Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions?

The survival of individual organisms facing stress is enhanced by the induction of a set of changes. As the intensity, duration and nature of stress is highly variable, the optimal response to stress may be unpredictable. To face such an uncertain future, it may be advantageous for a clonal population to increase its phenotypic heterogeneity (bet-hedging), ensuring that at least a subset of cells would survive the current stress. With current techniques, assessing the extent of this variability experimentally remains a challenge. Here, we use a bioinformatic approach to compare stress response genes with the rest of the genome for the presence of various kinds of repeated sequences, elements known to increase variability during the transfer of genetic information (i.e. during replication, but also during gene expression). We investigated the potential for illegitimate and homologous recombination of 296 Escherichia coli genes related to repair, recombination and physiological adaptations to different stresses. Although long repeats capable of engaging in homologous recombination are almost absent in stress response genes, we observed a significant high number of short close repeats capable of inducing phenotypic variability by slipped-mispair during DNA, RNA or protein synthesis.

[1]  A. Albertini,et al.  On the formation of spontaneous deletions: The importance of short sequence homologies in the generation of large deletions , 1982, Cell.

[2]  David Sankoff,et al.  Time Warps, String Edits, and Macromolecules: The Theory and Practice of Sequence Comparison , 1983 .

[3]  W. Rutter,et al.  Homology requirements for recombination in Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Singer,et al.  Deletion formation in bacteriophage T4. , 1988, Journal of molecular biology.

[5]  C. Kurland,et al.  Processivity errors of gene expression in Escherichia coli. , 1990, Journal of molecular biology.

[6]  A. Danchin,et al.  Evidence for horizontal gene transfer in Escherichia coli speciation. , 1991, Journal of molecular biology.

[7]  The effect of the length of direct repeats and the presence of palindromes on deletion between directly repeated DNA sequences in bacteriophage T7. , 1991, Nucleic acids research.

[8]  T. Haltia,et al.  Subunit III of cytochrome c oxidase is not involved in proton translocation: a site‐directed mutagenesis study. , 1991, The EMBO journal.

[9]  J Ninio,et al.  Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. , 1991, Genetics.

[10]  C. Kurland,et al.  Translational accuracy and the fitness of bacteria. , 1992, Annual review of genetics.

[11]  E. Dervyn,et al.  Frequency of deletion formation decreases exponentially with distance between short direct repeats , 1994, Molecular microbiology.

[12]  A Danchin,et al.  SubtiList: a relational database for the Bacillus subtilis genome. , 1995, Microbiology.

[13]  J. Miller,et al.  Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. , 1996, Annual review of microbiology.

[14]  W. L. Payne,et al.  High Mutation Frequencies Among Escherichia coli and Salmonella Pathogens , 1996, Science.

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

[16]  F. Taddei,et al.  Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Riley,et al.  Protein evolution viewed through Escherichia coli protein sequences: introducing the notion of a structural segment of homology, the module. , 1997, Journal of molecular biology.

[18]  L. Kirkham,et al.  The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Wills,et al.  Abundant microsatellite polymorphism in Saccharomyces cerevisiae, and the different distributions of microsatellites in eight prokaryotes and S. cerevisiae, result from strong mutation pressures and a variety of selective forces. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A Danchin,et al.  Oligonucleotide bias in Bacillus subtilis: general trends and taxonomic comparisons. , 1998, Nucleic acids research.

[21]  Alex van Belkum,et al.  Short-Sequence DNA Repeats in Prokaryotic Genomes , 1998, Microbiology and Molecular Biology Reviews.

[22]  R. L. Charlebois Organization of the Prokaryotic Genome , 1999 .

[23]  A Danchin,et al.  Functional and evolutionary roles of long repeats in prokaryotes. , 1999, Research in microbiology.

[24]  M. Marinus,et al.  Escherichia coli mutator genes. , 1999, Trends in microbiology.

[25]  J. Majewski,et al.  DNA sequence similarity requirements for interspecific recombination in Bacillus. , 1999, Genetics.

[26]  Stefan Kurtz,et al.  REPuter: fast computation of maximal repeats in complete genomes , 1999, Bioinform..

[27]  B. Michel Illegitimate Recombination in Bacteria , 1999 .

[28]  A Danchin,et al.  Analysis of long repeats in bacterial genomes reveals alternative evolutionary mechanisms in Bacillus subtilis and other competent prokaryotes. , 1999, Molecular biology and evolution.

[29]  L. Liu,et al.  Inversion/dimerization of plasmids mediated by inverted repeats. , 1999, Journal of molecular biology.

[30]  Genetic Analysis of an Incomplete mutSGene from Pseudomonas putida , 2000, Journal of bacteriology.

[31]  Y. Kashi,et al.  Simple sequence repeats in Escherichia coli: abundance, distribution, composition, and polymorphism. , 2000, Genome research.

[32]  François Taddei,et al.  Evolutionary Implications of the Frequent Horizontal Transfer of Mismatch Repair Genes , 2000, Cell.

[33]  W Arber,et al.  Genetic variation: molecular mechanisms and impact on microbial evolution. , 2000, FEMS microbiology reviews.

[34]  A. Oliver,et al.  High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. , 2000, Science.

[35]  Thomas Nyström,et al.  Bacterial senescence: protein oxidation in non‐proliferating cells is dictated by the accuracy of the ribosomes , 2001, The EMBO journal.

[36]  D. Chang,et al.  Microsatellites in the eukaryotic DNA mismatch repair genes as modulators of evolutionary mutation rate. , 2001, Genome research.

[37]  A. Oliver,et al.  The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants , 2002, Molecular microbiology.

[38]  S. Lovett,et al.  Recombination between repeats in Escherichia coli by a recA-independent, proximity-sensitive mechanism , 1994, Molecular and General Genetics MGG.