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Do bacteria have sex?

Nature Reviews Genetics volume 2, pages 634–639 (2001)Cite this article

Abstract

Do bacteria have genes for genetic exchange? The idea that the bacterial processes that cause genetic exchange exist because of natural selection for this process is shared by almost all microbiologists and population geneticists. However, this assumption has been perpetuated by generations of biology, microbiology and genetics textbooks without ever being critically examined.

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Figure 1: Genetic exchange in bacteria.
Figure 2: The role of RuvC in DNA replication and recombination.
Figure 3: Methods of DNA transfer.

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References

  1. Kondrashov, A. S. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84, 372–387 (1993).

    Article  CAS  PubMed  Google Scholar 

  2. Lenormand, T. & Otto, S. P. The evolution of recombination in a heterogeneous environment. Genetics 156, 423–438 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Lawrence, J. G. & Ochman, H. Molecular archaeology of the Escherichia coli genome. Proc. Natl Acad. Sci. USA 95, 9413–9417 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Burt, A. Perspective: sex, recombination, and the efficacy of selection — was Weismann right? Evolution 54, 337–351 (2000).

    CAS  PubMed  Google Scholar 

  6. West, S. A., Lively, C. M. & Read, A. F. A pluralist approach to sex and recombination. J. Evol. Biol. 12, 1003–1012 (1999).

    Article  Google Scholar 

  7. Papadopoulos, D. et al. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl Acad. Sci. USA 96, 3807–3812 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Redfield, R. J. Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? Genetics 119, 213–221 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Redfield, R., Schrag, M. & Dean, A. The evolution of bacterial transformation: sex with poor relations. Genetics 146, 27–38 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Tenaillon, O., Le Nagard, H., Godelle, B. & Taddei, F. Mutators and sex in bacteria: conflict between adaptive strategies. Proc. Natl Acad. Sci. USA 97, 10465–10470 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Souza, V., Turner, P. E. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. 5. Effects of recombination with immigrant genotypes on the rate of bacterial evolution. J. Evol. Biol. 10, 743–769 (1997).

    Article  Google Scholar 

  12. Cox, M. M. Recombinational DNA repair in bacteria and the RecA protein. Prog. Nucleic Acid Res. Mol. Biol. 63, 311–366 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Cox, M. M. et al. The importance of repairing stalled replication forks. Nature 404, 37–41 (2000).

    Article  CAS  PubMed  Google Scholar 

  14. Kuzminov, A. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16, 373–384 (1995).

    Article  CAS  PubMed  Google Scholar 

  15. Vincent, S. D., Mahdi, A. A. & Lloyd, R. G. The RecG branch migration protein of Escherichia coli dissociates R-loops. J. Mol. Biol. 264, 713–721 (1996).

    Article  CAS  PubMed  Google Scholar 

  16. Seigneur, M., Bidnenko, V., Ehrlich, S. D. & Michel, B. RuvAB acts at arrested replication forks. Cell 95, 419–430 (1998).

    Article  CAS  PubMed  Google Scholar 

  17. Lloyd, R. G. Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG. J. Bacteriol. 173, 5414–5418 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Milkman, R. et al. Molecular evolution of the Escherichia coli chromosome V. Recombination patterns among strains of diverse origin. Genetics 153, 539–554 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Sternberg, N. L. & Maurer, R. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 204, 18–43 (1991).

    Article  CAS  PubMed  Google Scholar 

  20. Vogel, W. & Schmieger, H. Selection of bacterial pac sites recognized by Salmonella phage P22. Mol. Gen. Genet. 205, 563–567 (1986).

    Article  CAS  PubMed  Google Scholar 

  21. Frost, L. S. Bacterial conjugation: everybody's doin' it. Can. J. Microbiol. 38, 1091–1096 (1992).

    Article  CAS  PubMed  Google Scholar 

  22. Solomon, J. M. & Grossman, A. D. Who's competent when: regulation of natural genetic competence in bacteria. Trends Genet. 12, 150–155 (1996).

    Article  CAS  PubMed  Google Scholar 

  23. Dubnau, D. DNA uptake in bacteria. Annu. Rev. Microbiol. 53, 217–244 (1999).

    Article  CAS  PubMed  Google Scholar 

  24. Levin, B. R. & Bergstrom, C. T. Bacteria are different: observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes. Proc. Natl Acad. Sci. USA 97, 6981–6985 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mortier-Barriere, I., Humbert, O., Martin, B., Prudhomme, M. & Claverys, J. P. Control of recombination rate during transformation of Streptococcus pneumoniae: an overview. Microb. Drug Resist. 3, 233–242 (1997).

    Article  CAS  PubMed  Google Scholar 

  26. Michod, R. E., Wojciechowski, M. & Hoelzer, M. DNA repair and the evolution of transformation in the bacterium Bacillus subtilis. Genetics 118, 31–39 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Wojciechowski, M. F., Hoelzer, M. A. & Michod, R. E. DNA repair and the evolution of transformation in Bacillus subtilis. II. Role of inducible repair. Genetics 121, 411–422 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Hoelzer, M. A. & Michod, R. E. DNA repair and the evolution of transformation in Bacillus subtilis. III. Sex with damaged DNA. Genetics 128, 215–223 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Redfield, R. J. Evolution of natural transformation: testing the DNA repair hypothesis in Bacillus subtilis and Haemophilus influenzae. Genetics 133, 755–761 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Redfield, R. J. Genes for breakfast: the have your cake and eat it too of transformation. J. Hered. 84, 400–404 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. Stouthamer, A. H. The search for correlation between theoretical and experimental growth yields. Int. Rev. Biochem. 21, 1–47 (1979).

    CAS  Google Scholar 

  32. Matthews, L., Spector, S., Lemm, J. & Potter, J. Studies on pulmonary secretions. 1. The overall chemical composition of pulmonary secretions from patients with cystic fibrosis, bronchiectasis and laryngectomy. Am. Rev. Respir. Dis. 88, 199–204 (1963).

    CAS  PubMed  Google Scholar 

  33. Hunt, J. N., Smith, J. L., Jiang, C. & Kessler, M. S. Effect of synthetic prostaglandin E1 analog on aspirin-induced gastric bleeding and secretion. Dig. Dis. Sci. 28, 897–902 (1983).

    Article  CAS  PubMed  Google Scholar 

  34. Blum, S. A. E., Lorenz, M. G. & Wackernagel, W. Mechanism of retarded DNA degradation and prokaryotic origin of DNases in nonsterile soils. Syst. Appl. Microbiol. 20, 513–521 (1997).

    Article  CAS  Google Scholar 

  35. Pifer, M. L. & Smith, H. O. Processing of donor DNA during Haemophilus influenzae transformation: analysis using a model plasmid system. Proc. Natl Acad. Sci. USA 82, 3731–3735 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Dorocicz, I., Williams, P. & Redfield, R. J. The Haemophilus influenzae adenylate cyclase gene: cloning, sequence and essential role in competence. J. Bacteriol. 175, 7142–7149 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Macfadyen, L. P., Dorocicz, I. R., Reizer, J., Saier, M. H. Jr & Redfield, R. J. Regulation of competence development and sugar utilization in Haemophilus influenzae Rd by a phosphoenolpyruvate:fructose phosphotransferase system. Mol. Microbiol. 21, 941–952 (1996).

    Article  CAS  PubMed  Google Scholar 

  38. Macfadyen, L. P. Regulation of Intracellular cAMP Levels and Competence Development in Haemophilus influenzae by a Phosphoenolpyruvate:Fructose Phosphotransferase System. Ph.D. thesis, Department of Zoology, University of British Columbia, British Columbia, Canada (1999).

    Google Scholar 

  39. Macfadyen, L. P. et al. Competence development by Haemophilus influenzae is regulated by the availability of nucleic acid precursors. Mol. Microbiol. 40, 700–707 (2001).

    Article  CAS  PubMed  Google Scholar 

  40. Hauser, P. M. & Karamata, D. A rapid and simple method for Bacillus subtilis transformation on solid media. Microbiology 140, 1613–1617 (1994).

    Article  CAS  PubMed  Google Scholar 

  41. Serror, P. & Sonenshein, A. L. CodY is required for nutritional repression of Bacillus subtilis genetic competence. J. Bacteriol. 178, 5910–5915 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Frisby, D. & Zuber, P. Mutations in pts cause catabolite-resistant sporulation and altered regulation of spo0H in Bacillus subtilis. J. Bacteriol. 176, 2587–2595 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kunst, F., Msadek, T., Bignon, J. & Rapoport, G. The DegS/DegU and ComP/ComA two-component systems are part of a network controlling degradative enzyme synthesis and competence in Bacillus subtilis. Res. Microbiol. 145, 393–402 (1994).

    Article  CAS  PubMed  Google Scholar 

  44. Inamine, G. S. & Dubnau, D. ComEA, a Bacillus subtilis integral membrane protein required for genetic transformation, is needed for both DNA binding and transport. J. Bacteriol. 177, 3045–3051 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Porstendorfer, D., Gohl, O., Mayer, F. & Averhoff, B. ComP, a pilin-like protein essential for natural competence in Acinetobacter sp. strain BD413: regulation, modification, and cellular localization. J. Bacteriol. 182, 3673–3680 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Tortosa, P. & Dubnau, D. Competence for transformation: a matter of taste. Curr. Opin. Microbiol. 2, 588–592 (1999).

    Article  CAS  PubMed  Google Scholar 

  47. Morrison, D. A. & Lee, M. S. Regulation of competence for genetic transformation in Streptococcus pneumoniae: a link between quorum sensing and DNA processing genes. Res. Microbiol. 151, 445–451 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. Swift, S., Throup, J. P., Williams, P., Salmond, G. P. & Stewart, G. S. Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem. Sci. 21, 214–219 (1996).

    Article  CAS  PubMed  Google Scholar 

  49. Macfadyen, L. P. Regulation of competence development in Haemophilus influenzae. J. Theor. Biol. 207, 349–359 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Rimini, R. et al. Global analysis of transcription kinetics during competence development in Streptococcus pneumoniae using high density DNA arrays. Mol. Microbiol. 36, 1279–1292 (2000).

    Article  CAS  PubMed  Google Scholar 

  51. Lang, A. S. & Beatty, J. T. Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc. Natl Acad. Sci. USA 97, 859–864 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lang, A. S. & Beatty, J. T. The gene transfer agent of Rhodobacter capsulatus and 'constitutive transduction' in prokaryotes. Arch. Microbiol. 175, 241–249 (2001).

    Article  CAS  PubMed  Google Scholar 

  53. Horiuchi, T. & Fujimura, Y. Recombinational rescue of the stalled DNA replication fork: a model based on analysis of an Escherichia coli strain with a chromosome region difficult to replicate. J. Bacteriol. 177, 783–791 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Weismann, A. Die Bedeutung der sexuellen Fortpflanzung fur die Selektiontheorie (Gustav Fischer, Jena, 1886).

    Google Scholar 

  55. Redfield, R. J. A truly pluralistic view of sex and recombination. J. Evol. Biol. 12, 1043–1046 (1999).

    Article  Google Scholar 

  56. Drake, J. W. The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Ann. NY Acad. Sci. 870, 100–107 (1999).

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Zoology, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Rosemary J. Redfield

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  1. Rosemary J. Redfield
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Related links

Related links

DATABASE LINKS

RecA

Rec

RecE

RecF

RecG

RecJ

RecN

RecO

RecQ

RuvABC

SSB

PolA

DNA ligase

DNA gyrase

CodY

PtsG

comEA

comEC

comEB

FURTHER INFORMATION

Salmonella

Escherichia coli

Redfield lab

Glossary

CATABOLITE REPRESSION

Transcriptional repression of a prokaryotic operon by the metabolic products of the enzymes that are encoded by the operon.

CONJUGATION

In prokaryotes, transfer of DNA from a donor cell to a recipient cell is mediated by direct cell–cell contact.

CONSPECIFICS

Members of the same species.

FITNESS

A measure of the capacity of an organism to survive and reproduce.

HOLLIDAY JUNCTIONS

Cross-shaped junctions at which four strands of DNA meet and exchange partners, an important intermediate of recombination.

HORIZONTAL TRANSFER

Acquisition of genetic information from another cell.

OPERON

A genetic unit or cluster that consists of one or more genes that are transcribed as a unit and are expressed in a coordinated manner.

PROPHAGE

An inactive bacteriophage genome integrated into the host genome.

PROTISTS

Single-celled eukaryotes.

QUORUM-SENSING PEPTIDES

Peptides secreted and detected by cells. Cells respond to extracellular peptide only when cell densities are sufficiently high (the 'quorum state') that the extracellular concentration of the peptide exceeds a threshold.

REC PROTEINS

A general class of protein that participates in recombination.

RECOMBINATIONAL REPAIR

DNA repair made possible when a damaged DNA strand base-pairs with a complementary undamaged strand from a different molecule.

RUV PROTEINS

Proteins that translocate and resolve Holliday junctions.

TRANSDUCTION

Virus- or phage-mediated introduction into a cell of a DNA fragment derived from a different cell.

TRANSFORMATION

Change of the genotype of a cell brought about by uptake of free DNA.

TRANSPOSASE

An enzyme that carries out the site-specific DNA recombination required for transposition.

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Redfield, R. Do bacteria have sex?. Nat Rev Genet 2, 634–639 (2001). https://doi.org/10.1038/35084593

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