Genome-Wide Transcriptional Profiling Analysis of Adaptation of Bacillus subtilis to High Salinity

ABSTRACT The gram-positive soil bacterium Bacillus subtilis often faces increases in the salinity in its natural habitats. A transcriptional profiling approach was utilized to investigate both the initial reaction to a sudden increase in salinity elicited by the addition of 0.4 M NaCl and the cellular adaptation reactions to prolonged growth at high salinity (1.2 M NaCl). Following salt shock, a sigB mutant displayed immediate and transient induction and repression of 75 and 51 genes, respectively. Continuous propagation of this strain in the presence of 1.2 M NaCl triggered the induction of 123 genes and led to the repression of 101 genes. In summary, our studies revealed (i) an immediate and transient induction of the SigW regulon following salt shock, (ii) a role of the DegS/DegU two-component system in sensing high salinity, (iii) a high-salinity-mediated iron limitation, and (iv) a repression of chemotaxis and motility genes by high salinity, causing severe impairment of the swarming capability of B. subtilis cells. Initial adaptation to salt shock and continuous growth at high salinity share only a limited set of induced and repressed genes. This finding strongly suggests that these two phases of adaptation require distinctively different physiological adaptation reactions by the B. subtilis cell. The large portion of genes with unassigned functions among the high-salinity-induced or -repressed genes demonstrates that major aspects of the cellular adaptation of B. subtilis to high salinity are unexplored so far.

[1]  E. Bremer,et al.  KtrAB and KtrCD: Two K+ Uptake Systems in Bacillus subtilis and Their Role in Adaptation to Hypertonicity , 2003, Journal of bacteriology.

[2]  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.

[3]  J. Helmann,et al.  Regulation of the Bacillus subtilis fur and perR Genes by PerR: Not All Members of the PerR Regulon Are Peroxide Inducible , 2002, Journal of bacteriology.

[4]  Mark Albano,et al.  Microarray analysis of the Bacillus subtilis K‐state: genome‐wide expression changes dependent on ComK , 2002, Molecular microbiology.

[5]  Min Cao,et al.  Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. , 2002, Journal of molecular biology.

[6]  U. Völker,et al.  High-Salinity-Induced Iron Limitation in Bacillus subtilis , 2002, Journal of bacteriology.

[7]  Naotake Ogasawara,et al.  Comprehensive DNA Microarray Analysis ofBacillus subtilis Two-Component Regulatory Systems , 2001, Journal of bacteriology.

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

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

[10]  T. Tanaka,et al.  DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B.subtilis two-component regulatory systems. , 2001, Nucleic acids research.

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

[12]  J. Bernhardt,et al.  A comprehensive two‐dimensional map of cytosolic proteins of Bacillus subtilis , 2001, Electrophoresis.

[13]  A. Sonenshein,et al.  Multiple Genes for the Last Step of Proline Biosynthesis in Bacillus subtilis , 2001, Journal of bacteriology.

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

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

[16]  M. Marahiel,et al.  The dhb Operon of Bacillus subtilisEncodes the Biosynthetic Template for the Catecholic Siderophore 2,3-Dihydroxybenzoate-Glycine-Threonine Trimeric Ester Bacillibactin* , 2001, The Journal of Biological Chemistry.

[17]  S. Bron,et al.  Signal Peptide-Dependent Protein Transport inBacillus subtilis: a Genome-Based Survey of the Secretome , 2000, Microbiology and Molecular Biology Reviews.

[18]  E. Bremer Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in B. subtilis , 2000 .

[19]  D. Mirel,et al.  Environmental Regulation of Bacillus subtilis ςD-Dependent Gene Expression , 2000, Journal of bacteriology.

[20]  S. Ruzal,et al.  Biochemical and biophysical studies of Bacillus subtilis envelopes under hyperosmotic stress. , 2000, International journal of food microbiology.

[21]  J. Helmann,et al.  Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins , 2000, Molecular microbiology.

[22]  J. Helmann,et al.  Interaction of Bacillus subtilis Fur (Ferric Uptake Repressor) with the dhb Operator In Vitro and In Vivo , 1999, Journal of bacteriology.

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

[24]  A. Moir,et al.  σM, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt , 1999, Molecular microbiology.

[25]  I. Booth,et al.  Managing hypoosmotic stress: aquaporins and mechanosensitive channels in Escherichia coli. , 1999, Current opinion in microbiology.

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

[27]  J. Boch,et al.  Two evolutionarily closely related ABC transporters mediate the uptake of choline for synthesis of the osmoprotectant glycine betaine in Bacillus subtilis , 1999, Molecular microbiology.

[28]  S. Ruzal,et al.  In Bacillus subtilis DegU-P Is a Positive Regulator of the Osmotic Response , 1998, Current Microbiology.

[29]  M Vingron,et al.  Transcriptional profiling on all open reading frames of Saccharomyces cerevisiae , 1998, Yeast.

[30]  E. Bremer,et al.  Osmoregulation of the opuE proline transport gene from Bacillus subtilis: contributions of the sigma A‐ and sigma B‐dependent stress‐responsive promoters , 1998, Molecular microbiology.

[31]  M. Débarbouillé,et al.  Characterization of a Novel Member of the DegS-DegU Regulon Affected by Salt Stress in Bacillus subtilis , 1998, Journal of bacteriology.

[32]  S. Ruzal,et al.  Osmotic Strength Blocks Sporulation at Stage II by Impeding Activation of Early Sigma Factors in Bacillus subtilis , 1998, Current Microbiology.

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

[34]  A. Alice,et al.  DNA Supercoiling and Osmoresistance in Bacillus subtilis 168 , 1997, Current Microbiology.

[35]  E. Bremer,et al.  Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B , 1997, Molecular microbiology.

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

[37]  E. Bremer,et al.  Bacillus subtilis : characterization of OpuD . osmoprotectant glycine betaine operate in Three transport systems for the , 1996 .

[38]  J. Boch,et al.  Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes , 1996, Journal of bacteriology.

[39]  M. Ogura,et al.  Transcription of Bacillus subtilis degR is sigma D dependent and suppressed by multicopy proB through sigma D , 1996, Journal of bacteriology.

[40]  R. Allmansberger,et al.  Changes in DNA supertwist as a response of Bacillus subtilis towards different kinds of stress. , 1995, FEMS microbiology letters.

[41]  J. Hansen,et al.  Characterization of a chimeric proU operon in a subtilin-producing mutant of Bacillus subtilis 168 , 1995, Journal of bacteriology.

[42]  E. Bremer,et al.  OpuA, an Osmotically Regulated Binding Protein-dependent Transport System for the Osmoprotectant Glycine Betaine in Bacillus subtilis(*) , 1995, The Journal of Biological Chemistry.

[43]  M. Hecker,et al.  Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses , 1995, Journal of bacteriology.

[44]  W. Schumann,et al.  The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshift , 1995, Journal of bacteriology.

[45]  G. Rapoport,et al.  Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis , 1995, Journal of bacteriology.

[46]  J. Boch,et al.  Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline , 1994, Journal of bacteriology.

[47]  J. Sekiguchi,et al.  Effect of degS-degU mutations on the expression of sigD, encoding an alternative sigma factor, and autolysin operon of Bacillus subtilis , 1994, Journal of bacteriology.

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

[49]  S. Ruzal,et al.  Physiological and genetic characterization of the osmotic stress response in Bacillus subtilis. , 1994, Canadian journal of microbiology.

[50]  C. Price,et al.  Stress-induced activation of the sigma B transcription factor of Bacillus subtilis , 1993, Journal of bacteriology.

[51]  M. Osburne,et al.  Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes , 1993, Journal of bacteriology.

[52]  J. Helmann,et al.  Metalloregulation in Bacillus subtilis: isolation and characterization of two genes differentially repressed by metal ions , 1993, Journal of bacteriology.

[53]  R. Reed,et al.  Determination of turgor pressure in Bacillus subtilis: a possible role for K+ in turgor regulation. , 1990, Journal of general microbiology.

[54]  J A Chudek,et al.  The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. , 1990, Journal of general microbiology.

[55]  M. Goodfellow,et al.  The Aerobic Endospore-Forming Bacteria: Classification and Identification , 1981 .

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

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

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

[59]  Antoine Danchin,et al.  SubtiList: the reference database for the Bacillus subtilis genome , 2002, Nucleic Acids Res..

[60]  E. Bremer Adaptation to Changing Osmolanty , 2002 .

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

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

[63]  G. Homuth,et al.  Alkaline shock induces the Bacillus subtilis sigma(W) regulon. , 2001, Molecular microbiology.

[64]  E. Bremer Coping with osmotic challenges : osmoregulation through accumulation and release of compatible solutes in bacteria , 2000 .

[65]  Ann M Stock,et al.  Two-component signal transduction. , 2000, Annual review of biochemistry.

[66]  S. Bron,et al.  Signal peptide-dependent protein transport in Bacillus subtilis , 2000 .

[67]  A. Wipat,et al.  The Bacillus subtilis genome sequence: the molecular blueprint of a soil bacterium , 1999 .

[68]  M. Hecker,et al.  Expression of the sigmaB-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. , 1999, Journal of bacteriology.

[69]  S. Ruzal,et al.  Variations of the Envelope Composition of Bacillus subtilis During Growth in Hyperosmotic Medium , 1998, Current Microbiology.

[70]  Nihon Hassei Seibutsu Gakkai,et al.  Genes to cells , 1996 .

[71]  J. M. Wood,et al.  Osmoadaptation by rhizosphere bacteria. , 1996, Annual review of microbiology.

[72]  G. Rapoport,et al.  A Signal Transduction Network in Bacillus subtilis Includes the DegS/DegU and ComP/ComA Two-Component Systems , 1995 .

[73]  R. Losick,et al.  Bacillus Subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics , 1993 .

[74]  G. Rapoport,et al.  Two-Component Regulatory Systems , 1993 .

[75]  F. Priest Systematics and Ecology of Bacillus , 1993 .

[76]  C. Harwood,et al.  Molecular biological methods for Bacillus , 1990 .

[77]  C. Price,et al.  Stress-Induced Activation of the cyB Transcription Factor of Bacillus subtilis , 2022 .