Control of ςB and ςH , 1998 .

[80]  T. Nyström,et al.  Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. , 1998, Genes & development.

[81]  M. Hecker,et al.  Non‐specific, general and multiple stress resistance of growth‐restricted Bacillus subtilis cells by the expression of the σB regulon , 1998, Molecular microbiology.

[82]  C. Price,et al.  General Stress Transcription Factor ςB and Sporulation Transcription Factor ςH Each Contribute to Survival of Bacillus subtilis under Extreme Growth Conditions , 1998, Journal of bacteriology.

[83]  A. Goffeau,et al.  The complete genome sequence of the Gram-positive bacterium Bacillus subtilis , 1997, Nature.

[84]  M. Marahiel,et al.  Cloning and characterization of a relA/spoT homologue from Bacillus subtilis , 1997, Molecular microbiology.

[85]  L. Shapiro,et al.  Protein localization and cell fate in bacteria. , 1997, Science.

[86]  J. Bernhardt,et al.  Specific and general stress proteins in Bacillus subtilis--a two-deimensional protein electrophoresis study. , 1997, Microbiology.

[87]  M. Marahiel,et al.  Cold shock stress-induced proteins in Bacillus subtilis , 1996, Journal of bacteriology.

[88]  C. Price,et al.  Bacillus subtilis operon under the dual control of the general stress transcription factor σB and the sporulation transcription factor σH , 1996, Molecular microbiology.

[89]  M. Hecker,et al.  Heat‐shock and general stress response in Bacillus subtilis , 1996, Molecular microbiology.

[90]  R. Fleischmann,et al.  Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. , 1995, Science.

[91]  S. Engelmann,et al.  Analysis of the induction of general stress proteins of Bacillus subtilis. , 1994, Microbiology.

[92]  C. Price,et al.  Transcription factor sigma B of Bacillus subtilis controls a large stationary-phase regulon , 1993, Journal of bacteriology.

[93]  C. Price,et al.  Genetic method to identify regulons controlled by nonessential elements: isolation of a gene dependent on alternate transcription factor sigma B of Bacillus subtilis , 1991, Journal of bacteriology.

[94]  M. Hecker,et al.  General stress proteins in Bacillus subtilis , 1990 .

[95]  F. Neidhardt,et al.  Ribosomes as sensors of heat and cold shock in Escherichia coli. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[96]  F. Neidhardt,et al.  Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli , 1987, Journal of bacteriology.

[97]  R. Losick,et al.  Regulation of a promoter that is utilized by minor forms of RNA polymerase holoenzyme in Bacillus subtilis. , 1986, Journal of molecular biology.

[98]  M. Hecker,et al.  Heat-shock proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study , 1986 .

[99]  U. N. Streips,et al.  Heat shock proteins in bacilli , 1985, Journal of bacteriology.

[100]  K. Ochi,et al.  Initiation of Bacillus subtilis sporulation by the stringent response to partial amino acid deprivation. , 1981, The Journal of biological chemistry.

[101]  A. Dromerick,et al.  Response of Guanosine 5′-Triphosphate Concentration to Nutritional Changes and Its Significance for Bacillus subtilis Sporulation , 1981, Journal of bacteriology.

[102]  E. Freese,et al.  The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. , 1979, Biochimica et biophysica acta.

[103]  F. Neidhardt,et al.  Levels of major proteins of Escherichia coli during growth at different temperatures , 1979, Journal of bacteriology.

[104]  J. Klose Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues , 1975, Humangenetik.

[105]  H. Dichtelmüller,et al.  Studies on the control of development. Accumulation of guanosine tetraphosphate and pentaphosphate in response to inhibition of protein synthesis in Bacillus subtilis. , 1975, European journal of biochemistry.

[106]  G. Scheele,et al.  Two-dimensional gel analysis of soluble proteins. Charaterization of guinea pig exocrine pancreatic proteins. , 1975, The Journal of biological chemistry.

[107]  P. O’Farrell High resolution two-dimensional electrophoresis of proteins. , 1975, The Journal of biological chemistry.

[108]  K. Bunai,et al.  Profiling and comprehensive expression analysis of ABC transporter solute‐binding proteins of Bacillus subtilis membrane based on a proteomic approach , 2004, Electrophoresis.

[109]  Eduardo P C Rocha,et al.  An analysis of determinants of amino acids substitution rates in bacterial proteins. , 2004, Molecular biology and evolution.

[110]  M. Hecker A proteomic view of cell physiology of Bacillus subtilis--bringing the genome sequence to life. , 2003, Advances in biochemical engineering/biotechnology.

[111]  C. Price,et al.  General Stress Response , 2002 .

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

[113]  M. Hecker,et al.  General stress response of Bacillus subtilis and other bacteria. , 2001, Advances in microbial physiology.

[114]  R. Losick,et al.  Bacillus Subtilis and Its Closest Relatives: From Genes to Cells , 2001 .

[115]  K. Yamane,et al.  Proteome analysis of Bacillus subtilis extracellular proteins: a two-dimensional protein electrophoretic study. , 2000, Microbiology.

[116]  J. Bernhardt,et al.  First steps from a two‐dimensional protein index towards a response‐regulation map for Bacillus subtilis , 1997, Electrophoresis.

[117]  D. Rickwood,et al.  The heterogeneity of mouse-chromatin nonhistone proteins as evidenced by two-dimensional polyacrylamide-gel electrophoresis and ion-exchange chromatography. , 1974, European journal of biochemistry.