1887

Abstract

Although homologous recombination (HR) is known to influence the structure, stability, and evolution of microbial genomes, few of its functional properties have been measured in cells of hyperthermophilic archaea. The present study manipulated various properties of the parental DNAs in high-resolution assays of transformation, and measured the impact on the efficiency and pattern of marker transfer to the recipient chromosome. The relative orientation of homologous sequences, the type and position of chromosomal mutation being replaced, and the length of DNA flanking the marked region all affected the efficiency, linkage, tract continuity, and other parameters of marker transfer. Effects predicted specifically by the classical reciprocal-exchange model of HR were not observed. One analysis observed only 90 % linkage between markers defined by adjacent bases; in another series of experiments, sequence divergence up to 4 % had no detectable impact on overall efficiency of HR or on the co-transfer of a distal non-selected marker. The effects of introducing DNA via conjugation, rather than transformation, were more difficult to assess, but appeared to increase co-transfer (i.e. linkage) of relatively distant non-selected markers. The results indicate that HR events between gene-sized duplex DNAs and the chromosome typically involve neither crossing over nor interference from a mismatch-activated anti-recombination system. Instead, the donor DNA may anneal to a transient chromosomal gap, as in the mechanism proposed for oligonucleotide-mediated transformation of and other micro-organisms.

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2013-09-01
2024-04-16
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References

  1. Ajon M., Fröls S., van Wolferen M., Stoecker K., Teichmann D., Driessen A. J., Grogan D. W., Albers S. V., Schleper C.( 2011). UV-inducible DNA exchange in hyperthermophilic archaea mediated by type IV pili. Mol Microbiol 82:807–817 [View Article][PubMed]
    [Google Scholar]
  2. Allers T., Lichten M.( 2001). Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57 [View Article][PubMed]
    [Google Scholar]
  3. Aylon Y., Kupiec M.( 2004). DSB repair: the yeast paradigm. DNA Repair (Amst) 3:797–815 [View Article][PubMed]
    [Google Scholar]
  4. Ayora S., Carrasco B., Cárdenas P. P., César C. E., Cañas C., Yadav T., Marchisone C., Alonso J. C.( 2011). Double-strand break repair in bacteria: a view from Bacillus subtilis.. FEMS Microbiol Rev 35:1055–1081 [View Article][PubMed]
    [Google Scholar]
  5. Bell J. S., McCulloch R.( 2003). Mismatch repair regulates homologous recombination, but has little influence on antigenic variation, in Trypanosoma brucei.. J Biol Chem 278:45182–45188 [View Article][PubMed]
    [Google Scholar]
  6. Brendel V., Brocchieri L., Sandler S. J., Clark A. J., Karlin S.( 1997). Evolutionary comparisons of RecA-like proteins across all major kingdoms of living organisms. J Mol Evol 44:528–541 [View Article][PubMed]
    [Google Scholar]
  7. Chen L., Brügger K., Skovgaard M., Redder P., She Q., Torarinsson E., Greve B., Awayez M., Zibat A.& other authors ( 2005). The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187:4992–4999 [View Article][PubMed]
    [Google Scholar]
  8. Constantinesco F., Forterre P., Koonin E. V., Aravind L., Elie C.( 2004). A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res 32:1439–1447 [View Article][PubMed]
    [Google Scholar]
  9. Datta A., Hendrix M., Lipsitch M., Jinks-Robertson S.( 1997). Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc Natl Acad Sci U S A 94:9757–9762 [View Article][PubMed]
    [Google Scholar]
  10. Elliott B., Richardson C., Winderbaum J., Nickoloff J. A., Jasin M.( 1998). Gene conversion tracts from double-strand break repair in mammalian cells. Mol Cell Biol 18:93–101[PubMed]
    [Google Scholar]
  11. Evans E., Alani E.( 2000). Roles for mismatch repair factors in regulating genetic recombination. Mol Cell Biol 20:7839–7844 [View Article][PubMed]
    [Google Scholar]
  12. Fujikane R., Ishino S., Ishino Y., Forterre P.( 2010). Genetic analysis of DNA repair in the hyperthermophilic archaeon, Thermococcus kodakaraensis.. Genes Genet Syst 85:243–257 [View Article][PubMed]
    [Google Scholar]
  13. Grogan D. W.( 1996). Exchange of genetic markers at extremely high temperatures in the archaeon Sulfolobus acidocaldarius. J Bacteriol 178:3207–3211[PubMed]
    [Google Scholar]
  14. Grogan D. W.( 2003). Cytosine methylation by the SuaI restriction-modification system: implications for genetic fidelity in a hyperthermophilic archaeon. J Bacteriol 185:4657–4661 [View Article][PubMed]
    [Google Scholar]
  15. Grogan D. W., Gunsalus R. P.( 1993). Sulfolobus acidocaldarius synthesizes UMP via a standard de novo pathway: results of biochemical-genetic study. J Bacteriol 175:1500–1507[PubMed]
    [Google Scholar]
  16. Grogan D. W., Rockwood J.( 2010). Discontinuity and limited linkage in the homologous recombination system of a hyperthermophilic archaeon. J Bacteriol 192:4660–4668 [View Article][PubMed]
    [Google Scholar]
  17. Grogan D. W., Stengel K. R.( 2008). Recombination of synthetic oligonucleotides with prokaryotic chromosomes: substrate requirements of the Escherichia coli/lambdaRed and Sulfolobus acidocaldarius recombination systems. Mol Microbiol 69:1255–1265 [View Article][PubMed]
    [Google Scholar]
  18. Haber J. E., Ira G., Malkova A., Sugawara N.( 2004). Repairing a double-strand chromosome break by homologous recombination: revisiting Robin Holliday’s model. Philos Trans R Soc Lond B Biol Sci 359:79–86 [View Article][PubMed]
    [Google Scholar]
  19. Hansen J. E., Dill A. C., Grogan D. W.( 2005). Conjugational genetic exchange in the hyperthermophilic archaeon Sulfolobus acidocaldarius: intragenic recombination with minimal dependence on marker separation. J Bacteriol 187:805–809 [View Article][PubMed]
    [Google Scholar]
  20. Hastings P. J., McGill C., Shafer B., Strathern J. N.( 1993). Ends-in vs. ends-out recombination in yeast. Genetics 135:973–980[PubMed]
    [Google Scholar]
  21. Kerr I. D., Wadsworth R. I., Cubeddu L., Blankenfeldt W., Naismith J. H., White M. F.( 2003). Insights into ssDNA recognition by the OB fold from a structural and thermodynamic study of Sulfolobus SSB protein. EMBO J 22:2561–2570 [View Article][PubMed]
    [Google Scholar]
  22. Kow Y. W., Bao G., Reeves J. W., Jinks-Robertson S., Crouse G. F.( 2007). Oligonucleotide transformation of yeast reveals mismatch repair complexes to be differentially active on DNA replication strands. Proc Natl Acad Sci U S A 104:11352–11357 [View Article][PubMed]
    [Google Scholar]
  23. Kreuzer K. N.( 2005). Interplay between DNA replication and recombination in prokaryotes. Annu Rev Microbiol 59:43–67 [View Article][PubMed]
    [Google Scholar]
  24. Kurosawa N., Grogan D. W.( 2005). Homologous recombination of exogenous DNA with the Sulfolobus acidocaldarius genome: properties and uses. FEMS Microbiol Lett 253:141–149 [View Article][PubMed]
    [Google Scholar]
  25. Kuzminov A.( 2001). DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc Natl Acad Sci U S A 98:8461–8468 [View Article][PubMed]
    [Google Scholar]
  26. Li G. M.( 2008). Mechanisms and functions of DNA mismatch repair. Cell Res 18:85–98 [View Article][PubMed]
    [Google Scholar]
  27. Li X. T., Costantino N., Lu L. Y., Liu D. P., Watt R. M., Cheah K. S., Court D. L., Huang J. D.( 2003). Identification of factors influencing strand bias in oligonucleotide-mediated recombination in Escherichia coli.. Nucleic Acids Res 31:6674–6687 [View Article][PubMed]
    [Google Scholar]
  28. Lovett S. T., Feschenko V. V.( 1996). Stabilization of diverged tandem repeats by mismatch repair: evidence for deletion formation via a misaligned replication intermediate. Proc Natl Acad Sci U S A 93:7120–7124 [View Article][PubMed]
    [Google Scholar]
  29. Maezato Y., Dana K., Blum P.( 2011). Engineering thermoacidophilic archaea using linear DNA recombination. Methods Mol Biol 765:435–445 [View Article][PubMed]
    [Google Scholar]
  30. Mao D., Grogan D. W.( 2012). Heteroduplex formation, mismatch resolution, and genetic sectoring during homologous recombination in the hyperthermophilic archaeon Sulfolobus acidocaldarius.. Front Microbiol 3:192 [View Article][PubMed]
    [Google Scholar]
  31. Michel B., Flores M. J., Viguera E., Grompone G., Seigneur M., Bidnenko V.( 2001). Rescue of arrested replication forks by homologous recombination. Proc Natl Acad Sci U S A 98:8181–8188 [View Article][PubMed]
    [Google Scholar]
  32. Mimitou E. P., Symington L. S.( 2009). DNA end resection: many nucleases make light work. DNA Repair (Amst) 8:983–995 [View Article][PubMed]
    [Google Scholar]
  33. Nickoloff J. A., Sweetser D. B., Clikeman J. A., Khalsa G. J., Wheeler S. L.( 1999). Multiple heterologies increase mitotic double-strand break-induced allelic gene conversion tract lengths in yeast. Genetics 153:665–679[PubMed]
    [Google Scholar]
  34. Opperman R., Emmanuel E., Levy A. A.( 2004). The effect of sequence divergence on recombination between direct repeats in Arabidopsis.. Genetics 168:2207–2215 [View Article][PubMed]
    [Google Scholar]
  35. Orr-Weaver T. L., Szostak J. W.( 1983). Yeast recombination: the association between double-strand gap repair and crossing-over. Proc Natl Acad Sci U S A 80:4417–4421 [View Article][PubMed]
    [Google Scholar]
  36. Prangishvili D. A., Vashakidze R. P., Chelidze M. G., Gabriadze I. Yu.( 1985). A restriction endonuclease SuaI from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius.. FEBS Lett 192:57–60 [View Article][PubMed]
    [Google Scholar]
  37. Reilly M. S., Grogan D. W.( 2001). Characterization of intragenic recombination in a hyperthermophilic archaeon via conjugational DNA exchange. J Bacteriol 183:2943–2946 [View Article][PubMed]
    [Google Scholar]
  38. Rolfsmeier M. L., Haseltine C. A.( 2010). The single-stranded DNA binding protein of Sulfolobus solfataricus acts in the presynaptic step of homologous recombination. J Mol Biol 397:31–45 [View Article][PubMed]
    [Google Scholar]
  39. Sakofsky C. J., Runck L. A., Grogan D. W.( 2011). Sulfolobus mutants, generated via PCR products, which lack putative enzymes of UV photoproduct repair.. Archaea 2011:864015 [View Article][PubMed]
    [Google Scholar]
  40. Trouiller B., Schaefer D. G., Charlot F., Nogué F.( 2006). MSH2 is essential for the preservation of genome integrity and prevents homeologous recombination in the moss Physcomitrella patens.. Nucleic Acids Res 34:232–242 [View Article][PubMed]
    [Google Scholar]
  41. Wagner M., Berkner S., Ajon M., Driessen A. J., Lipps G., Albers S. V.( 2009). Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus.. Biochem Soc Trans 37:97–101 [View Article][PubMed]
    [Google Scholar]
  42. Woese C. R., Kandler O., Wheelis M. L.( 1990). Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87:4576–4579 [View Article][PubMed]
    [Google Scholar]
  43. Zhang C., Guo L., Deng L., Wu Y., Liang Y., Huang L., She Q.( 2010). Revealing the essentiality of multiple archaeal pcna genes using a mutant propagation assay based on an improved knockout method. Microbiology 156:3386–3397 [View Article][PubMed]
    [Google Scholar]
  44. Zhang C., Tian B., Li S., Ao X., Dalgaard K., Gökce S., Liang Y., She Q.( 2013). Genetic manipulation in Sulfolobus islandicus and functional analysis of DNA repair genes. Biochem Soc Trans 41:405–410 [View Article][PubMed]
    [Google Scholar]
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