Abstract
The topological state of DNA in hyperthermophilic archaea appears to correspond to a linking excess in comparison with DNA in mesophilic organisms. Since DNA binding proteins often contribute to the control of DNA topology by affecting DNA geometry in the presence of DNA topoisomerases, we tested whether the histone-like protein Sso7d from the hyperthermophilic archaeon Sulfolobus solfataricus alters DNA conformation. In ligase-mediated supercoiling assays carried out at 37, 60, 70, 80 and 90 degrees C we found that DNA binding of increasing amounts of Sso7d led to a progressive decrease in plasmid linking number (Lk), producing negative supercoiling. Identical unwinding effects were observed when recombinant non-methylated Sso7d was used. For a given Sso7d concentration the DNA unwinding induced was augmented with increasing temperature. However, after correction for the overwinding effect of high temperature on DNA, plasmids ligated at 60-90 degrees C exhibited similar sigma values at the highest Sso7d concentrations assayed. These results suggest that Sso7d may play a compensatory role in vivo by counteracting the overwinding effect of high temperature on DNA. Additionally, Sso7d unwinding could be involved in the topological changes observed during thermal stress (heat and cold shock), playing an analogous role in crenarchaeal cells to that proposed for HU in bacteria.
Full Text
The Full Text of this article is available as a PDF (300.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Atlung T., Ingmer H. H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol. 1997 Apr;24(1):7–17. doi: 10.1046/j.1365-2958.1997.3151679.x. [DOI] [PubMed] [Google Scholar]
- Baumann H., Knapp S., Karshikoff A., Ladenstein R., Härd T. DNA-binding surface of the Sso7d protein from Sulfolobus solfataricus. J Mol Biol. 1995 Apr 14;247(5):840–846. doi: 10.1006/jmbi.1995.0184. [DOI] [PubMed] [Google Scholar]
- Baumann H., Knapp S., Lundbäck T., Ladenstein R., Härd T. Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus. Nat Struct Biol. 1994 Nov;1(11):808–819. doi: 10.1038/nsb1194-808. [DOI] [PubMed] [Google Scholar]
- Broyles S. S., Pettijohn D. E. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol. 1986 Jan 5;187(1):47–60. doi: 10.1016/0022-2836(86)90405-5. [DOI] [PubMed] [Google Scholar]
- Charbonnier F., Erauso G., Barbeyron T., Prieur D., Forterre P. Evidence that a plasmid from a hyperthermophilic archaebacterium is relaxed at physiological temperatures. J Bacteriol. 1992 Oct;174(19):6103–6108. doi: 10.1128/jb.174.19.6103-6108.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Choli T., Henning P., Wittmann-Liebold B., Reinhardt R. Isolation, characterization and microsequence analysis of a small basic methylated DNA-binding protein from the Archaebacterium, Sulfolobus solfataricus. Biochim Biophys Acta. 1988 Jul 13;950(2):193–203. doi: 10.1016/0167-4781(88)90011-5. [DOI] [PubMed] [Google Scholar]
- Choli T., Wittmann-Liebold B., Reinhardt R. Microsequence analysis of DNA-binding proteins 7a, 7b, and 7e from the archaebacterium Sulfolobus acidocaldarius. J Biol Chem. 1988 May 25;263(15):7087–7093. [PubMed] [Google Scholar]
- Clark D. J., Felsenfeld G. Formation of nucleosomes on positively supercoiled DNA. EMBO J. 1991 Feb;10(2):387–395. doi: 10.1002/j.1460-2075.1991.tb07960.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Depew D. E., Wang J. C. Conformational fluctuations of DNA helix. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4275–4279. doi: 10.1073/pnas.72.11.4275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drlica K. Control of bacterial DNA supercoiling. Mol Microbiol. 1992 Feb;6(4):425–433. doi: 10.1111/j.1365-2958.1992.tb01486.x. [DOI] [PubMed] [Google Scholar]
- Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duguet M. The helical repeat of DNA at high temperature. Nucleic Acids Res. 1993 Feb 11;21(3):463–468. doi: 10.1093/nar/21.3.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Felsenfeld G., Boyes J., Chung J., Clark D., Studitsky V. Chromatin structure and gene expression. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9384–9388. doi: 10.1073/pnas.93.18.9384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fusi P., Tedeschi G., Aliverti A., Ronchi S., Tortora P., Guerritore A. Ribonucleases from the extreme thermophilic archaebacterium S. solfataricus. Eur J Biochem. 1993 Jan 15;211(1-2):305–310. doi: 10.1111/j.1432-1033.1993.tb19899.x. [DOI] [PubMed] [Google Scholar]
- Grogan D. W. Phenotypic characterization of the archaebacterial genus Sulfolobus: comparison of five wild-type strains. J Bacteriol. 1989 Dec;171(12):6710–6719. doi: 10.1128/jb.171.12.6710-6719.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guagliardi A., Napoli A., Rossi M., Ciaramella M. Annealing of complementary DNA strands above the melting point of the duplex promoted by an archaeal protein. J Mol Biol. 1997 Apr 11;267(4):841–848. doi: 10.1006/jmbi.1996.0873. [DOI] [PubMed] [Google Scholar]
- Ivanchenko M., Hassan A., van Holde K., Zlatanova J. H1 binding unwinds DNA. Evidence from topological assays. J Biol Chem. 1996 Dec 20;271(51):32580–32585. doi: 10.1074/jbc.271.51.32580. [DOI] [PubMed] [Google Scholar]
- Jentoft N., Dearborn D. G. Protein labeling by reductive alkylation. Methods Enzymol. 1983;91:570–579. doi: 10.1016/s0076-6879(83)91052-2. [DOI] [PubMed] [Google Scholar]
- Jones P. G., Krah R., Tafuri S. R., Wolffe A. P. DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J Bacteriol. 1992 Sep;174(18):5798–5802. doi: 10.1128/jb.174.18.5798-5802.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keller W. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4876–4880. doi: 10.1073/pnas.72.12.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knapp S., Karshikoff A., Berndt K. D., Christova P., Atanasov B., Ladenstein R. Thermal unfolding of the DNA-binding protein Sso7d from the hyperthermophile Sulfolobus solfataricus. J Mol Biol. 1996 Dec 20;264(5):1132–1144. doi: 10.1006/jmbi.1996.0701. [DOI] [PubMed] [Google Scholar]
- La Teana A., Brandi A., Falconi M., Spurio R., Pon C. L., Gualerzi C. O. Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10907–10911. doi: 10.1073/pnas.88.23.10907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laine B., Culard F., Maurizot J. C., Sautière P. The chromosomal protein MC1 from the archaebacterium Methanosarcina sp. CHTI 55 induces DNA bending and supercoiling. Nucleic Acids Res. 1991 Jun 11;19(11):3041–3045. doi: 10.1093/nar/19.11.3041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lundbäck T., Hansson H., Knapp S., Ladenstein R., Härd T. Thermodynamic characterization of non-sequence-specific DNA-binding by the Sso7d protein from Sulfolobus solfataricus. J Mol Biol. 1998 Mar 6;276(4):775–786. doi: 10.1006/jmbi.1997.1558. [DOI] [PubMed] [Google Scholar]
- López-García P., Forterre P. DNA topology in hyperthermophilic archaea: reference states and their variation with growth phase, growth temperature, and temperature stresses. Mol Microbiol. 1997 Mar;23(6):1267–1279. doi: 10.1046/j.1365-2958.1997.3051668.x. [DOI] [PubMed] [Google Scholar]
- Malik M., Bensaid A., Rouviere-Yaniv J., Drlica K. Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. J Mol Biol. 1996 Feb 16;256(1):66–76. doi: 10.1006/jmbi.1996.0068. [DOI] [PubMed] [Google Scholar]
- McAfee J. G., Edmondson S. P., Datta P. K., Shriver J. W., Gupta R. Gene cloning, expression, and characterization of the Sac7 proteins from the hyperthermophile Sulfolobus acidocaldarius. Biochemistry. 1995 Aug 8;34(31):10063–10077. doi: 10.1021/bi00031a031. [DOI] [PubMed] [Google Scholar]
- Mead D. A., Szczesna-Skorupa E., Kemper B. Single-stranded DNA 'blue' T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng. 1986 Oct-Nov;1(1):67–74. doi: 10.1093/protein/1.1.67. [DOI] [PubMed] [Google Scholar]
- Mizushima T., Kataoka K., Ogata Y., Inoue R., Sekimizu K. Increase in negative supercoiling of plasmid DNA in Escherichia coli exposed to cold shock. Mol Microbiol. 1997 Jan;23(2):381–386. doi: 10.1046/j.1365-2958.1997.2181582.x. [DOI] [PubMed] [Google Scholar]
- Mizushima T., Natori S., Sekimizu K. Relaxation of supercoiled DNA associated with induction of heat shock proteins in Escherichia coli. Mol Gen Genet. 1993 Apr;238(1-2):1–5. doi: 10.1007/BF00279523. [DOI] [PubMed] [Google Scholar]
- Musgrave D. R., Sandman K. M., Reeve J. N. DNA binding by the archaeal histone HMf results in positive supercoiling. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10397–10401. doi: 10.1073/pnas.88.23.10397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ogata Y., Inoue R., Mizushima T., Kano Y., Miki T., Sekimizu K. Heat shock-induced excessive relaxation of DNA in Escherichia coli mutants lacking the histone-like protein HU. Biochim Biophys Acta. 1997 Sep 12;1353(3):298–306. doi: 10.1016/s0167-4781(97)00105-x. [DOI] [PubMed] [Google Scholar]
- Pérez-Martín J., Rojo F., de Lorenzo V. Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol Rev. 1994 Jun;58(2):268–290. doi: 10.1128/mr.58.2.268-290.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson H., Gao Y. G., McCrary B. S., Edmondson S. P., Shriver J. W., Wang A. H. The hyperthermophile chromosomal protein Sac7d sharply kinks DNA. Nature. 1998 Mar 12;392(6672):202–205. doi: 10.1038/32455. [DOI] [PubMed] [Google Scholar]
- Rouvière-Yaniv J., Yaniv M., Germond J. E. E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell. 1979 Jun;17(2):265–274. doi: 10.1016/0092-8674(79)90152-1. [DOI] [PubMed] [Google Scholar]
- Saavedra R. A., Huberman J. A. Both DNA topoisomerases I and II relax 2 micron plasmid DNA in living yeast cells. Cell. 1986 Apr 11;45(1):65–70. doi: 10.1016/0092-8674(86)90538-6. [DOI] [PubMed] [Google Scholar]
- Schmid M. B. More than just "histone-like" proteins. Cell. 1990 Nov 2;63(3):451–453. doi: 10.1016/0092-8674(90)90438-k. [DOI] [PubMed] [Google Scholar]
- Sinden R. R., Carlson J. O., Pettijohn D. E. Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell. 1980 Oct;21(3):773–783. doi: 10.1016/0092-8674(80)90440-7. [DOI] [PubMed] [Google Scholar]
- Starich M. R., Sandman K., Reeve J. N., Summers M. F. NMR structure of HMfB from the hyperthermophile, Methanothermus fervidus, confirms that this archaeal protein is a histone. J Mol Biol. 1996 Jan 12;255(1):187–203. doi: 10.1006/jmbi.1996.0016. [DOI] [PubMed] [Google Scholar]
- Travers A. A. Chromatin structure and dynamics. Bioessays. 1994 Sep;16(9):657–662. doi: 10.1002/bies.950160911. [DOI] [PubMed] [Google Scholar]