A conserved anti‐repressor controls horizontal gene transfer by proteolysis

The mobile genetic element ICEBs1 is an integrative and conjugative element (a conjugative transposon) found in the Bacillus subtilis chromosome. The SOS response and the RapI‐PhrI sensory system activate ICEBs1 gene expression, excision and transfer by inactivating the ICEBs1 repressor protein ImmR. Although ImmR is similar to many characterized phage repressors, we found that, unlike these repressors, inactivation of ImmR requires an ICEBs1‐encoded anti‐repressor ImmA (YdcM). ImmA was needed for the degradation of ImmR in B. subtilis. Coexpression of ImmA and ImmR in Escherichia coli or co‐incubation of purified ImmA and ImmR resulted in site‐specific cleavage of ImmR. Homologues of immR and immA are found in many mobile genetic elements. We found that the ImmA homologue encoded by B. subtilis phage φ105 is required for inactivation of the φ105 repressor (an ImmR homologue). ImmA‐dependent proteolysis of ImmR repressors may be a conserved mechanism for regulating horizontal gene transfer.

[1]  A. Grossman,et al.  Identification and characterization of int (integrase), xis (excisionase) and chromosomal attachment sites of the integrative and conjugative element ICEBs1 of Bacillus subtilis , 2007, Molecular microbiology.

[2]  A. Grossman,et al.  Identification of the Origin of Transfer (oriT) and DNA Relaxase Required for Conjugation of the Integrative and Conjugative Element ICEBs1 of Bacillus subtilis , 2007, Journal of bacteriology.

[3]  A. Grossman,et al.  Identification and characterization of the immunity repressor (ImmR) that controls the mobile genetic element ICEBs1 of Bacillus subtilis , 2007, Molecular microbiology.

[4]  Lei Wang,et al.  Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir , 2007, Proceedings of the National Academy of Sciences.

[5]  W. Shi,et al.  [Biology of two lysogenic phages from Bacillus thuringiensis MZ1]. , 2007, Wei sheng wu xue bao = Acta microbiologica Sinica.

[6]  C. Morel,et al.  Derepression of Excision of Integrative and Potentially Conjugative Elements from Streptococcus thermophilus by DNA Damage Response: Implication of a cI-Related Repressor , 2006, Journal of bacteriology.

[7]  A. Grossman,et al.  Characterization of the Global Transcriptional Responses to Different Types of DNA Damage and Disruption of Replication in Bacillus subtilis , 2006, Journal of bacteriology.

[8]  S. J. Billington,et al.  Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. , 2006, Genome research.

[9]  Eli S. Groban,et al.  Genetic Composition of the Bacillus subtilis SOS System , 2005, Journal of bacteriology.

[10]  Laura S. Frost,et al.  Mobile genetic elements: the agents of open source evolution , 2005, Nature Reviews Microbiology.

[11]  A. Grossman,et al.  Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Salyers,et al.  Regulation of Excision Genes of the Bacteroides Conjugative Transposon CTnDOT , 2005, Journal of bacteriology.

[13]  K. Jarrell,et al.  The genome of BCJA1c: a bacteriophage active against the alkaliphilic bacterium, Bacillus clarkii , 2005, Extremophiles.

[14]  A. Grossman,et al.  Control of DNA replication initiation by recruitment of an essential initiation protein to the membrane of Bacillus subtilis , 2004, Molecular microbiology.

[15]  Vincent Burrus,et al.  Shaping bacterial genomes with integrative and conjugative elements. , 2004, Research in microbiology.

[16]  Ulrich Dobrindt,et al.  Genomic islands in pathogenic and environmental microorganisms , 2004, Nature Reviews Microbiology.

[17]  David A Rasko,et al.  The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. , 2004, Nucleic acids research.

[18]  Ghislain Fournous,et al.  Prophage Genomics , 2003, Microbiology and Molecular Biology Reviews.

[19]  J. R. van der Meer,et al.  Genomic islands and the evolution of catabolic pathways in bacteria. , 2003, Current opinion in biotechnology.

[20]  Andreas Martin,et al.  Evolutionary stabilization of the gene-3-protein of phage fd reveals the principles that govern the thermodynamic stability of two-domain proteins. , 2003, Journal of molecular biology.

[21]  S. Salzberg,et al.  The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria , 2003, Nature.

[22]  J. García,et al.  Genome Organization and Molecular Analysis of the Temperate Bacteriophage MM1 of Streptococcus pneumoniae , 2003, Journal of bacteriology.

[23]  T. D. Read,et al.  Role of Mobile DNA in the Evolution of Vancomycin-Resistant Enterococcus faecalis , 2003, Science.

[24]  A. Salyers,et al.  The role of Bacteroides conjugative transposons in the dissemination of antibiotic resistance genes , 2002, Cellular and Molecular Life Sciences CMLS.

[25]  L. Rice Association of different mobile elements to generate novel integrative elements , 2002, Cellular and Molecular Life Sciences CMLS.

[26]  P. Mullany,et al.  Mechanism of integration and excision in conjugative transposons , 2002, Cellular and Molecular Life Sciences CMLS.

[27]  K. Scott The role of conjugative transposons in spreading antibiotic resistance between bacteria that inhabit the gastrointestinal tract , 2002, Cellular and Molecular Life Sciences CMLS.

[28]  Guillaume Pavlovic,et al.  Conjugative transposons: the tip of the iceberg , 2002, Molecular microbiology.

[29]  Lewis Y. Geer,et al.  CDART: protein homology by domain architecture. , 2002, Genome research.

[30]  Guillaume Pavlovic,et al.  The ICESt1 element of Streptococcus thermophilus belongs to a large family of integrative and conjugative elements that exchange modules and change their specificity of integration. , 2002, Plasmid.

[31]  M. Waldor,et al.  A satellite phage‐encoded antirepressor induces repressor aggregation and cholera toxin gene transfer , 2002, The EMBO journal.

[32]  John W. Beaber,et al.  Genomic and Functional Analyses of SXT, an Integrating Antibiotic Resistance Gene Transfer Element Derived from Vibrio cholerae , 2002, Journal of bacteriology.

[33]  Jian Wang,et al.  A complete sequence of the T. tengcongensis genome. , 2002, Genome research.

[34]  L. Gautier,et al.  Comparative Genomics of Listeria Species , 2001, Science.

[35]  J. Courcelle,et al.  Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. , 2001, Genetics.

[36]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[37]  R. Woodgate,et al.  Identification of additional genes belonging to the LexA regulon in Escherichia coli , 2000, Molecular microbiology.

[38]  M. Loessner,et al.  Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes : implications for phage evolution , 2000, Molecular microbiology.

[39]  H. Brüssow,et al.  Similarly organized lysogeny modules in temperate Siphoviridae from low GC content gram-positive bacteria. , 1999, Virology.

[40]  Thomas L. Madden,et al.  BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. , 1999, FEMS microbiology letters.

[41]  E. Haggård-Ljungquist,et al.  The E protein of satellite phage P4 acts as an anti‐repressor by binding to the C protein of helper phage P2 , 1998, Molecular microbiology.

[42]  J. Celli,et al.  Circularization of Tn916 is required for expression of the transposon‐encoded transfer functions: characterization of long tetracycline‐inducible transcripts reading through the attachment site , 1998, Molecular microbiology.

[43]  K. Shearwin,et al.  The Tum Protein of Coliphage 186 Is an Antirepressor* , 1998, The Journal of Biological Chemistry.

[44]  D. van Sinderen,et al.  Sequence analysis and characterization of phi O1205, a temperate bacteriophage infecting Streptococcus thermophilus CNRZ1205. , 1997, Microbiology.

[45]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[46]  S. Michaelis,et al.  A Novel Membrane-associated Metalloprotease, Ste24p, Is Required for the First Step of NH2-terminal Processing of the Yeast a-Factor Precursor , 1997, The Journal of cell biology.

[47]  Bradley T. Smith,et al.  The Bacillus subtilis dinR Gene Codes for the Analogue of Escherichia coli LexA , 1996, The Journal of Biological Chemistry.

[48]  E. Craig,et al.  Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. , 1996, Genetics.

[49]  K. Devine,et al.  The phage-like element PBSX and part of the skin element, which are resident at different locations on the Bacillus subtilis chromosome, are highly homologous. , 1996, Microbiology.

[50]  R. Losick,et al.  SpoIIAA governs the release of the cell-type specific transcription factor sigma F from its anti-sigma factor SpoIIAB. , 1996, Journal of molecular biology.

[51]  R. Yasbin,et al.  Phenotypic differentiation of "smart" versus "naive" bacteriophages of Bacillus subtilis , 1996, Journal of bacteriology.

[52]  D. Belin,et al.  Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter , 1995, Journal of bacteriology.

[53]  D. McConnell,et al.  Genetic control of bacterial suicide: regulation of the induction of PBSX in Bacillus subtilis , 1994, Journal of bacteriology.

[54]  T. Heinzel,et al.  C1 repressor of phage P1 is inactivated by noncovalent binding of P1 Coi protein. , 1992, The Journal of biological chemistry.

[55]  M. Van Montagu,et al.  Purification and in vitro DNA-binding specificity of the Bacillus subtilis phage phi 105 repressor. , 1989, The Journal of biological chemistry.

[56]  A. Grossman,et al.  Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis , 1989, Journal of bacteriology.

[57]  M. Van Montagu,et al.  Transcriptional control in the EcoRI-F immunity region of Bacillus subtilis phage phi 105. Identification and unusual structure of the operator. , 1987, Journal of molecular biology.

[58]  J. W. Little,et al.  Lysine-156 and serine-119 are required for LexA repressor cleavage: a possible mechanism. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. A. Rupley,et al.  Intramolecular cleavage of LexA and phage lambda repressors: dependence of kinetics on repressor concentration, pH, temperature, and solvent. , 1986, Biochemistry.

[60]  R. Yasbin,et al.  Genetic characterization of the inducible SOS-like system of Bacillus subtilis , 1984, Journal of bacteriology.

[61]  J. W. Little,et al.  Autodigestion of lexA and phage lambda repressors. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[62]  R. Sauer,et al.  Cleavage of the lambda and P22 repressors by recA protein. , 1982, The Journal of biological chemistry.

[63]  N. Vasantha,et al.  Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides , 1980, Journal of bacteriology.

[64]  J. Roberts,et al.  Escherichia coli recA gene product inactivates phage lambda repressor. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[65]  R. Schoenfeld,et al.  Comparative Genomics of Listeria Species , 1976 .

[66]  ro Jorge Serment-Guerrero,et al.  The SOS response of Escherichia coli , 2005 .

[67]  John W. Beaber,et al.  SOS response promotes horizontal dissemination of antibiotic resistance genes , 2004, Nature.

[68]  G. Churchward Conjugative Transposons and Related Mobile Elements , 2002 .

[69]  P. Stragier,et al.  Plasmids for ectopic integration in Bacillus subtilis. , 1996, Gene.

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

[71]  M. Ptashne A Genetic Switch , 1986 .

[72]  P. Youderian,et al.  Bacteriophage P22 Antirepressor and Its Control , 1983 .

[73]  J. Roberts,et al.  Proteolytic cleavage of bacteriophage lambda repressor in induction. , 1975, Proceedings of the National Academy of Sciences of the United States of America.