Validating the significance of genomic properties of Chi sites from the distribution of all octamers in Escherichia coli.

Chi sites (5'-GCTGGTGG-3') are homologous recombinational hotspot octamer sequences, which attenuate the exonuclease activity of RecBCD in Escherichia coli. They are overrepresented in the genome (1008 occurrences), preferentially located within coding regions (98%), oriented in the direction of replication (75%), and occur most commonly on the mRNA-synonymous sense strand of the double helix (79%). Previous statistical studies of the genome sequence suggested that these genomic properties of Chi sites appear to be related to their role in recombinational repair and therefore to replication and transcription. In this study, we employ three mathematical models to predict the properties of Chi sites from single nucleotide and multi-nucleotide compositions, and validate them statistically using the distribution of all octamer sequences in the entire genome, or exclusively within ORFs. The model based on the overall distribution of all octamers provided better predictions than the single nucleotide composition model, and the ORF and sense strand preference of Chi sites were shown to be within the standard deviation of all octamers. In contrast, the orientation bias of the Chi sites in the direction of replication was significant, although the bias was not as pronounced as with the single nucleotide composition model, suggesting a selective pressure related to the role of RecBCD in replication.

[1]  I. Biswas,et al.  A 7-base-pair sequence protects DNA from exonucleolytic degradation in Lactococcus lactis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Piero R Bianco,et al.  Direct visualization of RecBCD movement reveals cotranslocation of the RecD motor after chi recognition. , 2005, Molecular cell.

[3]  Gerald R. Smith,et al.  RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity , 2003, Nature.

[4]  S. Kowalczykowski,et al.  Identification of the RecA protein-loading domain of RecBCD enzyme. , 2000, Journal of molecular biology.

[5]  F. Chédin,et al.  The Recombination Hot Spot Chi Is Embedded within Islands of Preferred DNA Pairing Sequences in the E. coli Genome , 1997, Cell.

[6]  A. Gruss,et al.  Edinburgh Research Explorer Identification of the lactococcal exonuclease/recombinase and its modulation by the putative Chi sequence , 2022 .

[7]  Sophie Schbath,et al.  Exceptional Motifs in Different Markov Chain Models for a Statistical Analysis of DNA Sequences , 1995, J. Comput. Biol..

[8]  D. Forsdyke,et al.  Crossover hot-spot instigator (Chi) sequences in Escherichia coli occupy distinct recombination/transcription islands. , 2000, Gene.

[9]  S. Salzberg,et al.  Skewed oligomers and origins of replication. , 1998, Gene.

[10]  E. Tillier,et al.  The Contributions of Replication Orientation, Gene Direction, and Signal Sequences to Base-Composition Asymmetries in Bacterial Genomes , 2000, Journal of Molecular Evolution.

[11]  F. Chédin,et al.  A five‐nucleotide sequence protects DNA from exonucleolytic degradation by AddAB, the RecBCD analogue of Bacillus subtilis , 1998, Molecular microbiology.

[12]  S. Kowalczykowski,et al.  The recombination hotspot Chi is recognized by the translocating RecBCD enzyme as the single strand of DNA containing the sequence 5'-GCTGGTGG-3'. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Meriem El Karoui,et al.  Identification of the Chi site of Haemophilus influenzae as several sequences related to the Escherichia coli Chi site , 1998, Molecular microbiology.

[14]  G. R. Smith,et al.  Homologous recombination near and far from DNA breaks: alternative roles and contrasting views. , 2001, Annual review of genetics.

[15]  T. Colbert,et al.  Genomics, Chi sites and codons: 'islands of preferred DNA pairing' are oceans of ORFs. , 1998, Trends in genetics : TIG.

[16]  S. Schbath,et al.  Characteristics of Chi distribution on different bacterial genomes. , 1999, Research in microbiology.

[17]  K. Kreuzer Interplay between DNA replication and recombination in prokaryotes. , 2005, Annual review of microbiology.

[18]  S. Ehrlich,et al.  The Bacillus subtilis AddAB helicase/nuclease is regulated by its cognate Chi sequence in vitro. , 2000, Journal of molecular biology.

[19]  S. Ohno Grammatical analysis of DNA sequences provides a rationale for the regulatory control of an entire chromosome. , 1990, Genetical research.

[20]  Y. Nakayama,et al.  Over-representation of Chi sequences caused by di-codon increase in Escherichia coli K-12. , 2006, Gene.

[21]  A. Gruss,et al.  Codon usage can explain GT‐rich islands surrounding Chi sites on the Escherichia coli genome , 1998, Molecular microbiology.

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

[23]  J. Lobry,et al.  Polarisation of prokaryotic chromosomes. , 2003, Current opinion in microbiology.

[24]  D. Forsdyke,et al.  Correlation of chi orientation with transcription indicates a fundamental relationship between recombination and transcription. , 1998, Gene.

[25]  S. Kowalczykowski,et al.  Biochemistry of homologous recombination in Escherichia coli. , 1994, Microbiological reviews.

[26]  J. Martínez-Salazar,et al.  The Recombination Genes addAB Are Not Restricted to Gram-Positive Bacteria: Genetic Analysis of the Recombination Initiation Enzymes RecF and AddAB in Rhizobium etli , 2004, Journal of bacteriology.

[27]  A. Sorokin,et al.  Orientation specificity of the Lactococcus lactis Chi site , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[28]  K. H. Wolfe,et al.  Base Composition Skews, Replication Orientation, and Gene Orientation in 12 Prokaryote Genomes , 1998, Journal of Molecular Evolution.

[29]  S. Kowalczykowski,et al.  In vitro selection of preferred DNA pairing sequences by the Escherichia coli RecA protein. , 1996, Genes & development.

[30]  Temple F. Smith,et al.  Patterns of Genome Organization in Bacteria , 1998, Science.

[31]  F. Blattner,et al.  DNA sequence and analysis of 136 kilobases of the Escherichia coli genome: organizational symmetry around the origin of replication. , 1993, Genomics.

[32]  S. Kowalczykowski,et al.  RecBCD enzyme is a bipolar DNA helicase , 2003, Nature.

[33]  Y. Nakayama,et al.  The orientation bias of Chi sequences is a general tendency of G-rich oligomers. , 2000, Gene.

[34]  Masaru Tomita,et al.  G-language Genome Analysis Environment: a workbench for nucleotide sequence data mining , 2003, Bioinform..

[35]  F. Chédin,et al.  A novel family of regulated helicases/nucleases from Gram‐positive bacteria: insights into the initiation of DNA recombination , 2002, Molecular microbiology.

[36]  Eduardo P C Rocha,et al.  The replication-related organization of bacterial genomes. , 2004, Microbiology.

[37]  A. Kuzminov Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. , 1999, Microbiology and molecular biology reviews : MMBR.