Gene conversion and concerted evolution in bacterial genomes

Gene conversion is defined as the non-reciprocal transfer of information between homologous sequences. Despite methodological problems to establish non-reciprocity, gene conversion has been demonstrated in a wide variety of bacteria. Besides examples of high-frequency reversion of mutations in repeated genes, gene conversion in bacterial genomes has been implicated in concerted evolution of multigene families. Gene conversion also has a prime importance in the generation of antigenic variation, an interesting mechanism whereby some bacterial pathogens are able to avoid the host immune system. In this review, we analyze examples of bacterial gene conversion (some of them spawned from the current genomic revolution), as well as the molecular models that explain gene conversion and its association with crossovers.

[1]  L. N. Ornston,et al.  Properties of Acinetobacter calcoaceticus recA and its contribution to intracellular gene conversion , 1994, Molecular microbiology.

[2]  K. Sanderson,et al.  Salmonella typhi contains identical intervening sequences in all seven rrl genes , 1996, Journal of bacteriology.

[3]  D. Zickler,et al.  Early Decision Meiotic Crossover Interference prior to Stable Strand Exchange and Synapsis , 2004, Cell.

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

[5]  E. Böttger,et al.  RecA-Mediated Gene Conversion and Aminoglycoside Resistance in Strains Heterozygous for rRNA , 1999, Antimicrobial Agents and Chemotherapy.

[6]  M. Radman,et al.  2-Aminopurine Allows Interspecies Recombination by a Reversible Inactivation of the Escherichia coli Mismatch Repair System , 2003, Journal of bacteriology.

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

[8]  Kazuo Yamamoto.  Dissection of functional domains in Escherichia coli DNA photolyase by linker-insertion mutagenesis , 1992, Molecular and General Genetics MGG.

[9]  K. Brayton,et al.  Antigenic variation of Anaplasma marginale msp2 occurs by combinatorial gene conversion , 2002, Molecular microbiology.

[10]  C. Rodríguez,et al.  Repeated sequences in bacterial chromosomes and plasmids: a glimpse from sequenced genomes. , 1999, Research in microbiology.

[11]  F. Rurangirwa,et al.  Antigenic Variation of Anaplasma marginale by Expression of MSP2 Mosaics , 2000, Infection and Immunity.

[12]  A. Kuzminov.  Single-strand interruptions in replicating chromosomes cause double-strand breaks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  F. Stahl.  Genetic recombination : thinking about it in phage and fungi , 1979 .

[14]  I. Kobayashi,et al.  Nonconservative recombination in Escherichia coli. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Seifert,et al.  Iron availability regulates DNA recombination in Neisseria gonorrhoeae , 2000, Molecular microbiology.

[16]  F. Stahl,et al.  The Holliday junction on its thirtieth anniversary. , 1994, Genetics.

[17]  P. Markham,et al.  Mycoplasma synoviae has two distinct phase-variable major membrane antigens, one of which is a putative hemagglutinin , 1997, Infection and immunity.

[18]  D. Liao.  Gene Conversion Drives Within Genic Sequences: Concerted Evolution of Ribosomal RNA Genes in Bacteria and Archaea , 2000, Journal of Molecular Evolution.

[19]  J. Bakken,et al.  Human ehrlichioses: newly recognized infections transmitted by ticks. , 1998, Annual review of medicine.

[20]  A. Kuzminov.  DNA replication meets genetic exchange: Chromosomal damage and its repair by homologous recombination , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Hughes.  Co-evolution of the tuf genes links gene conversion with the generation of chromosomal inversions. , 2000, Journal of molecular biology.

[22]  H. Seifert,et al.  Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation , 2000, Molecular microbiology.

[23]  D. Leach,et al.  Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. , 2001, Molecular cell.

[24]  B. Michel,et al.  Rescue of arrested replication forks by homologous recombination , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Skurnik,et al.  Intervening sequences (IVSs) in the 23S ribosomal RNA genes of pathogenic Yersinia enterocolitica strains. The IVSs in Y enterocolitica and Salmonella typhimurium have a common origin , 1991, Molecular microbiology.

[26]  H. Seifert,et al.  Frequency of Pilin Antigenic Variation inNeisseria gonorrhoeae , 1998, Journal of bacteriology.

[27]  R. Leclercq,et al.  High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. , 2003, The Journal of infectious diseases.

[28]  I. Kobayashi,et al.  Evidence for the double-strand break repair model of bacteriophage lambda recombination. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. Seifert,et al.  Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair , 1998, Molecular microbiology.

[30]  P. Bork,et al.  Evolution of tuf genes: ancient duplication, differential loss and gene conversion , 2001, FEBS letters.

[31]  I. Kobayashi,et al.  Apparent gene conversion in an Escherichia coli rec+ strain is explained by multiple rounds of reciprocal crossing-over , 1988, Molecular and General Genetics MGG.

[32]  W. Heyer.  Recombination: Holliday Junction Resolution and Crossover Formation , 2004, Current Biology.

[33]  J. Gogarten,et al.  Orthologs, paralogs and genome comparisons. , 1999, Current opinion in genetics & development.

[34]  P. Alifano,et al.  Phenotypes of a Naturally Defective recB Allele in Neisseria meningitidis Clinical Isolates , 2002, Infection and Immunity.

[35]  F. Taddei,et al.  Highly variable mutation rates in commensal and pathogenic Escherichia coli. , 1997, Science.

[36]  F. Taddei,et al.  Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut , 2001, Science.

[37]  S. Sawyer.  Statistical tests for detecting gene conversion. , 1989, Molecular biology and evolution.

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

[39]  A. Clark.  rec genes and homologous recombination proteins in Escherichia coli. , 1991, Biochimie.

[40]  I. Kobayashi,et al.  Double-stranded gap repair of DNA by gene conversion in Escherichia coli. , 1988, Genetics.

[41]  D. Hughes,et al.  Evidence against reciprocal recombination as the basis for tuf gene conversion in Salmonella enterica serovar Typhimurium. , 2004, Journal of molecular biology.

[42]  B. Molini,et al.  Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection , 2004, Molecular microbiology.

[43]  A. Koren,et al.  Control of meiotic recombination initiation: a role for the environment? , 2002, Current Genetics.

[44]  Eric P. Skaar,et al.  Recombination, repair and replication in the pathogenic Neisseriae: the 3 R′s of molecular genetics of two human‐specific bacterial pathogens , 2003, Molecular microbiology.

[45]  G. Drouin,et al.  Detecting and characterizing gene conversions between multigene family members. , 1999, Molecular biology and evolution.

[46]  J. Roth,et al.  Reciprocality of recombination events that rearrange the chromosome. , 1988, Genetics.

[47]  Markus Landthaler,et al.  Group I Intron Homing in Bacillus Phages SPO1 and SP82: a Gene Conversion Event Initiated by a Nicking Homing Endonuclease , 2004, Journal of bacteriology.

[48]  P. Markham,et al.  Multigene Families Encoding the Major Hemagglutinins in Phylogenetically Distinct Mycoplasmas , 1998, Infection and Immunity.

[49]  S. Lovett,et al.  Crossing over between regions of limited homology in Escherichia coli. RecA-dependent and RecA-independent pathways. , 2002, Genetics.

[50]  I. Kobayashi,et al.  Evidence for conservative (two-progeny) DNA double-strand break repair. , 1995, Genetics.

[51]  Stephen C. West,et al.  Molecular views of recombination proteins and their control , 2003, Nature Reviews Molecular Cell Biology.

[52]  R Palacios,et al.  Gene amplification and genomic plasticity in prokaryotes. , 1997, Annual review of genetics.

[53]  M. Syvanen,et al.  Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[54]  G. Paul,et al.  Inhibitor-resistant TEM beta-lactamases: phenotypic, genetic and biochemical characteristics. , 1999, The Journal of antimicrobial chemotherapy.

[55]  D. Knowles,et al.  Efficient use of a small genome to generate antigenic diversity in tick-borne ehrlichial pathogens , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  D. Piñero,et al.  Reiterated DNA sequences in Rhizobium and Agrobacterium spp , 1987, Journal of bacteriology.

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

[58]  T. Allers,et al.  Differential Timing and Control of Noncrossover and Crossover Recombination during Meiosis , 2001, Cell.

[59]  Eric P. Skaar,et al.  Roles of the recJ and recN Genes in Homologous Recombination and DNA Repair Pathways of Neisseria gonorrhoeae , 2002, Journal of bacteriology.

[60]  D. Hartl,et al.  Horizontal acquisition of divergent chromosomal DNA in bacteria: effects of mutator phenotypes. , 2003, Genetics.

[61]  R. Holliday.  A mechanism for gene conversion in fungi. , 1964, Genetical research.

[62]  P. Markham,et al.  A novel mechanism for control of antigenic variation in the haemagglutinin gene family of Mycoplasma synoviae , 2000, Molecular microbiology.

[63]  I. Kobayashi,et al.  Orientation dependence in homologous recombination. , 1996, Genetics.

[64]  M. Chaussee,et al.  Characterization of the recD gene of Neisseria gonorrhoeae MS11 and the effect of recD inactivation on pilin variation and DNA transformation. , 1999, Microbiology.

[65]  I. Kobayashi,et al.  Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model. , 1992, Advances in biophysics.

[66]  F. Stahl.  Meiotic Recombination in Yeast: Coronation of the Double-Strand-Break Repair Model , 1996, Cell.

[67]  M. Blaser,et al.  Concerted evolution between duplicated genetic elements in Helicobacter pylori. , 2002, Journal of molecular biology.

[68]  Archana Belle,et al.  Intronless homing: site-specific endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. , 2002, Genes & development.

[69]  K. Sanderson,et al.  Salmonella typhimurium LT2 possesses three distinct 23S rRNA intervening sequences , 1996, Journal of bacteriology.

[70]  E. Koonin,et al.  Gene conversions in genes encoding outer-membrane proteins in H. pylori and C. pneumoniae. , 2001, Trends in genetics : TIG.

[71]  F. Taddei,et al.  Role of mutator alleles in adaptive evolution , 1997, Nature.

[72]  J. Cannon,et al.  Antigenic variation of gonococcal pilin expression in vivo: analysis of the strain FA1090 pilin repertoire and identification of the pilS gene copies recombining with pilE during experimental human infection. , 2001, Microbiology.

[73]  W. Broughton,et al.  Prediction, identification, and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[74]  M. Radman,et al.  Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[76]  S. Maloy,et al.  Inactivation of mismatch repair overcomes the barrier to transduction between Salmonella typhimurium and Salmonella typhi , 1994, Journal of bacteriology.

[77]  Jack W. Szostak,et al.  The double-strand-break repair model for recombination , 1983, Cell.

[78]  K. Sanderson,et al.  Intervening Sequences in rrl Genes and Fragmentation of 23S rRNA in Genera of the FamilyEnterobacteriaceae , 2001, Journal of bacteriology.

[79]  I. Kobayashi,et al.  Accumulation of large non-circular forms of the chromosome in recombination-defective mutants of Escherichia coli , 2003, BMC Molecular Biology.

[80]  J. Donelson,et al.  Mechanisms of Antigenic Variation in Borrelia hermsii and African Trypanosomes (*) , 1995, The Journal of Biological Chemistry.

[81]  Archana Belle,et al.  SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. , 2003, Journal of molecular biology.

[82]  I. Kobayashi,et al.  Genetic analysis of double-strand break repair in Escherichia coli , 1993, Journal of bacteriology.

[83]  H. Seifert,et al.  The recX gene potentiates homologous recombination in Neisseria gonorrhoeae , 2001, Molecular microbiology.

[84]  S. Norris,et al.  Genetic Variation of the Borrelia burgdorferi Gene vlsE Involves Cassette-Specific, Segmental Gene Conversion , 1998, Infection and Immunity.

[85]  L. N. Ornston,et al.  Influence of the catBCE sequence on the phenotypic reversion of a pcaE mutation in Acinetobacter calcoaceticus , 1987, Journal of bacteriology.

[86]  Anna Malkova,et al.  Srs2 and Sgs1–Top3 Suppress Crossovers during Double-Strand Break Repair in Yeast , 2003, Cell.

[87]  T. Meyer,et al.  The repertoire of silent pilus genes in neisseria gonorrhoeae: Evidence for gene conversion , 1986, Cell.

[88]  A. Segall,et al.  Approaches to half-tetrad analysis in bacteria: recombination between repeated, inverse-order chromosomal sequences. , 1994, Genetics.

[89]  C. Quinto,et al.  Nitrogenase reductase: A functional multigene family in Rhizobium phaseoli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[90]  R. Reenan,et al.  Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. , 1994, Genetics.

[91]  T. Petes,et al.  Meiotic recombination hot spots and cold spots , 2001, Nature Reviews Genetics.

[92]  K. Marians.  Mechanisms of replication fork restart in Escherichia coli. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[93]  M. Koomey,et al.  Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[94]  A. Barbour,et al.  Antigen diversity in the bacterium B. hermsii through “Somatic” mutations in rearranged vmp genes , 1994, Cell.

[95]  C. Rodríguez,et al.  Multiple recombination events maintain sequence identity among members of the nitrogenase multigene family in Rhizobium etli. , 1998, Genetics.

[96]  P. Awadalla.  The evolutionary genomics of pathogen recombination , 2003, Nature Reviews Genetics.

[97]  T. Meyer,et al.  Silent pilin genes of Neisseria gonorrhoeae MS11 and the occurrence of related hypervariant sequences among other gonococcal isolates , 1992, Molecular microbiology.

[98]  C. Higgins,et al.  Repetitive extragenic palindromic sequences, mRNA stability and gene expression: evolution by gene conversion? A review. , 1988, Gene.

[99]  S. Chávez,et al.  Mitotic recombination in yeast: elements controlling its incidence , 2000, Yeast.

[100]  C. Quinto,et al.  Reiteration of nitrogen fixation gene sequences in Rhizobium phaseoli , 1982, Nature.

[101]  D. Hughes,et al.  Homologous recombination between the tuf genes of Salmonella typhimurium. , 1996, Journal of molecular biology.

[102]  I. Kobayashi,et al.  Gene conversion in the Escherichia coli RecF pathway: a successive half crossing-over model , 1992, Molecular and General Genetics MGG.

[103]  F. Prado,et al.  Mitotic recombination in Saccharomyces cerevisiae , 2002, Current Genetics.

[104]  Molecular drive. , 2002, Science.

[105]  W. Brown,et al.  Emergence of Anaplasma marginaleAntigenic Variants during Persistent Rickettsemia , 1999, Infection and Immunity.

[106]  Diarmaid Hughes,et al.  Evaluating genome dynamics: the constraints on rearrangements within bacterial genomes , 2000, Genome Biology.

[107]  G. Kowalchuk,et al.  Nucleotide sequences transferred by gene conversion in the bacterium Acinetobacter calcoaceticus. , 1995, Gene.

[108]  M S Meselson,et al.  A general model for genetic recombination. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[109]  J. Roth,et al.  Role of recBC function in formation of chromosomal rearrangements: a two-step model for recombination. , 1989, Genetics.

[110]  S. Norris,et al.  Antigenic Variation in Lyme Disease Borreliae by Promiscuous Recombination of VMP-like Sequence Cassettes , 1997, Cell.

[111]  R. Meinersmann,et al.  Concerted evolution of duplicate fla genes in Campylobacter. , 2000, Microbiology.

[112]  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.

[113]  P. Carter,et al.  Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme , 1997, Journal of clinical microbiology.

[114]  S. Bergström,et al.  Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. , 1987, Genetics.