DNA secretion and gene-level selection in bacteria Free

Abstract

Natural genetic transformation can facilitate gene transfer in many genera of bacteria and requires the presence of extracellular DNA. Although cell lysis can contribute to this extracellular DNA pool, several studies have suggested that the secretion of DNA from living bacteria may also provide genetic material for transformation. This paper reviews the evidence for specific secretion of DNA from intact bacteria into the extracellular environment and examines this behaviour from a population-genetics perspective. A mathematical model demonstrates that the joint action of DNA secretion and transformation creates a novel type of gene-level natural selection. This model demonstrates that gene-level selection could explain the existence of DNA secretion mechanisms that provide no benefit to individual cells or populations of bacteria. Additionally, the model predicts that any trait affecting DNA secretion will experience selection at the gene level in a transforming population. This analysis confirms that the secretion of DNA from intact bacterial cells is fully explicable with evolutionary theory, and reveals a novel mechanism for bacterial evolution.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29013-0
2006-09-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/9/2683.html?itemId=/content/journal/micro/10.1099/mic.0.29013-0&mimeType=html&fmt=ahah

References

  1. Bergstrom C. T, Lipsitch M, Levin B. R. 2000; Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505–1519
    [Google Scholar]
  2. Borenstein S, Ephrati-Elizur E. 1969; Spontaneous release of DNA in sequential genetic order by Bacillus subtilis . J Mol Biol 45:137–152 [CrossRef]
    [Google Scholar]
  3. Bulygina L. G, Prozorov A. A. 1973; Mutants of Bacillus subtilis with modified DNA donor ability in spontaneous transformation. 4. Study of relation of transformability and donor activity. Genetika 9:91–96
    [Google Scholar]
  4. Catlin B. W. 1956; Extracellular deoxyribonucleic acid of bacteria and a deoxyribonuclease inhibitor. Science 124:441–442 [CrossRef]
    [Google Scholar]
  5. Catlin B. W. 1960; Transformation of Neisseria meningitidis by deoxyribonucleates from cells and from culture slime. J Bacteriol 79:579–590
    [Google Scholar]
  6. de Vries J., Wackernagel W. 2004; Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266:91–104
    [Google Scholar]
  7. Hamilton H. L, Dominguez N. M, Schwartz K. J, Hackett K. T, Dillard J. P. 2005; Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55:1704–1721 [CrossRef]
    [Google Scholar]
  8. Hara T, Ueda S. 1981; A study on the mechanism of DNA excretion from P. aeruginosa Kyu-1 – effect of mitomycin-C on extracellular DNA production. Agric Biol Chem 45:2457–2461 [CrossRef]
    [Google Scholar]
  9. Hendrickx L, Hausner M, Wuertz S. 2003; Natural genetic transformation in monoculture Acinetobacter sp. strain BD413 biofilms. Appl Environ Microbiol 69:1721–1727 [CrossRef]
    [Google Scholar]
  10. Lamb B. C, Helmi S. 1982; The extent to which gene conversion can change allele frequencies in populations. Genet Res 39:199–217 [CrossRef]
    [Google Scholar]
  11. Li Y. H, Lau P. C. Y, Lee J. H, Ellen R. P, Cvitkovitch D. G. 2001; Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897–908 [CrossRef]
    [Google Scholar]
  12. Lorenz M. G, Wackernagel W. 1994; Bacterial gene-transfer by natural genetic-transformation in the environment. Microbiol Rev 58:563–602
    [Google Scholar]
  13. Lorenz M. G, Gerjets D, Wackernagel W. 1991; Release of transforming plasmid and chromosomal DNA from two cultured soil bacteria. Arch Microbiol 156:319–326 [CrossRef]
    [Google Scholar]
  14. Marais G. 2003; Biased gene conversion: implications for genome and sex evolution. Trends Genet 19:330–338 [CrossRef]
    [Google Scholar]
  15. Molin S, Tolker-Nielsen T. 2003; Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261 [CrossRef]
    [Google Scholar]
  16. Nagylaki T. 1983; Evolution of a large population under gene conversion. Proc Natl Acad Sci U S A 80:5941–5945 [CrossRef]
    [Google Scholar]
  17. Ottolenghi E, Hotchkiss R. D. 1962; Release of genetic transforming agent from pneumococcal cultures during growth and disintegration. J Exp Med 116:491–519 [CrossRef]
    [Google Scholar]
  18. Shapiro J. A. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104 [CrossRef]
    [Google Scholar]
  19. Sinha R. P, Iyer V. N. 1971; Competence for genetic transformation and the release of DNA from Bacillus subtilis . Biochim Biophys Acta 232:61–71 [CrossRef]
    [Google Scholar]
  20. Smithies W. R, Gibbons N. E. 1955; The deoxyribose nucleic acid slime layer of some halophilic bacteria. Can J Microbiol 1:614–621 [CrossRef]
    [Google Scholar]
  21. Steinmoen H, Knutsen E, Havarstein L. S. 2002; Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc Natl Acad Sci U S A 99:7681–7686 [CrossRef]
    [Google Scholar]
  22. Stewart G. J, Carlson C. A. 1986; The biology of natural transformation. Annu Rev Microbiol 40:211–235 [CrossRef]
    [Google Scholar]
  23. Stewart G. J, Carlson C. A, Ingraham J. L. 1983; Evidence for an active role of donor cells in natural transformation of Pseudomonas stutzeri . J Bacteriol 156:30–35
    [Google Scholar]
  24. Streips U. N, Young F. E. 1974; Transformation in Bacillus subtilis using excreted DNA. Mol Gen Genet 133:47–55 [CrossRef]
    [Google Scholar]
  25. Takahashi I. 1962; Genetic transformation of Bacillus subtilis by extracellular DNA. Biochem Biophys Res Commun 7:467–470 [CrossRef]
    [Google Scholar]
  26. Teske A. P, Stahl D. 2002; Microbial mats and biofilms: evolution, structure, and function of fixed microbial communities. In Biodiversity of Microbial Life: Foundations of Earth's Biosphere pp  49–100 Edited by Staley J. T., Reysenbach A. L. New York: Wiley-Liss;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29013-0
Loading
/content/journal/micro/10.1099/mic.0.29013-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed