Abstract
ABSTRACT The organization of chromatin has a major impact on cellular activities, such as gene expression. For bacteria, it was suggested that the spatial organization of the genetic material correlates with transcriptional levels, implying a specific architecture of the chromosome within the cytoplasm. Accordingly, recent technological advances have emphasized the organization of the genetic material within nucleoid structures. Gemmata obscuriglobus , a member of the phylum Planctomycetes , exhibits a distinctive nucleoid structure in which chromatin is encapsulated within a discrete membrane-bound compartment. Here, we show that this soil and freshwater bacterium tolerates high doses of UV and ionizing radiation. Cryoelectron tomography of frozen hydrated sections and electron microscopy of freeze-substituted cells have indicated a more highly ordered condensed-chromatin organization in actively dividing and stationary-phase G. obscuriglobus cells. These three-dimensional analyses revealed a complex network of double membranes that engulf the condensed DNA. Bioinformatics analysis has revealed the existence of a putative component involved in nonhomologous DNA end joining that presumably plays a role in maintaining chromatin integrity within the bacterium. Thus, our observations further support the notion that packed chromatin organization enhances radiation tolerance.
References
59
Referenced
45
-
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.
(
10.1016/j.jsb.2004.03.010
) / J. Struct. Biol. (2004) -
Aravind, L., and E. V. Koonin. 2001. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res. 11 : 1365-1374.
(
10.1101/gr.181001
) / Genome Res. (2001) -
Blasius, M., R. Buob, I. V. Shevelev, and U. Hubscher. 2007. Enzymes involved in DNA ligation and end-healing in the radioresistant bacterium Deinococcus radiodurans. BMC Mol. Biol. 8 : 69.
(
10.1186/1471-2199-8-69
) / BMC Mol. Biol. (2007) -
Brochier, C., and H. Philippe. 2002. Phylogeny: a non-hyperthermophilic ancestor for bacteria. Nature 417 : 244.
(
10.1038/417244a
) / Nature (2002) -
Chedin, F., P. Noirot, V. Biaudet, and S. D. Ehrlich. 1998. A five-nucleotide sequence protects DNA from exonucleolytic degradation by AddAB, the RecBCD analogue of Bacillus subtilis. Mol. Microbiol. 29 : 1369-1377.
(
10.1046/j.1365-2958.1998.01018.x
) / Mol. Microbiol. (1998) -
Courcelle, J., and P. C. Hanawalt. 2003. RecA-dependent recovery of arrested DNA replication forks. Annu. Rev. Genet. 37 : 611-646.
(
10.1146/annurev.genet.37.110801.142616
) / Annu. Rev. Genet. (2003) -
Cox, M. M., and J. R. Battista. 2005. Deinococcus radiodurans—the consummate survivor. Nat. Rev. Microbiol. 3 : 882-892.
(
10.1038/nrmicro1264
) / Nat. Rev. Microbiol. (2005) -
Cox, M. M., M. F. Goodman, K. N. Kreuzer, D. J. Sherratt, S. J. Sandler, and K. J. Marians. 2000. The importance of repairing stalled replication forks. Nature 404 : 37-41.
(
10.1038/35003501
) / Nature (2000) -
Della, M., P. L. Palmbos, H. M. Tseng, L. M. Tonkin, J. M. Daley, L. M. Topper, R. S. Pitcher, A. E. Tomkinson, T. E. Wilson, and A. J. Doherty. 2004. Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science 306 : 683-685.
(
10.1126/science.1099824
) / Science (2004) -
Doherty, A. J., S. P. Jackson, and G. R. Weller. 2001. Identification of bacterial homologues of the Ku DNA repair proteins. FEBS Lett. 500 : 186-188.
(
10.1016/S0014-5793(01)02589-3
) / FEBS Lett. (2001) 10.1128/JB.187.23.8047-8054.2005
10.1128/JB.186.18.5973-5977.2004
-
Errington, J. 2003. Dynamic proteins and a cytoskeleton in bacteria. Nat. Cell Biol. 5 : 175-178.
(
10.1038/ncb0303-175
) / Nat. Cell Biol. (2003) -
Feder, N., and R. L. Sidman. 1958. Methods and principles of fixation by freeze-substitution. J. Biophys. Biochem. Cytol. 4 : 593-600.
(
10.1083/jcb.4.5.593
) / J. Biophys. Biochem. Cytol. (1958) -
Frangakis, A. S., and R. Hegerl. 2001. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135 : 239-250.
(
10.1006/jsbi.2001.4406
) / J. Struct. Biol. (2001) -
Franzmann, P. D., and V. B. Skerman. 1984. Gemmata obscuriglobus, a new genus and species of the budding bacteria. Antonie van Leeuwenhoek 50 : 261-268.
(
10.1007/BF02342136
) / Antonie van Leeuwenhoek (1984) -
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.
(
10.1093/emboj/20.5.1184
) / EMBO J. (2001) -
Frenkiel-Krispin, D., and A. Minsky. 2006. Nucleoid organization and the maintenance of DNA integrity in E. coli, B. subtilis and D. radiodurans. J. Struct. Biol. 156 : 311-319.
(
10.1016/j.jsb.2006.05.014
) / J. Struct. Biol. (2006) 10.1128/JB.186.11.3525-3530.2004
-
Fuerst, J. A., and R. I. Webb. 1991. Membrane-bounded nucleoid in the eubacterium Gemmatata obscuriglobus. Proc. Natl. Acad. Sci. USA 88 : 8184-8188.
(
10.1073/pnas.88.18.8184
) / Proc. Natl. Acad. Sci. USA (1991) -
Gascon, J., A. Oubina, A. Perez-Lezaun, and J. Urmeneta. 1995. Sensitivity of selected bacterial species to UV radiation. Curr. Microbiol. 30 : 177-182.
(
10.1007/BF00296205
) / Curr. Microbiol. (1995) -
Gitai, Z. 2005. The new bacterial cell biology: moving parts and subcellular architecture. Cell 120 : 577-586.
(
10.1016/j.cell.2005.02.026
) / Cell (2005) -
Gong, C., A. Martins, P. Bongiorno, M. Glickman, and S. Shuman. 2004. Biochemical and genetic analysis of the four DNA ligases of Mycobacteria. J. Biol. Chem. 279 : 20594-20606.
(
10.1074/jbc.M401841200
) / J. Biol. Chem. (2004) -
Grimm, R., H. Singh, R. Rachel, D. Typke, W. Zillig, and W. Baumeister. 1998. Electron tomography of ice-embedded prokaryotic cells. Biophys. J. 74 : 1031-1042.
(
10.1016/S0006-3495(98)74028-7
) / Biophys. J. (1998) - Gruska, M., O. Medalia, W. Baumeister, and A. Leis. 2007. Electron tomography of vitreous sections from cultured mammalian cells. J. Struct. Biol. 161 : 384-392. / J. Struct. Biol. (2007)
-
Hegerl, R. 1996. The EM program package: a platform for image processing in biological electron microscopy. J. Struct. Biol. 116 : 30-34.
(
10.1006/jsbi.1996.0006
) / J. Struct. Biol. (1996) 10.1128/jb.162.3.960-971.1985
-
Hohenberg, H., K. Mannweiler, and M. Muller. 1994. High-pressure freezing of cell suspensions in cellulose capillary tubes. J. Microsc. 175 : 34-43.
(
10.1111/j.1365-2818.1994.tb04785.x
) / J. Microsc. (1994) 10.1128/aem.47.5.915-918.1984
-
Kowalczykowski, S. C. 1991. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Biophys. Chem. 20 : 539-575.
(
10.1146/annurev.bb.20.060191.002543
) / Annu. Rev. Biophys. Biophys. Chem. (1991) 10.1128/mr.58.3.401-465.1994
10.1128/MMBR.63.4.751-813.1999
-
Leforestier, A., and F. Livolant. 1993. Supramolecular ordering of DNA in the cholesteric liquid crystalline phase: an ultrastructural study. Biophys. J. 65 : 56-72.
(
10.1016/S0006-3495(93)81063-4
) / Biophys. J. (1993) -
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.
(
10.1126/science.1077865
) / Science (2003) -
Lindsay, M. R., R. I. Webb, M. Strous, M. S. Jetten, M. K. Butler, R. J. Forde, and J. A. Fuerst. 2001. Cell compartmentalisation in Planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175 : 413-429.
(
10.1007/s002030100280
) / Arch. Microbiol. (2001) 10.1128/MMBR.65.1.44-79.2001
10.1128/jb.178.3.633-637.1996
-
Minsky, A. 2003. Structural aspects of DNA repair: the role of restricted diffusion. Mol. Microbiol. 50 : 367-376.
(
10.1046/j.1365-2958.2003.03705.x
) / Mol. Microbiol. (2003) -
Minsky, A., E. Shimoni, and D. Frenkiel-Krispin. 2002. Stress, order and survival. Nat. Rev. Mol. Cell Biol. 3 : 50-60.
(
10.1038/nrm700
) / Nat. Rev. Mol. Cell Biol. (2002) 10.1128/JB.186.13.4192-4198.2004
-
Olins, A. L., B. A. Moyer, S. H. Kim, and D. P. Allison. 1989. Synthesis of a more stable osmium ammine electron-dense DNA stain. J. Histochem. Cytochem. 37 : 395-398.
(
10.1177/37.3.2465337
) / J. Histochem. Cytochem. (1989) -
Pennisi, E. 2004. Evolutionary biology: the birth of the nucleus. Science 305 : 766-768.
(
10.1126/science.305.5685.766
) / Science (2004) -
Pitcher, R. S., T. E. Wilson, and A. J. Doherty. 2005. New insights into NHEJ repair processes in prokaryotes. Cell Cycle 4 : 675-678.
(
10.4161/cc.4.5.1676
) / Cell Cycle (2005) 10.1128/aem.61.10.3633-3638.1995
-
Reich, Z., S. Levin-Zaidman, S. B. Gutman, T. Arad, and A. Minsky. 1994. Supercoiling-regulated liquid-crystalline packaging of topologically-constrained, nucleosome-free DNA molecules. Biochemistry 33 : 14177-14184.
(
10.1021/bi00251a029
) / Biochemistry (1994) 10.1128/mr.58.2.211-232.1994
-
Roca, A. I., and M. M. Cox. 1997. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucleic Acid Res. Mol. Biol. 56 : 129-223.
(
10.1016/S0079-6603(08)61005-3
) / Prog. Nucleic Acid Res. Mol. Biol. (1997) -
Schlesner, H. 1994. The development of media suitable for the microorganisms morphologically resembling Planctomyces spp., Pirellula spp., and other Planctomycetales from various aquatic habitats using dilute media. Syst. Appl. Microbiol. 17 : 135-145.
(
10.1016/S0723-2020(11)80042-1
) / Syst. Appl. Microbiol. (1994) -
Serianni, R. W., and A. K. Bruce. 1968. Radioresistance of Micrococcus radiodurans during the growth cycle. Radiat. Res. 36 : 193-207.
(
10.2307/3572645
) / Radiat. Res. (1968) -
Setlow, P. 1995. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49 : 29-54.
(
10.1146/annurev.mi.49.100195.000333
) / Annu. Rev. Microbiol. (1995) -
Studer, D., W. Graber, A. Al-Amoudi, and P. Eggli. 2001. A new approach for cryofixation by high-pressure freezing. J. Microsc. 203 : 285-294.
(
10.1046/j.1365-2818.2001.00919.x
) / J. Microsc. (2001) 10.1128/JB.01449-07
-
Weller, G. R., V. L. Brandt, and D. B. Roth. 2004. Doing more with less in bacterial DNA repair. Nat. Struct. Mol. Biol. 11 : 1158-1159.
(
10.1038/nsmb1204-1158
) / Nat. Struct. Mol. Biol. (2004) -
Weller, G. R., and A. J. Doherty. 2001. A family of DNA repair ligases in bacteria? FEBS Lett. 505 : 340-342.
(
10.1016/S0014-5793(01)02831-9
) / FEBS Lett. (2001) -
Weller, G. R., B. Kysela, R. Roy, L. M. Tonkin, E. Scanlan, M. Della, S. K. Devine, J. P. Day, A. Wilkinson, F. d'Adda di Fagagna, K. M. Devine, R. P. Bowater, P. A. Jeggo, S. P. Jackson, and A. J. Doherty. 2002. Identification of a DNA nonhomologous end-joining complex in bacteria. Science 297 : 1686-1689.
(
10.1126/science.1074584
) / Science (2002) -
Woebken, D., H. Teeling, P. Wecker, A. Dumitriu, I. Kostadinov, E. F. Delong, R. Amann, and F. O. Glockner. 2007. Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. Isme J. 1 : 419-435.
(
10.1038/ismej.2007.63
) / Isme J. (2007) 10.1128/mr.51.2.221-271.1987
-
Zhu, H., and S. Shuman. 2007. Characterization of Agrobacterium tumefaciens DNA ligases C and D. Nucleic Acids Res. 35 : 3631-3645.
(
10.1093/nar/gkm145
) / Nucleic Acids Res. (2007) -
Zimmerman, J. M., and J. R. Battista. 2005. A ring-like nucleoid is not necessary for radioresistance in the Deinococcaceae. BMC Microbiol. 5 : 17.
(
10.1186/1471-2180-5-17
) / BMC Microbiol. (2005)
Dates
Type | When |
---|---|
Created | 16 years, 8 months ago (Dec. 12, 2008, 9:48 p.m.) |
Deposited | 4 years ago (July 29, 2021, 1:10 p.m.) |
Indexed | 1 year, 2 months ago (June 3, 2024, 3:17 a.m.) |
Issued | 16 years, 5 months ago (March 1, 2009) |
Published | 16 years, 5 months ago (March 1, 2009) |
Published Print | 16 years, 5 months ago (March 1, 2009) |
@article{Lieber_2009, title={Chromatin Organization and Radio Resistance in the Bacterium Gemmata obscuriglobus}, volume={191}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.01513-08}, DOI={10.1128/jb.01513-08}, number={5}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Lieber, Arnon and Leis, Andrew and Kushmaro, Ariel and Minsky, Abraham and Medalia, Ohad}, year={2009}, month=mar, pages={1439–1445} }