Global Impact of sdiA Amplification Revealed by Comprehensive Gene Expression Profiling of Escherichia coli

ABSTRACT In Escherichia coli the amplification ofsdiA, a positive activator of ftsQAZ, genes that are essential for septation, results in mitomycin C resistance. To help us understand this resistance phenotype, genes whose expression was altered by increased sdiA dosage were identified using a DNA microarray-based, comprehensive transcript profiling method. The expression of 62 genes was reduced by more than threefold; of these, 41 are involved in motility and chemotaxis. Moreover, the expression of 75 genes, 36 of which had been previously characterized, was elevated at least threefold. As expected, increased sdiA dosage led to significantly elevated sdiA and ′ddlB-ftsQAZ-lpxC operon expression. Transcription of two genes, uvrY and uvrC, located downstream ofsdiA and oriented in the same direction, was elevated about 10-fold, although the intervening gene, yecF, of opposite polarity was unaffected by increased sdiA dosage. Three genes (mioC and gidAB) flanking the replication origin, oriC, were transcribed more often whensdiA dosage was high, as were 12 genes within 1 min of a terminus of replication, terB. Transcription of theacrABDEF genes, mapping in three widely spaced loci, was elevated significantly, while several genes involved in DNA repair and replication (e.g., nei, recN, mioC, and mcrC) were moderately elevated in expression. Such global analysis provides a link between septation and the response to DNA-damaging agents.

[1]  R. D'ari,et al.  Metabolic Alarms and Cell Division inEscherichia coli , 1999, Journal of bacteriology.

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

[3]  W. Degraff,et al.  Mechanisms of hypoxic and aerobic cytotoxicity of mitomycin C in Chinese hamster V79 cells. , 1991, Cancer research.

[4]  S. Nakajima,et al.  Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12 , 1997, Journal of bacteriology.

[5]  H. Nikaido,et al.  AcrD of Escherichia coli Is an Aminoglycoside Efflux Pump , 2000, Journal of bacteriology.

[6]  Y. Hotta,et al.  Cell Division , 2021, Nature.

[7]  J. Hearst,et al.  The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals , 1996, Molecular microbiology.

[8]  M. Tomasz,et al.  The mitomycin bioreductive antitumor agents: cross-linking and alkylation of DNA as the molecular basis of their activity. , 1997, Pharmacology & therapeutics.

[9]  J. van Reeuwijk,et al.  Salmonella typhimurium Encodes an SdiA Homolog, a Putative Quorum Sensor of the LuxR Family, That Regulates Genes on the Virulence Plasmid , 1998, Journal of bacteriology.

[10]  R. Painter,et al.  DNA repair mechanisms , 1978, Nature.

[11]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[12]  B. Ames,et al.  A new Salmonella tester strain (TA102) with A X T base pairs at the site of mutation detects oxidative mutagens. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[13]  T. Okazaki,et al.  Cell cycle-dependent transcription from the gid and mioC promoters of Escherichia coli , 1994, Journal of bacteriology.

[14]  H. Nikaido.  Multidrug efflux pumps of gram-negative bacteria , 1996, Journal of bacteriology.

[15]  L. Rothfield,et al.  A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. , 1991, The EMBO journal.

[16]  D. Lockhart,et al.  Expression monitoring by hybridization to high-density oligonucleotide arrays , 1996, Nature Biotechnology.

[17]  D. Botstein,et al.  Advanced bacterial genetics , 1980 .

[18]  B. Bachmann,et al.  Linkage map of Escherichia coli K-12, edition 8 , 1990, Microbiological reviews.

[19]  R. Larossa,et al.  In Vivo Titration of Mitomycin C Action by Four Escherichia coli Genomic Regions on Multicopy Plasmids , 2001, Journal of bacteriology.

[20]  J. Laval.  Role of DNA repair enzymes in the cellular resistance to oxidative stress. , 1996, Pathologie-biologie.

[21]  J. Hoeijmakers,et al.  DNA repair mechanisms. , 2001, Maturitas.

[22]  Monica Riley,et al.  Escherichia coli gene products: Physiological functions and common ancestries , 1996 .

[23]  P. H. Makela.  Enterobacterial Common Antigen , 2022 .

[24]  K. Takagi,et al.  RobA‐lnduced Multiple Antibiotic Resistance Largely Depends on the Activation of the AcrAB Efflux , 1997, Microbiology and immunology.

[25]  T. Baldwin,et al.  Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  E. Meighen,et al.  Molecular biology of bacterial bioluminescence. , 1991, Microbiological reviews.

[27]  R. Larossa,et al.  Improved bacterial SOS promoter∷lux fusions for genotoxicity detection. , 2000, Mutation research.

[28]  Frederick R. Blattner,et al.  High-Density Microarray-Mediated Gene Expression Profiling of Escherichia coli , 2001, Journal of bacteriology.

[29]  W. Rupp.  DNA Repair Mechanisms , 1999 .

[30]  M Aldea,et al.  Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. , 1993, The EMBO journal.

[31]  F. Neidhardt,et al.  Linkage Map of Escherichia coli K-12 , 1987 .

[32]  R. Menzel,et al.  A microtiter plate-based system for the semiautomated growth and assay of bacterial cells for beta-galactosidase activity. , 1989, Analytical biochemistry.