very early in eukaryotic evolution? Possibly, with
increasing genome size, it was necessary to limit
histone assembly to defined nucleosomes to allow
further compaction into precisely organized but
still readily accessible higher-order chromatin.
With diversification into four distinct histones
and numerous histone variants, plus the addition
of HF extensions and tails, eukaryotes further
gained the ability to selectively position nucleosomes, have a conserved chromatin architecture
recognizable by regulatory proteins, and develop
elaborate epigenetic regulation through posttranslational modification of histone tails. Intriguingly, some recently identified archaeal
histone sequences do have histone tails, hinting
at the beginnings of this diversification (fig. S1B).
However, to date, there is no evidence for archaeal
functional homologs, and thus determining the
ancestry of eukaryotic histone chaperones, chromatin remodelers, and posttranslational histone
regulators remains a challenge (22).
REFERENCES AND NOTES
1. K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent,
T. J. Richmond, Nature 389, 251–260 (1997).
2. K. Sandman, J. N. Reeve, Curr. Opin. Microbiol. 9, 520–525 (2006).
3. H. S. Malik, S. Henikoff, Nat. Struct. Biol. 10, 882–891 (2003).
4. P. B. Talbert, S. Henikoff, Nat. Rev. Mol. Cell Biol. 11, 264–275 (2010).
5. K. Zaremba-Niedzwiedzka et al., Nature 541, 353–358 (2017).
6. H. Nishida, T. Oshima, J. Gen. Appl. Microbiol. 63, 28–35 (2017).
7. K. Luger, T. J. Richmond, Curr. Opin. Genet. Dev. 8, 140–146 (1998).
8. K. A. Bailey, S. L. Pereira, J. Widom, J. N. Reeve, J. Mol. Biol.
303, 25–34 (2000).
9. K. Sandman, D. Soares, J. N. Reeve, Biochimie 83, 277–281 (2001).
10. K. Decanniere, A. M. Babu, K. Sandman, J. N. Reeve,
U. Heinemann, J. Mol. Biol. 303, 35–47 (2000).
11. K. Sandman, H. Louvel, R. Y. Samson, S. L. Pereira, J. N. Reeve,
Extremophiles 12, 811–817 (2008).
12. D. J. Soares, K. Sandman, J. N. Reeve, J. Mol. Biol. 297, 39–47 (2000).
13. R. S. Edayathumangalam, P. Weyermann, J. M. Gottesfeld,
P. B. Dervan, K. Luger, Proc. Natl. Acad. Sci. U.S.A. 101,
14. N. Nalabothula et al., BMC Genomics 14, 391 (2013).
15. H. Maruyama et al., EMBO Rep. 14, 711–717 (2013).
16. M. Tomschik, M. A. Karymov, J. Zlatanova, S. H. Leuba,
Structure 9, 1201–1211 (2001).
17. S. Tan, C. A. Davey, Curr. Opin. Struct. Biol. 21, 128–136
18. D. Kato et al., Science 356, 205–208 (2017).
19. F. Song et al., Science 344, 376–380 (2014).
20. T. H. Hileman, T. J. Santangelo, Front. Microbiol. 3, 195 (2012).
21. T. J. Santangelo, L. Cuboňová, J. N. Reeve, Mol. Microbiol. 81,
22. L. Aravind, A. M. Burroughs, D. Zhang, L. M. Iyer, Cold Spring
Harb. Perspect. Biol. 6, a016063 (2014).
We thank the University of Colorado BioFrontiers Institute Next-
Generation Sequencing Core Facility for performing BioAnalzyer
runs and the Protein Expression and Purification Facility at
Colorado State University for reagents. This work was supported
by NIH grants GM 067777 (to K.L.), GM53185 (to J.N.R.),
GM100329 (to T.J.S.), and GM114594 (to N.G.A.). F.M. is funded by
the European Molecular Biology Organization (ALTF 1267-2013)
and the Dutch Cancer Society (KWF 2014-6649). K.L. is supported
by the Howard Hughes Medical Institute. F.M. finalized the
structure, designed mutants, performed the analytical
ultracentrifugation and qRT-PCR experiments, and contributed to
structure analysis, the MNase experiments, and manuscript
preparation. S.B. processed and phased the x-ray data, built and
refined the model, and helped analyze the structure. P.N.D. and
K.S. prepared complexes, obtained crystals, and collected data.
P.N.D. performed in vitro complex analysis, and A.E. W. performed
the MNase and histone-extraction experiments. T.J.S., B. W.B.,
and K.R.B. constructed and characterized the T. kodakarensis strains
and grew biomass. T.L. and N.G.A. performed mass spectrometry.
T.J.S. assisted in manuscript preparation. J.N.R. and K.L. conceived
and directed the project, wrote the manuscript, analyzed the
structure, and prepared figures. The structure has been deposited in
the Protein Data Bank (PDB accession code 5T5K).
Materials and Methods
Figs. S1 to S6
Tables S1 to S4
8 September 2016; resubmitted 16 May 2017
Accepted 5 July 2017
612 11 AUGUST 2017 • VOL 357 ISSUE 6351 sciencemag.org SCIENCE
RESEARCH | REPORTS