Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections

Journal of Bacteriology

Volumn 187, Issue 23, 2005, Pages 8047-8054

  Eltsov, Mikhail ^a   Dubochet, Jacques ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; CELL STRUCTURE; CRYOELECTRON MICROSCOPY; CYTOPLASM; DEINOCOCCUS RADIODURANS; DNA STRAND BREAKAGE; LIQUID CRYSTAL; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; TRANSMISSION ELECTRON MICROSCOPY;

CRYOELECTRON MICROSCOPY; DEINOCOCCUS; DNA, BACTERIAL; RADIATION TOLERANCE;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS;

EID: 28044437733     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.23.8047-8054.2005     Document Type: Article

References (41)

1. Adrian, M., J. Dubochet, J. Lepault, and A. W. McDowall. 1984. Cryo-electron microscopy of viruses. Nature 308:32-36.
2. Al-Amoudi, A., J. J. Chang, A. Leforestier, A. McDowall, L. M. Salamin, L. P. Norlen, K. Richter, N. S. Blanc, D. Studer, and J. Dubochet. 2004. Cryo-electron microscopy of vitreous sections. EMBO J. 23:3583-3588.
3. Al-Amoudi, A., L. P. Norlen, and J. Dubochet. 2004. Cryo-electron microscopy of vitreous sections of native biological cells and tissues. J. Struct. Biol. 148:131-135.
4. Battista, J. R. 1997. Against all odds: the survival strategies of Deinococcus radiodurans. Annu. Rev. Microbiol. 51:203-224.
5. Baumeister, W., M. Barth, R. Hegerl, R. Guckenberger, M. Hahn, and W. O. Saxton. 1986. Three-dimensional structure of the regular surface layer (HPI layer) of Deinococcus radiodurans. J. Mol. Biol. 187:241-250.
6. Bednar, J., P. Furrer, A. Stasiak, J. Dubochet, E. H. Egelman, and A. D. Bates. 1994. The twist, writhe and overall shape of supercoiled DNA change during counterion-induced transition from a loosely to a tightly interwound superhelix. Possible implications for DNA structure in vivo. J. Mol. Biol. 235:825-847.
7. Bohrmann, B., W. Villiger, R. Johansen, and E. Kellenberger. 1991. Coralline shape of the bacterial nucleoid after cryofixation. J. Bacteriol. 173:3149-3158.
8. Bouligand, Y. 1978. Liquid crystalline order in biological materials, p 261-297. In A. Blumstein (ed.), Liquid crystalline order in polymers. Academic Press, New York, N.Y.
9. Daly, M. J., E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, M. Zhai, A. Venkateswaran, M. Hess, M. V. Omelchenko, H. M. Kostandarithes, K. S. Makarova, L. P. Wackelt, J. K. Fredrickson, and D. Ghosal. 2004. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025-1028.
10. Daly, M. J., and K. W. Minton. 1997. Recombination between a resident plasmid and the chromosome following irradiation of the radioresistant bacterium Deinococcus radiodurans. Gene 187:225-229.
11. Dubochet, J. 1975. Carbon loss during irradiation of T4 bacteriophages and E. coli bacteria in electron microscopes. J. Ultrastruct. Res. 52:276-288.
12. Dubochet, J., J. Bednar, P. Furrer, A. Z. Stasiak, A. Stasiak, and A. A. Bolshoy. 1994. Determination of the DNA helical repeat by cryo-electron microscopy. Nat. Struct. Biol. 1:361-363.
13. Englander, J., E. Klein, V. Brumfeld, A. K. Sharma, A. J. Doherty, and A. Minsky. 2004. DNA toroids: framework for DNA repair in Deinococcus radiodurans and in germinating bacterial spores. J. Bacteriol. 186:5973-5977.
14. Finkel, S. E., and R. Kolter. 1999. Evolution of microbial diversity during prolonged starvation. Proc. Natl. Acad. Sci. USA 96:4023-4027.
15. Frenkiel-Krispin, D., I. Ben-Avraham, J. Englander, E. Shimoni, S. G. Wolf, and A. Minsky. 2004. Nucleoid restructuring in stationary-state bacteria. Mol. Microbiol. 51:395-405.
16. Frenkiel-Krispin, D., S. Levin-Zaidman, E. Shimoni, S. G. Wolf, E. J. Wachtel, T. Arad, S. E. Finkel, R. Kolter, and A. Minsky. 2001. Regulated phase transitions of bacterial chromatin: a non-enzymatic pathway for generic DNA protection. EMBO J. 20:1184-1191.
17. Ghosal, D., M. V. Omelchenko, E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, A. Venkateswaran, M. Zhai, H. M. Kostandarithes, H. Brim, and K. S. Makarova. 2005. How radiation kills cells: Survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol. Rev. 29:361-375.
18. Hansen, M. T. 1978. Multiplicity of genome equivalents in the radiation-resistant bacterium Micrococcus radiodurans. J. Bacteriol. 134:71-75.
19. Hobot, J. A., W. Villiger, J. Escaig, M. Maeder, A. Ryter, and E. Kellenberger. 1985. Shape and fine structure of nucleoids observed on sections of ultrarapidly frozen and cryosubstituted bacteria. J. Bacteriol. 162:960-971.
20. Hud, N. V., and K. H. Downing. 2001. Cryoelectron microscopy of lambda phage DNA condensates in vitreous ice: The fine structure of DNA toroids. Proc. Natl. Acad. Sci. USA 98:14925-14930.
21. Hud, N. V., and I. D. Vilfan. 2005. Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining Size. Annu. Rev. Biophys. Biomol. Struct. 34:295-318.
22. Jary, D., and J. L. Sikorav. 1999. Cyclization of globular DNA. Implications for DNA-DNA interactions in vivo. Biochemistry 38:3223-3227.
23. Kellenberger, E., and B. Arnold-Schulz-Gahmen. 1992. Chromatins of low- protein content: special features of their compaction and condensation. FEMS Microbiol. Lett. 79:361-370.
24. Keller, L. C., and R. B. Maxcy. 1984. Effect of physiological age on radiation resistance of some bacteria that are highly radiation resistant. Appl. Environ. Microbiol. 47:915-918.
25. Lange, C. C., L. P. Wackett, K. W. Minton, and M. J. Daly. 1998. Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments. Nat. Biotechnol. 16:929-933.
26. Leforestier, A., and F. Livolant. 1993. Supramolecular ordering of DNA in the cholesteric liquid crystalline phase: an ultrastructural study. Biophys. J. 65:56-72.
27. Leforestier, A., H. U. Nissen, and J. Dubochet. 1995. DNA-DNA interaction in thin layer analysed by cryo-electron microscopy. C. R. Acad. Sci. Ser. III Sci. Vie 318:1015-1020.
28. Leibowitz, P. J., L. S. Schwartzberg, and A. K. Brace. 1976. The in vivo association of manganese with the chromosome of Micrococcus radiodurans. Photochem. Photobiol. 23:45-50.
29. Levin-Zaidman, S., J. Englander, E. Shimoni, A. K. Sharma, K. W. Minton, and A. Minsky. 2003. Ringlike structure of the Deinococcus radiodurans genome: a key to radioresistance? Science 299:254-256.
30. Matias, V. R., A. Al-Amoudi, J. Dubochet, and T. J. Beveridge. 2003. Cryotransmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185:6112-6118.
31. Matias, V. R., and T. J. Beveridge. 2005. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56:240-251.
32. Minton, K. W., and M. J. Daly. 1995. A model for repair of radiation-induced DNA double-strand breaks in the extreme radiophile Deinococcus radiodurans. Bioessays 17:457-464.
33. Moseley, B. E., and A. Mattingly. 1971. Repair of irradiation transforming deoxyribonucleic acid in wild type and a radiation-sensitive mutant of Micrococcus radiodurans. J. Bacteriol. 105:976-983.
34. Reich, Z., E. J. Wachtel, and A. Minsky. 1994. Liquid-crystalline mesophases of plasmid DNA in bacteria. Science 264:1460-1463.
35. Rill, R. L., F. Livolant, H. C. Aldrich, and M. W. Davidson. 1989. Electron microscopy of liquid crystalline DNA: direct evidence for cholesteric-like organization of DNA in dinoflagellate chromosomes. Chromosoma 98:280-286.
36. Sartori Blanc, N., A. Senn, A. Leforestier, F. Livolant, and J. Dubochet. 2001. DNA in human and stallion spermatozoa forms local hexagonal packing with twist and many defects. J. Struct. Biol. 134:76-81.
37. Sleytr, U. B., M. Kocur, A. M. Glauert, and M. J. Thornley. 1973. A study by freeze-etching of the fine structure of Micrococcus radiodurans. Arch. Microbiol. 94:77-87.
38. Sleytr, U. B., M. T. Silva, M. Kocur, and N. F. Lewis. 1976. The fine structure of Micrococcus radiophilus and Micrococcus radioproteolyticus. Arch. Microbiol. 107:313-320.
39. Thornley, M. J., R. W. Horne, and A. M. Glauert. 1965. The fine structure of Micrococcus radiodurans. Arch. Mikrobiol. 51:267-289.
40. Work, E., and H. Griffiths. 1968. Morphology and chemistry of cell walls of Micrococcus radiodurans. J. Bacteriol. 95:641-657.
41. Zimmerman, J. M., and J. R. Battista. 2005. A ring-like nucleoid is not necessary for radioresistance in the Deinococcaceae. BMC Microbiol. 5:17.