Spatial patterns of transcriptional activity in the chromosome of Escherichia coli

BackgroundAlthough genes on the chromosome are organized in a fixed order, the spatial correlations in transcription have not been systematically evaluated. We used a combination of genomic and signal processing techniques to investigate the properties of transcription in the genome of Escherichia coli K12 as a function of the position of genes on the chromosome.ResultsSpectral analysis of transcriptional series revealed the existence of statistically significant patterns in the spatial series of transcriptional activity. These patterns could be classified into three categories: short-range, of up to 16 kilobases (kb); medium-range, over 100-125 kb; and long-range, over 600-800 kb. We show that the significant similarities in gene activities extend beyond the length of an operon and that local patterns of coexpression are dependent on DNA supercoiling. Unlike short-range patterns, the formation of medium and long-range transcriptional patterns does not strictly depend on the level of DNA supercoiling. The long-range patterns appear to correlate with the patterns of distribution of DNA gyrase on the bacterial chromosome.ConclusionsLocalization of structural components in the transcriptional signal revealed an asymmetry in the distribution of transcriptional patterns along the bacterial chromosome. The demonstration that spatial patterns of transcription could be modulated pharmacologically and genetically, along with the identification of molecular correlates of transcriptional patterns, offer for the first time strong evidence of physiologically determined higher-order organization of transcription in the bacterial chromosome.

[1]  Araceli M. Huerta,et al.  Regulatory network of Escherichia coli: consistency between literature knowledge and microarray profiles. , 2003, Genome research.

[2]  C. Smith,et al.  Transcription regulates oxolinic acid-induced DNA gyrase cleavage at specific sites on the E. coli chromosome. , 1990, Nucleic acids research.

[3]  N R Cozzarelli,et al.  Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  T. Speed,et al.  Statistical issues in cDNA microarray data analysis. , 2003, Methods in molecular biology.

[5]  A. Worcel,et al.  On the structure of the folded chromosome of Escherichia coli. , 1972, Journal of molecular biology.

[6]  Ronald W. Davis,et al.  Quantitative Monitoring of Gene Expression Patterns with a Complementary DNA Microarray , 1995, Science.

[7]  A. Khodursky,et al.  Topoisomerase IV is a target of quinolones in Escherichia coli. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[9]  Gerald M Rubin,et al.  Evidence for large domains of similarly expressed genes in the Drosophila genome , 2002, Journal of biology.

[10]  A. Grossman,et al.  Localization of bacterial DNA polymerase: evidence for a factory model of replication. , 1998, Science.

[11]  R. Sinden,et al.  Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Patrick T. McGrath,et al.  Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  G. Church,et al.  A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression , 2000, Nature Genetics.

[14]  N. Cozzarelli,et al.  Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Niki,et al.  Dynamic organization of chromosomal DNA in Escherichia coli. , 2000, Genes & development.

[16]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[17]  Albert-László Barabási,et al.  Spurious spatial periodicity of co-expression in microarray data due to printing design. , 2003, Nucleic acids research.

[18]  Patrick O. Brown,et al.  Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[20]  S. T. Buckland,et al.  An Introduction to the Bootstrap. , 1994 .

[21]  R. Tibshirani,et al.  Significance analysis of microarrays applied to the ionizing radiation response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Wang,et al.  Transcription and DNA supercoiling. , 1993, Current opinion in genetics & development.

[23]  S. Hiraga Chromosome and plasmid partition in Escherichia coli. , 1992, Annual review of biochemistry.

[24]  P. Young,et al.  Time series analysis, forecasting and control , 1972, IEEE Transactions on Automatic Control.

[25]  A. Khodursky,et al.  Escherichia coli spotted double-strand DNA microarrays: RNA extraction, labeling, hybridization, quality control, and data management. , 2003, Methods in molecular biology.

[26]  S Brunak,et al.  A DNA structural atlas for Escherichia coli. , 2000, Journal of molecular biology.

[27]  M. Gerstein,et al.  Relationship between gene co-expression and probe localization on microarray slides , 2003, BMC Genomics.

[28]  J. Yamagishi,et al.  Quinolone-resistant mutations of the gyrA gene of Escherichia coli , 2004, Molecular and General Genetics MGG.

[29]  Michael Grunstein,et al.  Histone acetylation and deacetylation in yeast , 2003, Nature Reviews Molecular Cell Biology.

[30]  Temple F. Smith,et al.  Operons in Escherichia coli: genomic analyses and predictions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Gary A. Churchill,et al.  Analysis of Variance for Gene Expression Microarray Data , 2000, J. Comput. Biol..

[32]  Jeremy D. Glasner,et al.  Genome-Scale Analysis of the Uses of the Escherichia coli Genome: Model-Driven Analysis of Heterogeneous Data Sets , 2003, Journal of bacteriology.

[33]  D. Botstein,et al.  DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[35]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[36]  M. Gellert,et al.  Regulation of the genes for E. coli DNA gyrase: Homeostatic control of DNA supercoiling , 1983, Cell.

[37]  J. Roth,et al.  Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium , 1996, Journal of bacteriology.

[38]  S. Dudoit,et al.  Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. , 2002, Nucleic acids research.

[39]  C. D. Hardy,et al.  Topological domain structure of the Escherichia coli chromosome. , 2004, Genes & development.

[40]  R. Bernander,et al.  Characterization of dnaC2 and dnaC28Mutants by Flow Cytometry , 1998, Journal of bacteriology.

[41]  K. Nordström,et al.  Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure , 1999, Molecular microbiology.

[42]  Gwilym M. Jenkins,et al.  Time series analysis, forecasting and control , 1972 .

[43]  Javier Tamames,et al.  Evolution of gene order conservation in prokaryotes , 2001, Genome Biology.

[44]  Lucy Shapiro,et al.  Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle , 2002, Proceedings of the National Academy of Sciences of the United States of America.