, Volume 134, Issue 2, pp 205–210 | Cite as

Mutation rate and genome reduction in endosymbiotic and free-living bacteria

  • Gabriel A. B. Marais
  • Alexandra Calteau
  • Olivier Tenaillon


Genome reduction has been considered the hallmark of endosymbiotic bacteria, such as endocellular mutualists or obligatory pathogens until it was found exactly the same in several free-living bacteria. In endosymbiotic bacteria genome reduction is mainly attributed to degenerative processes due to small population size. These cannot affect the free-living bacteria with reduced genomes because they are known to have very large population sizes. It has been proposed that selection for simplification drove genome reduction in these free-living bacteria. For at least one of them (Prochlorococcus), genome reduction is associated with accelerated evolution and we suggest an alternative hypothesis based on increase in mutation rate as the primary cause of genome reduction in free-living bacteria.


Bacterial genomics Error threshold Genome size Molecular evolution Mutation–selection balance 



We thank Siv Andersson, Vincent Daubin, and Eduardo Rocha and Pierre Alexis Gros for helpful comments on this manuscript. G.M. is a CNRS fellow, A.C. has a PhD fellowship from the French ministry of research and O.T. was funded by Agence Nationale de la Recherche grant (ANR-05JCJC0136-01).


  1. André JB, Godelle B (2006) The evolution of mutation rate in finite asexual populations. Genetics 172:611–626PubMedCrossRefGoogle Scholar
  2. Biebricher CK, Eigen M (2005) The error threshold. Virus Res 107:117–127PubMedCrossRefGoogle Scholar
  3. Coleman ML, Sullivan MB, Martiny AC et al (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311:1768–1770PubMedCrossRefGoogle Scholar
  4. Cox EC, Yanofsky C (1967) Altered base ratios in the DNA of an Escherichia coli mutator strain. Proc Natl Acad Sci USA 58:1895–1902PubMedCrossRefGoogle Scholar
  5. Dagan T, Blekhman R, Graur D (2006) The “domino theory” of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens. Mol Biol Evol 23:310–316PubMedCrossRefGoogle Scholar
  6. Dale C, Wang B, Moran N et al (2003) Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20:1188–1194PubMedCrossRefGoogle Scholar
  7. Denamur E, Lecointre G, Darlu P et al (2000) Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103:711–721PubMedCrossRefGoogle Scholar
  8. Dufresne A, Salanoubat M, Partensky F et al (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100:10020–10025PubMedCrossRefGoogle Scholar
  9. Dufresne A, Garczarek L, Partensky F (2005) Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6:R14PubMedCrossRefGoogle Scholar
  10. Eigen M (1971) Selforganization of matter and the evolution of macromolecules. Naturwissenschaften 64:465–523CrossRefGoogle Scholar
  11. Gerrish PJ, Colato A, Perelson AS et al (2007) Complete genetic linkage can subvert natural selection. Proc Natl Acad Sci USA 104:6266–6271PubMedCrossRefGoogle Scholar
  12. Giovannoni SJ, Tripp HJ, Givan S et al (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245PubMedCrossRefGoogle Scholar
  13. Haigh J (1978) The accumulation of deleterious genes in a population—Muller’s Ratchet. Theor Popul Biol 14:251–267PubMedCrossRefGoogle Scholar
  14. Itoh T, Martin W, Nei M (2002) Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA 99:12944–12948PubMedCrossRefGoogle Scholar
  15. Kurland CG, Andersson SG (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64:786–820PubMedCrossRefGoogle Scholar
  16. Lynch M (2006) The origins of eukaryotic gene structure. Mol Biol Evol 23:450–468PubMedCrossRefGoogle Scholar
  17. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404PubMedCrossRefGoogle Scholar
  18. Mackay WJ, Han S, Samson LD (1994) DNA alkylation repair limits spontaneous base substitution mutations in Escherichia coli. J Bacteriol 176:3224–3230PubMedGoogle Scholar
  19. Martiny AC, Coleman ML, Chisholm SW (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103:12552–12557PubMedCrossRefGoogle Scholar
  20. Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17:589–596PubMedCrossRefGoogle Scholar
  21. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583–586PubMedCrossRefGoogle Scholar
  22. Rocap G, Larimer FW, Lamerdin J et al (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047PubMedCrossRefGoogle Scholar
  23. Rocha EP, Danchin A (2002) Base composition bias might result from competition for metabolic resources. Trends Genet 18:291–294PubMedCrossRefGoogle Scholar
  24. Saumaa S, Tover A, Kasak L et al (2002) Different spectra of stationary-phase mutations in early-arising versus late-arising mutants of Pseudomonas putida: involvement of the DNA repair enzyme MutY and the stationary-phase sigma factor RpoS. J Bacteriol 184:6957–6965PubMedCrossRefGoogle Scholar
  25. Sniegowski PD, Gerrish PJ, Lenski RE (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature 387:703–705PubMedCrossRefGoogle Scholar
  26. Taddei F, Radman M, Maynard-Smith J et al (1997) Role of mutator alleles in adaptive evolution. Nature 387:700–702PubMedCrossRefGoogle Scholar
  27. Tenaillon O, Toupance B, Le Nagard H et al (1999) Mutators, population size, adaptive landscape the adaptation of asexual populations of bacteria. Genetics 152:485–493PubMedGoogle Scholar
  28. Tenaillon O, Le Nagard H, Godelle B et al (2000) Mutators and sex in bacteria: conflict between adaptive strategies. Proc Natl Acad Sci USA 97:10465–10470PubMedCrossRefGoogle Scholar
  29. Vulic M, Dionisio F, Taddei F et al (1997) Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc Natl Acad Sci USA 94:9763–9767PubMedCrossRefGoogle Scholar
  30. Wiehe T (2000) Model dependency of error thresholds: the role of fitness functions and contrasts between the finite and infinite sites models. Genetical Research 69:127–136CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Gabriel A. B. Marais
    • 1
  • Alexandra Calteau
    • 1
    • 2
  • Olivier Tenaillon
    • 3
    • 4
  1. 1.Université de Lyon; Université de Lyon 1; Centre National de la Recherche Scientifique, UMR5558, Laboratoire de Biométrie et Biologie évolutiveVilleurbanne CedexFrance
  2. 2.Commissariat à l’Energie Atomique (CEA), Direction des Sciences du Vivant, Institut de Génomique, Genoscope, Laboratoire de Génomique ComparativeEvry CedexFrance
  3. 3.Institut National de la Santé et de la Recherche Médicale; Universite Denis Diderot Paris 7, INSERM U722, Ecology and Evolution of MicroorganismsParis Cedex 18France
  4. 4.INSERM U722, Faculté de médecine Xavier BichatUniversité Paris 7ParisFrance

Personalised recommendations