UV-inducible DNA exchange in hyperthermophilic archaea mediated by type IV pili

Molecular Microbiology

Volumn 82, Issue 4, 2011, Pages 807-817

  Ajon, Małgorzata ^a   Fröls, Sabrina ^b,e   van Wolferen, Marleen ^c   Stoecker, Kilian ^b,f   Teichmann, Daniela ^b   Driessen, Arnold J M ^a   Grogan, Dennis W ^d   Albers, Sonja Verena ^c   Schleper, Christa ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF VIENNA   (Austria)

^c MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^d UNIVERSITY OF CINCINNATI   (United States)

^e DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^f FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM PILUS; CELL AGGREGATION; CELL SURVIVAL; CHROMOSOME MARKER; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA TRANSFER; FLUORESCENCE IN SITU HYBRIDIZATION; GENE INACTIVATION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; SPECIES DIFFERENCE; SULFOLOBALES; SULFOLOBUS ACIDOCALDARIUS; SULFOLOBUS SOLFATARICUS; SULFOLOBUS TOKODAII; ULTRAVIOLET RADIATION;

BIOLOGICAL TRANSPORT; DNA, ARCHAEAL; GENE TRANSFER, HORIZONTAL; IN SITU HYBRIDIZATION, FLUORESCENCE; RECOMBINATION, GENETIC; SULFOLOBUS;

CRENARCHAEOTA; EUKARYOTA; SULFOLOBALES; SULFOLOBUS; SULFOLOBUS ACIDOCALDARIUS;

EID: 80855131627     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07861.x     Document Type: Article

References (44)

1. Albers, S.V., and Pohlschroder, M. (2009) Diversity of archaeal type IV pilin-like structures. Extremophiles 13: 403-410.
2. Ayers, M., Howell, P.L., and Burrows, L.L. (2010) Architecture of the type II secretion and type IV pilus machineries. Future Microbiol 5: 1203-1218.
3. Bonura, T., and Smith, K.C. (1975) Enzymatic production of deoxyribonucleic acid double-strand breaks after ultraviolet irradiation of Escherichia coli K-12. J Bacteriol 121: 511-517.
4. Boudsocq, F., Iwai, S., Hanaoka, F., and Woodgate, R. (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta. Nucleic Acids Res 29: 4607-4616.
5. Brock, T.D., Brock, K.M., Belly, R.T., and Weiss, R.L. (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Microbiol 84: 54-68.
6. Carter, M.Q., Chen, J., and Lory, S. (2010) The Pseudomonas aeruginosa pathogenicity island PAPI-1 is transferred via a novel type IV pilus. J Bacteriol 192: 3249-3258.
7. Chen, I., Christie, P.J., and Dubnau, D. (2005) The ins and outs of DNA transfer in bacteria. Science 310: 1456-1460.
8. Daims, H., Stoecker, K., and Wagner, M. (2005) Fluorescence in situ hybridization for the detection of prokaryotes. In Advanced Methods in Molecular Microbial Ecology. Osborn, A.M., and Smith, C.J. (eds). Abingdon, UK: Bios-Garland, pp. 213-239.
9. Delmas, S., Shunburne, L., Ngo, H.P., and Allers, T. (2009) Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination. PLoS Genet 5: e1000552.
10. Dudas, A., and Chovanec, M. (2004) DNA double-strand break repair by homologous recombination. Mutat Res 566: 131-167.
11. Eppley, J.M., Tyson, G.W., Getz, W.M., and Banfield, J.F. (2007) Genetic exchange across a species boundary in the archaeal genus ferroplasma. Genetics 177: 407-416.
12. Filloux, A. (2010) A variety of bacterial pili involved in horizontal gene transfer. J Bacteriol 192: 3243-3245.
13. Fröls, S., Gordon, P.M., Panlilio, M.A., Duggin, I.G., Bell, S.D., Sensen, C.W., and Schleper, C. (2007) Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage. J Bacteriol 189: 8708-8718.
14. Fröls, S., Ajon, M., Wagner, M., Teichmann, D., Zolghadr, B., Folea, M., etal. (2008) UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 70: 938-952.
15. Garinis, G.A., Mitchell, J.R., Moorhouse, M.J., Hanada, K., de Waard, H., Vandeputte, D., etal. (2005) Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J 24: 3952-3962.
16. Gotz, D., Paytubi, S., Munro, S., Lundgren, M., Bernander, R., and White, M.F. (2007) Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol 8: R220.
17. Grogan, D.W. (1996) Exchange of genetic markers at extremely high temperatures in the archaeon Sulfolobus acidocaldarius. J Bacteriol 178: 3207-3211.
18. Grogan, D.W. (2009) Homologous recombination in Sulfolobus acidocaldarius: genetic assays and functional properties. Biochem Soc Trans 37: 88-91.
19. Grogan, D.W., and Gunsalus, R.P. (1993) Sulfolobus acidocaldarius synthesizes UMP via a standard de novo pathway: results of biochemical-genetic study. J Bacteriol 175: 1500-1507.
20. Grogan, D.W., and Hansen, J.E. (2003) Molecular characteristics of spontaneous deletions in the hyperthermophilic archaeon Sulfolobus acidocaldarius. J Bacteriol 185: 1266-1272.
21. Grogan, D.W., Carver, G.T., and Drake, J.W. (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci USA 98: 7928-7933.
22. Hansen, J.E., Dill, A.C., and 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.
23. Kim, S.R., and Komano, T. (1997) The plasmid R64 thin pilus identified as a type IV pilus. J Bacteriol 179: 3594-3603.
24. Koerdt, A., Godeke, J., Berger, J., Thormann, K.M., and Albers, S.V. (2010) Crenarchaeal biofilm formation under extreme conditions. PLoS ONE 5: e14104.
25. Kondo, S., Yamagishi, A., and Oshima, T. (1991) Positive selection for uracil auxotrophs of the sulfur-dependent thermophilic archaebacterium Sulfolobus acidocaldarius by use of 5-fluoroorotic acid. J Bacteriol 173: 7698-7700.
26. Kurosawa, N., and Grogan, D.W. (2005) Homologous recombination of exogenous DNA with the Sulfolobus acidocaldarius genome: properties and uses. FEMS Microbiol Lett 253: 141-149.
27. McKenzie, R.L., Aucamp, P.J., Bais, A.F., Bjorn, L.O., and Ilyas, M. (2007) Changes in biologically-active ultraviolet radiation reaching the Earth's surface. Photochem Photobiol Sci 6: 218-231.
28. Martusewitsch, E., Sensen, C.W., and Schleper, C. (2000) High spontaneous mutation rate in the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by transposable elements. J Bacteriol 182: 2574-2581.
29. Papke, R.T., Koenig, J.E., Rodriguez-Valera, F., and Doolittle, W.F. (2004) Frequent recombination in a saltern population of Halorubrum. Science 306: 1928-1929.
30. Papke, R.T., Zhaxybayeva, O., Feil, E.J., Sommerfeld, K., Muise, D., and Doolittle, W.F. (2007) Searching for species in haloarchaea. Proc Natl Acad Sci USA 104: 14092-14097.
31. Quaiser, A., Constantinesco, F., White, M.F., Forterre, P., and Elie, C. (2008) The Mre11 protein interacts with both Rad50 and the HerA bipolar helicase and is recruited to DNA following gamma irradiation in the archaeon Sulfolobus acidocaldarius. BMC Mol Biol 9: 25.
32. Reilly, M.S., and Grogan, D.W. (2001) Characterization of intragenic recombination in a hyperthermophilic archaeon via conjugational DNA exchange. J Bacteriol 183: 2943-2946.
33. Reilly, M.S., and Grogan, D.W. (2002) Biological effects of DNA damage in the hyperthermophilic archaeon Sulfolobus acidocaldarius. FEMS Microbiol Lett 208: 29-34.
34. Rosenshine, I., Tchelet, R., and Mevarech, M. (1989) The mechanism of DNA transfer in the mating system of an archaebacterium. Science 245: 1387-1389.
35. Sakofsky, C.J., Runck, L.A., and Grogan, D.W. (2011) Sulfolobus mutants, generated via PCR products, which lack putative enzymes of UV photoproduct repair. Archaea 2011: 864015.
36. Schelert, J., Dixit, V., Hoang, V., Simbahan, J., Drozda, M., and Blum, P. (2004) Occurrence and characterization of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186: 427-437.
37. Schleper, C., Holz, I., Janekovic, D., Murphy, J., and Zillig, W. (1995) A multicopy plasmid of the extremely thermophilic archaeon Sulfolobus effects its transfer to recipients by mating. J Bacteriol 177: 4417-4426.
38. Schmidt, K.J., Beck, K.E., and Grogan, D.W. (1999) UV stimulation of chromosomal marker exchange in Sulfolobus acidocaldarius: implications for DNA repair, conjugation and homologous recombination at extremely high temperatures. Genetics 152: 1407-1415.
39. She, Q., Phan, H., Garrett, R.A., Albers, S.V., Stedman, K.M., and Zillig, W. (1998) Genetic profile of pNOB8 from Sulfolobus: the first conjugative plasmid from an archaeon. Extremophiles 2: 417-425.
40. Stedman, K.M., She, Q., Phan, H., Holz, I., Singh, H., Prangishvili, D., etal. (2000) pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota. J Bacteriol 182: 7014-7020.
41. Wagner, M., Berkner, S., Ajon, M., Driessen, A.J.M., Lipps, G., and Albers, S.V. (2009) Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus. Biochem Soc Trans 37: 97-101.
42. Whitaker, R.J., Grogan, D.W., and Taylor, J.W. (2005) Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol Biol Evol 22: 2354-2361.
43. White, M.F. (2003) Archaeal DNA repair: paradigms and puzzles. Biochem Soc Trans 31: 690-693.
44. Wood, E.R., Ghane, F., and Grogan, D.W. (1997) Genetic responses of the thermophilic archaeon Sulfolobus acidocaldarius to short-wavelength UV light. J Bacteriol 179: 5693-5698.