Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1998 Jan 15;26(2):427–430. doi: 10.1093/nar/26.2.427

Evidence for an early prokaryotic origin of histones H2A and H4 prior to the emergence of eukaryotes.

A I Slesarev 1, G I Belova 1, S A Kozyavkin 1, J A Lake 1
PMCID: PMC147304  PMID: 9421495

Abstract

Histones have been identified recently in many prokaryotes. These histones, unlike their eukaryotic homologs, are of a single uniform type that is thought to resemble the archetypal ancestor of the eukaryotic histone family. In this paper we report the finding, the cloning and the phylogenetic analysis of the sequence of a prokaryotic histone from the hyperthermophile Methanopyrus kandleri . Unlike previously described prokaryotic histones, the Methanopyrus sequence has a novel structure consisting of two tandemly repeated histone fold motifs in a single polypeptide. Sequence analyses indicate that the N-terminal repeat is most closely related to eukaryotic H2A and H4 histones, whereas the C-terminal repeat resembles that found in prokaryotic histones. These results imply an early divergence within the histone gene family prior to the emergence of eukaryotes and may represent an evolutionary step leading to eukaryotic histones.

Full Text

The Full Text of this article is available as a PDF (258.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arents G., Burlingame R. W., Wang B. C., Love W. E., Moudrianakis E. N. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. doi: 10.1073/pnas.88.22.10148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arents G., Moudrianakis E. N. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11170–11174. doi: 10.1073/pnas.92.24.11170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barton G. J. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 1993 Jan;6(1):37–40. doi: 10.1093/protein/6.1.37. [DOI] [PubMed] [Google Scholar]
  4. Bliska J. B., Cozzarelli N. R. Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol. 1987 Mar 20;194(2):205–218. doi: 10.1016/0022-2836(87)90369-x. [DOI] [PubMed] [Google Scholar]
  5. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. doi: 10.1126/science.273.5278.1058. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Darcy T. J., Sandman K., Reeve J. N. Methanobacterium formicicum, a mesophilic methanogen, contains three HFo histones. J Bacteriol. 1995 Feb;177(3):858–860. doi: 10.1128/jb.177.3.858-860.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grayling R. A., Bailey K. A., Reeve J. N. DNA binding and nuclease protection by the HMf histones from the hyperthermophilic archaeon Methanothermus fervidus. Extremophiles. 1997 May;1(2):79–88. doi: 10.1007/s007920050018. [DOI] [PubMed] [Google Scholar]
  9. Grayling R. A., Sandman K., Reeve J. N. Histones and chromatin structure in hyperthermophilic Archaea. FEMS Microbiol Rev. 1996 May;18(2-3):203–213. doi: 10.1111/j.1574-6976.1996.tb00237.x. [DOI] [PubMed] [Google Scholar]
  10. Hayes J. J., Tullius T. D., Wolffe A. P. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405–7409. doi: 10.1073/pnas.87.19.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Iwabe N., Kuma K., Hasegawa M., Osawa S., Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355–9359. doi: 10.1073/pnas.86.23.9355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kornberg R. D. Chromatin structure: a repeating unit of histones and DNA. Science. 1974 May 24;184(4139):868–871. doi: 10.1126/science.184.4139.868. [DOI] [PubMed] [Google Scholar]
  13. Kornberg R. D., Thomas J. O. Chromatin structure; oligomers of the histones. Science. 1974 May 24;184(4139):865–868. doi: 10.1126/science.184.4139.865. [DOI] [PubMed] [Google Scholar]
  14. Kozyavkin S. A., Krah R., Gellert M., Stetter K. O., Lake J. A., Slesarev A. I. A reverse gyrase with an unusual structure. A type I DNA topoisomerase from the hyperthermophile Methanopyrus kandleri is a two-subunit protein. J Biol Chem. 1994 Apr 15;269(15):11081–11089. [PubMed] [Google Scholar]
  15. Lake J. A. Calculating the probability of multitaxon evolutionary trees: bootstrappers Gambit. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9662–9666. doi: 10.1073/pnas.92.21.9662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lake J. A. Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1455–1459. doi: 10.1073/pnas.91.4.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Menzel R., Gellert M. Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell. 1983 Aug;34(1):105–113. doi: 10.1016/0092-8674(83)90140-x. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Reeve J. N., Sandman K., Daniels C. J. Archaeal histones, nucleosomes, and transcription initiation. Cell. 1997 Jun 27;89(7):999–1002. doi: 10.1016/s0092-8674(00)80286-x. [DOI] [PubMed] [Google Scholar]
  20. Richmond T. J., Finch J. T., Rushton B., Rhodes D., Klug A. Structure of the nucleosome core particle at 7 A resolution. Nature. 1984 Oct 11;311(5986):532–537. doi: 10.1038/311532a0. [DOI] [PubMed] [Google Scholar]
  21. Rinker A. G., Jr, Evans D. R. Isolation of chromosomal DNA from a methanogenic archaebacteria using a French pressure cell press. Biotechniques. 1991 Nov;11(5):612–613. [PubMed] [Google Scholar]
  22. Rivera M. C., Lake J. A. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science. 1992 Jul 3;257(5066):74–76. doi: 10.1126/science.1621096. [DOI] [PubMed] [Google Scholar]
  23. Ronimus R. S., Musgrave D. R. A gene, han1A, encoding an archaeal histone-like protein from the Thermococcus species AN1: homology with eukaryal histone consensus sequences and the implications for delineation of the histone fold. Biochim Biophys Acta. 1996 Jun 3;1307(1):1–7. doi: 10.1016/0167-4781(96)00031-0. [DOI] [PubMed] [Google Scholar]
  24. Ronimus R. S., Musgrave D. R. Purification and characterization of a histone-like protein from the Archaeal isolate AN1, a member of the Thermococcales. Mol Microbiol. 1996 Apr;20(1):77–86. doi: 10.1111/j.1365-2958.1996.tb02490.x. [DOI] [PubMed] [Google Scholar]
  25. Sandman K., Grayling R. A., Dobrinski B., Lurz R., Reeve J. N. Growth-phase-dependent synthesis of histones in the archaeon Methanothermus fervidus. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12624–12628. doi: 10.1073/pnas.91.26.12624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sandman K., Krzycki J. A., Dobrinski B., Lurz R., Reeve J. N. HMf, a DNA-binding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5788–5791. doi: 10.1073/pnas.87.15.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sandman K., Perler F. B., Reeve J. N. Histone-encoding genes from Pyrococcus: evidence for members of the HMf family of archaeal histones in a non-methanogenic Archaeon. Gene. 1994 Dec 2;150(1):207–208. doi: 10.1016/0378-1119(94)90890-7. [DOI] [PubMed] [Google Scholar]
  28. Slesarev A. I., Lake J. A., Stetter K. O., Gellert M., Kozyavkin S. A. Purification and characterization of DNA topoisomerase V. An enzyme from the hyperthermophilic prokaryote Methanopyrus kandleri that resembles eukaryotic topoisomerase I. J Biol Chem. 1994 Feb 4;269(5):3295–3303. [PubMed] [Google Scholar]
  29. Slesarev A. I., Stetter K. O., Lake J. A., Gellert M., Krah R., Kozyavkin S. A. DNA topoisomerase V is a relative of eukaryotic topoisomerase I from a hyperthermophilic prokaryote. Nature. 1993 Aug 19;364(6439):735–737. doi: 10.1038/364735a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Tabassum R., Sandman K. M., Reeve J. N. HMt, a histone-related protein from Methanobacterium thermoautotrophicum delta H. J Bacteriol. 1992 Dec;174(24):7890–7895. doi: 10.1128/jb.174.24.7890-7895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang J. C. DNA topoisomerases. Annu Rev Biochem. 1996;65:635–692. doi: 10.1146/annurev.bi.65.070196.003223. [DOI] [PubMed] [Google Scholar]
  33. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES