Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T19:38:13.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Atomic Force Microscopy Dissects the Hierarchy of Genome Architectures in Eukaryote, Prokaryote, and Chloroplast

Published online by Cambridge University Press:  18 January 2007

R.L. Ohniwa ,
K. Morikawa ,
J. Kim ,
T. Kobori ,
K. Hizume ,
R. Matsumi ,
H. Atomi ,
T. Imanaka ,
T. Ohta  and
C. Wada
...Show all authors
R.L. Ohniwa
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
K. Morikawa
Affiliation:
Institute for Basic Medical Sciences, Tsukuba University, Tsukuba, Japan
J. Kim
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
T. Kobori
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
K. Hizume
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
R. Matsumi
Affiliation:
Kyoto University Graduate School of Engineering, Katsura, Kyoto, Japan
H. Atomi
Affiliation:
Kyoto University Graduate School of Engineering, Katsura, Kyoto, Japan
T. Imanaka
Affiliation:
Kyoto University Graduate School of Engineering, Katsura, Kyoto, Japan
T. Ohta
Affiliation:
Institute for Basic Medical Sciences, Tsukuba University, Tsukuba, Japan
C. Wada
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
S.H. Yoshimura
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
K. Takeyasu
Affiliation:
Kyoto University Graduate School of Biostudies, Sakyo-ku, Kyoto 606-8502, Japan
Get access

Abstract

Because of its applicability to biological specimens (nonconductors), a single-molecule-imaging technique, atomic force microscopy (AFM), has been particularly powerful for visualizing and analyzing complex biological processes. Comparative analyses based on AFM observation revealed that the bacterial nucleoids and human chromatin were constituted by a detergent/salt-resistant 30–40-nm fiber that turned into thicker fibers with beads of 70–80 nm diameter. AFM observations of the 14-kbp plasmid and 110-kbp F plasmid purified from Escherichia coli demonstrated that the 70–80-nm fiber did not contain a eukaryotic nucleosome-like “beads-on-a-string” structure. Chloroplast nucleoid (that lacks bacterial-type nucleoid proteins and eukaryotic histones) also exhibited the 70–80-nm structural units. Interestingly, naked DNA appeared when the nucleoids from E. coli and chloroplast were treated with RNase, whereas only 30-nm chromatin fiber was released from the human nucleus with the same treatment. These observations suggest that the 30–40-nm nucleoid fiber is formed with a help of nucleoid proteins and RNA in E. coli and chroloplast, and that the eukaryotic 30-nm chromatin fiber is formed without RNA. On the other hand, the 70–80-nm beaded structures in both E. coli and human are dependent on RNA.

Keywords

atomic force microscopynucleoidgenome architectureEscherichia coliStaphylococcus aureusClostridium perfringensChloroplastHeLa cell
Type
Research Article
Information
Microscopy and Microanalysis , Volume 13 , Issue 1: Special Issue: Environmental, Industrial, and AppliedMicrobiology , February 2007 , pp. 3 - 12
Copyright
2007 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Azam, T.A., Hiraga, S. & Ishihama, A. (2000). Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5, 613–626.Google Scholar
Azam, T.A. & Ishihama, A. (1999). Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274, 33105–33113.Google Scholar
Cannon, G.C., Ward, L.N., Case, C.I. & Heinhorst, S. (1999). The 68 kDa DNA compacting nucleoid protein from soybean chloroplasts inhibits DNA synthesis in vitro. Plant Mol Biol 39, 835–845.Google Scholar
Carninci, P., Kasukawa, T., Katayama, S., et al. (2005). The transcriptional landscape of the mammalian genome. Science 309, 1559–1563.Google Scholar
Cunha, S., Odijk, T., Suleymanoglu, E. & Woldringh, C.L. (2001). Isolation of the Escherichia coli nucleoid. Biochimie 83, 149–154.Google Scholar
Dame, R.T. (2005). The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol Microbiol 56, 858–870.Google Scholar
Gottesman, S. (2004). The small RNA regulators of Escherichia coli: Roles and mechanisms. Annu Rev Microbiol 58, 303–328.Google Scholar
Hecht, R.M. & Pettijohn, D.E. (1976). Studies of DNA bound RNA molecules isolated from nucleoids of Escherichia coli. Nucleic Acids Res 3, 767–788.Google Scholar
Hizume, K., Yoshimura, S.H. & Takeyasu, K. (2004). Atomic force microscopy demonstrates a critical role of DNA superhelicity in nucleosome dynamics. Cell Biochem Biophys 40, 249–262.Google Scholar
Hizume, K., Yoshimura, S.H. & Takeyasu, K. (2005). Linker histone H1 per se can induce three-dimensional folding of chromatin fiber. Biochemistry 44, 12978–12989.Google Scholar
Kim, J., Yoshimura, S.H., Hizume, K., Ohniwa, R.L., Ishihama, A. & Takeyasu, K. (2004). Fundamental structural units of the Escherichia coli nucleoid revealed by atomic force microscopy. Nucleic Acids Res 32, 1982–1992.Google Scholar
Kleppe, K., Ovrebo, S. & Lossius, I. (1979). The bacterial nucleoid. J Gen Microbiol 112, 1–13.Google Scholar
Kobori, T., Yoshino, T., Sugiyama, S. & Ohtani, T. (2003). Hierarchical chromatin structure of Schizosaccharomyces pombe revealed by atomic force microscopy. Curr Microbiol 47, 404–407.Google Scholar
Mizuno, T., Chou, M.Y. & Inouye, M. (1984). A unique mechanism regulating gene expression: Translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci USA 81, 1966–1970.Google Scholar
Moller, T., Franch, T., Hojrup, P., Keene, D.R., Bachinger, H.P., Brennan, R.G. & Valentin-Hansen, P. (2002). Hfq: A bacterial Sm-like protein that mediates RNA–RNA interaction. Mol Cell 9, 23–30.Google Scholar
Morgan, C., Rosenkranz, H.S., Carr, H.S. & Rose, H.M. (1967). Electron microscopy of chloramphenicol-treated Escherichia coli. J Bacteriol 93, 1987–2002.Google Scholar
Morikawa, K., Ohniwa, R.L., Kim, J., Maruyama, A., Ohta, T. & Takeyasu, K. (2006). Bacterial nucleoid dynamics: Oxidative stress response in Staphylococcus aureus. Genes Cells 11, 409–423.Google Scholar
Motamedi, M.R., Verdel, A., Colmenares, S.U., Gerber, S.A., Gygi, S.P. & Moazed, D. (2004). Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789–802.Google Scholar
Murphy, L.D. & Zimmerman, S.B. (1997). Isolation and characterization of spermidine nucleoids from Escherichia coli. J Struct Biol 119, 321–335.Google Scholar
Murphy, L.D. & Zimmerman, S.B. (2002). Hypothesis: The RNase-sensitive restraint to unfolding of spermidine nucleoids from Escherichia coli is composed of cotranslational insertion linkages. Biophys Chem 101–102, 321–331.Google Scholar
Nakai, T., Hizume, K., Yoshimura, S.H., Takeyasu, K. & Yoshikawa, K. (2005). Phase transition in reconstituted chromain. Europhys Lett 69, 1024–1030.Google Scholar
Pettijohn, D.E. & Hecht, R. (1974). RNA molecules bound to the folded bacterial genome stabilize DNA folds and segregate domains of supercoiling. Cold Spring Harb Symp Quant Biol 38, 31–41.Google Scholar
Poplawski, A. & Bernander, R. (1997). Nucleoid structure and distribution in thermophilic Archaea. J Bacteriol 179, 7625–7630.Google Scholar
Robinow, C. & Kellenberger, E. (1994). The bacterial nucleoid revisited. Microbiol Rev 58, 211–232.Google Scholar
Schneider, S.W., Larmer, J., Henderson, R.M. & Oberleithner, H. (1998). Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflugers Arch 435, 362–367.Google Scholar
Takeyasu, K., Kim, J., Ohniwa, R.L., Kobori, T., Inose, Y., Morikawa, K., Ohta, T., Ishihama, A. & Yoshimura, S.H. (2004). Genome architecture studied by nanoscale imaging: Analyses among bacterial phyla and their implication to eukaryotic genome folding. Cytogenet Genome Res 107, 38–48.Google Scholar
van Noort, J., Verbrugge, S., Goosen, N., Dekker, C. & Dame, R.T. (2004). Dual architectural roles of HU: Formation of flexible hinges and rigid filaments. Proc Natl Acad Sci USA 101, 6969–6974.Google Scholar
Vos-Scheperkeuter, G.H. & Witholt, B. (1982). Co-translational insertion of envelope proteins: Theoretical consideration and implications. Ann Microbiol (Paris) 133A, 129–138.Google Scholar
Wolffe, A.P. (1995). Centromeric chromatin. Histone deviants. Curr Biol 5, 452–454.Google Scholar
Worcel, A. & Burgi, E. (1972). On the structure of the folded chromosome of Escherichia coli. J Mol Biol 71, 127–147.Google Scholar
Yoshimura, S.H., Kim, J. & Takeyasu, K. (2003). On-substrate lysis treatment combined with scanning probe microscopy revealed chromosome structures in eukaryotes and prokaryotes. J Electron Microsc (Tokyo) 52, 415–423.Google Scholar
Yurina, N.P., Belkina, G.G., Karapetyan, N.V. & Odintsova, M.S. (1995). Nucleoids of pea chloroplasts: Microscopic and chemical characterization. Occurrence of histone-like proteins. Biochem Mol Biol Int 36, 145–154.Google Scholar
Zamore, P.D. & Haley, B. (2005). Ribo-genome: The big world of small RNAs. Science 309, 1519–1524.Google Scholar
Zhang, A., Wassarman, K.M., Ortega, J., Steven, A.C. & Storz, G. (2002). The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9, 11–22.Google Scholar
Zhang, X.P. & Glaser, E. (2002). Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci 7, 14–21.Google Scholar
Zimmerman, S.B. & Murphy, L.D. (1996). Macromolecular crowding and the mandatory condensation of DNA in bacteria. FEBS Lett 390, 245–248.Google Scholar