Bacterial genome size reduction by experimental evolution.

Bacterial evolution toward endosymbiosis with eukaryotic cells is associated with extensive bacterial genome reduction and loss of metabolic and regulatory capabilities. Here we examined the rate and process of genome reduction in the bacterium Salmonella enterica by a serial passage experimental evolution procedure. The initial rate of DNA loss was estimated to be 0.05 bp per chromosome per generation for a WT bacterium and approximately 50-fold higher for a mutS mutant defective in methyl-directed DNA mismatch repair. The endpoints were identified for seven chromosomal deletions isolated during serial passage and in two separate genetic selections. Deletions ranged in size from 1 to 202 kb, and most of them were not associated with DNA repeats, indicating that they were formed via RecA-independent recombination events. These results suggest that extensive genome reduction can occur on a short evolutionary time scale and that RecA-dependent homologous recombination only plays a limited role in this process of jettisoning superfluous DNA.

[1]  N. Moran,et al.  50 Million Years of Genomic Stasis in Endosymbiotic Bacteria , 2002, Science.

[2]  T. Vartiainen,et al.  Genotoxic effects of the drinking water mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2[5H]-furanone (MX) in mammalian cells in vitro and in rats in vivo. , 1991, Mutation research.

[3]  Rekha R Meyer,et al.  Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid , 2004, Nature Genetics.

[4]  R. Wilson,et al.  Complete genome sequence of Salmonella enterica serovar Typhimurium LT2 , 2001, Nature.

[5]  J. A. Halliday,et al.  Mechanisms of spontaneous mutation in DNA repair-proficient Escherichia coli. , 1991, Mutation research.

[6]  A. Danchin,et al.  Mutations in the bglY gene increase the frequency of spontaneous deletions in Escherichia coli K-12. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[7]  T. Sicheritz-Pontén,et al.  The genome sequence of Rickettsia prowazekii and the origin of mitochondria , 1998, Nature.

[8]  A. Moya,et al.  Genome size reduction through multiple events of gene disintegration in Buchnera APS. , 2001, Trends in genetics : TIG.

[9]  H. Shinagawa,et al.  RecA-independent high-frequency deletion of recombinant cosmid DNA in Escherichia coli. , 1990, Journal of general microbiology.

[10]  K. Sanderson,et al.  A physical map of the Salmonella typhimurium LT2 genome made by using XbaI analysis , 1992, Journal of bacteriology.

[11]  R. Schaaper,et al.  Spontaneous mutation in the Escherichia coli lacI gene. , 1991, Genetics.

[12]  N. Moran,et al.  Microbial Minimalism Genome Reduction in Bacterial Pathogens , 2002, Cell.

[13]  B. Ames,et al.  Positive selection for loss of tetracycline resistance , 1980, Journal of bacteriology.

[14]  Arthur Thompson,et al.  Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica , 2002, Molecular microbiology.

[15]  N. Moran,et al.  Deletional bias and the evolution of bacterial genomes. , 2001, Trends in genetics : TIG.

[16]  N. Uematsu,et al.  DNA sequence analysis of spontaneous tonB deletion mutations in a polA1 strain of Escherichia coli K12. , 1999, Biochemical and biophysical research communications.

[17]  H. Ochman,et al.  Lateral and oblique gene transfer. , 2001, Current opinion in genetics & development.

[18]  T. Fuchs,et al.  Large‐scale identification of essential Salmonella genes by trapping lethal insertions , 2004, Molecular microbiology.

[19]  N. Moran,et al.  The process of genome shrinkage in the obligate symbiont Buchnera aphidicola , 2001, Genome Biology.

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

[21]  S. Andersson,et al.  Evolution of minimal-gene-sets in host-dependent bacteria. , 2004, Trends in microbiology.

[22]  Hiroshi Mizoguchi,et al.  Cell size and nucleoid organization of engineered Escherichia coli cells with a reduced genome , 2004, Molecular microbiology.

[23]  E. Rocha An appraisal of the potential for illegitimate recombination in bacterial genomes and its consequences: from duplications to genome reduction. , 2003, Genome research.

[24]  H. Ochman,et al.  Molecular archaeology of the Escherichia coli genome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  A. Moya,et al.  Why are the genomes of endosymbiotic bacteria so stable? , 2003, Trends in genetics : TIG.

[26]  S. A. Chow,et al.  Ionic inhibition of formation of RecA nucleoprotein networks blocks homologous pairing. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Schofield,et al.  DNA mismatch repair: molecular mechanisms and biological function. , 2003, Annual review of microbiology.

[28]  H. Ikeda,et al.  The DNA gyrase of Escherichia coli participates in the formation of a spontaneous deletion by recA-independent recombination in vivo , 1990, Molecular and General Genetics MGG.

[29]  A. Thompson,et al.  Comparative Genomic Indexing Reveals the Phylogenomics of Escherichia coli Pathogens , 2003, Infection and Immunity.

[30]  B. Barrell,et al.  Massive gene decay in the leprosy bacillus , 2001, Nature.

[31]  Eduardo P C Rocha,et al.  Order and disorder in bacterial genomes. , 2004, Current opinion in microbiology.

[32]  Guy Plunkett,et al.  Engineering a reduced Escherichia coli genome. , 2002, Genome research.

[33]  Henry Huang,et al.  Homologous recombination in Escherichia coli: dependence on substrate length and homology. , 1986, Genetics.