Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs
- Narasimharao Nalabothula†1,
- Liqun Xi†2,
- Sucharita Bhattacharyya3,
- Jonathan Widom^3,
- Ji-Ping Wang2,
- John N Reeve4,
- Thomas J Santangelo4, 5 and
- Yvonne N Fondufe-Mittendorf1Email author
© Nalabothula et al.; licensee BioMed Central Ltd. 2013
Received: 19 February 2013
Accepted: 31 May 2013
Published: 10 June 2013
Histone wrapping of DNA into nucleosomes almost certainly evolved in the Archaea, and predates Eukaryotes. In Eukaryotes, nucleosome positioning plays a central role in regulating gene expression and is directed by primary sequence motifs that together form a nucleosome positioning code. The experiments reported were undertaken to determine if archaeal histone assembly conforms to the nucleosome positioning code.
Eukaryotic nucleosome positioning is favored and directed by phased helical repeats of AA/TT/AT/TA and CC/GG/CG/GC dinucleotides, and disfavored by longer AT-rich oligonucleotides. Deep sequencing of genomic DNA protected from micrococcal nuclease digestion by assembly into archaeal nucleosomes has established that archaeal nucleosome assembly is also directed and positioned by these sequence motifs, both in vivo in Methanothermobacter thermautotrophicus and Thermococcus kodakarensis and in vitro in reaction mixtures containing only one purified archaeal histone and genomic DNA. Archaeal nucleosomes assembled at the same locations in vivo and in vitro, with much reduced assembly immediately upstream of open reading frames and throughout the ribosomal rDNA operons. Providing further support for a common positioning code, archaeal histones assembled into nucleosomes on eukaryotic DNA and eukaryotic histones into nucleosomes on archaeal DNA at the same locations. T. kodakarensis has two histones, designated HTkA and HTkB, and strains with either but not both histones deleted grow normally but do exhibit transcriptome differences. Comparisons of the archaeal nucleosome profiles in the intergenic regions immediately upstream of genes that exhibited increased or decreased transcription in the absence of HTkA or HTkB revealed substantial differences but no consistent pattern of changes that would correlate directly with archaeal nucleosome positioning inhibiting or stimulating transcription.
The results obtained establish that an archaeal histone and a genome sequence together are sufficient to determine where archaeal nucleosomes preferentially assemble and where they avoid assembly. We confirm that the same nucleosome positioning code operates in Archaea as in Eukaryotes and presumably therefore evolved with the histone-fold mechanism of DNA binding and compaction early in the archaeal lineage, before the divergence of Eukaryotes.
KeywordsArchaea Nucleosome positioning Dinucleotide repeats Histone deletions rDNA expression Chromatin evolution
Histone wrapping of nuclear DNA generates nucleosomes, the basic unit of chromatin in virtually all Eukaryotes. Nucleosomes are dynamically associated with the genome and their distribution is not random, but often plays a major role in regulating gene expression [1–4]. Nucleosome assembly is favored or deterred by differences in the enthalpic and entropic costs inherent in wrapping and maintaining different sequences in the rigid nucleosome toroid, and this has resulted in a eukaryotic nucleosome positioning code [1, 3, 5–8]. Histones, and presumably histone-DNA interactions, evolved before the divergence of the archaeal and eukaryotic lineages with histones now distributed throughout the Euryarchaea, Nanoarchaea and Thaumarchaea and also present in some Crenarchaea[9–11].
Sequencing DNA molecules selected from a large random population by repetitive selection (SELEX) and PCR-amplification, based on increased archaeal histone-DNA affinity, revealed that DNA molecules preferentially assembled into archaeal nucleosomes in vitro had sequences that conformed to the eukaryotic nucleosome positioning code . However, the technology was not then available to determine if this was also the case in vivo and so confirm in vivo these results obtained in vitro. But, with the advent of large-scale DNA sequencing technologies, such comparisons became possible, and here we document that archaeal nucleosome assembly in vivo is directed by the nucleosome positioning code in both Methanothermobacter thermautotrophicus and Thermococcus kodakarensis, and that this is reproduced in vitro with archaeal genomic DNA and purified archaeal or eukaryotic histones. With recently developed genetic technologies, it was possible to delete either, but not both of the two archaeal histone-encoding genes present in T. kodakarensis generating strains that grow normally but exhibit transcriptome changes when compared with the parental strain . Here we show that the histone deletions also result in changes in the archaeal nucleosome profiles upstream of the genes that have increased or decreased transcription.
Nucleosome positioning motifs in vivo
In contrast to A/T-rich dinucleotides that, in a 10 bp periodicity, offer flexibility and so facilitate DNA incorporation, poly (dA:dT) tracts are relatively rigid. This deters their incorporation into nucleosomes [1–3, 6, 8, 22, 23] and poly (dA:dT) tracts are significantly underrepresented in DNA incorporated into eukaryotic nucleosomes [1, 6–8, 23–33]. Analyses of the archaeal ~60 bp nucleosomal DNA fragments revealed that A/T-rich oligonucleotides were also excluded from incorporation into archaeal nucleosomes assembled in M. thermautotrophicus and T. kodakarensis. For example, as illustrated in Figures 2c and 2d, when the frequencies of occurrence of each of the 1064 pentamers was determined, all of the 32 pentamers that contain only A and/or T were underrepresented relative to the presence in the genome sequences with ATATA (=TATAT) being the most disfavored pentamer in both Archaea. Oligo A/T-rich sequences are consequently located preferentially in nucleosome-depleted regions. In contrast, all of the 32 pentamers that contain only G and/or C were enriched in the ~60 bp MN-protected fragments generated from both Archaea relative to their abundances in the genome sequences (Figure 2c and 2d).
Exclusion of nucleosomes from intergenic regions
Conservation of archaeal nucleosome positioning in vivo and in vitro
As established for the parental strain (Figure 1a), the ~60 bp fragments of the T. kodakarensis genome protected from MN digestion by only HTkA or HTkB assembly in vivo and in vitro also contained 10 bp helical-periodicity repeats of AA/AT/TA/TT and GG/GC/CG/CC dinucleotides, offset by 5 bp, and pentamers containing only A and/or T were under-represented, and those containing only G and/or C were over-represented, relative to their occurrences in the T. kodakarensis genome (Additional file 1: Figure S1). Together these results confirm that the positions at which HTkA and HTkB assemble to form archaeal nucleosomes are predominantly determined by the T. kodakarensis genome sequence and, as concluded from eukaryotic nucleosome studies [7, 33, 38, 43–46], from an archaeal genome sequence , it should be possible to predict where archaeal nucleosomes will preferentially assemble in vivo.
Evolutionary conservation of the nucleosome positioning code
Archaeal histone deletion changes transcription and nucleosome positioning
Conservation and ancestral origin of the nucleosome positioning code
Whether a sequence will favor or disfavor assemble into a nucleosome can be predicted from the below- or above-average energy requirements needed to distort that sequence into the circular configuration of DNA wrapped around the nucleosome core [19, 47, 48]. To a large extent, these predictions have been confirmed experimentally by the sequences of DNA isolated from eukaryotic nucleosomes and so in the definition of a nucleosome positioning code [5–8, 19, 21, 33, 38, 43]. The results reported here confirm that two basic features of this code, namely a 10 bp periodicity of AA/AT/TA/TT dinucleotides offset by 5 bp from GG/GC/CG/CC dinucleotides, and the exclusion of A/T-rich oligonucleotides also direct archaeal nucleosome assembly in vivo and in vitro. In the structures established for the eukaryotic nucleosome [49, 50], the AA/AT/TA/TT dinucleotide repeats facilitate DNA wrapping as the dinucleotides that most readily accept the distortion needed , where the minor groove faces inwards towards the histone octamer. The GG/GC/CG/CC dinucleotide repeats, offset by half a helical turn, facilitate the distortion needed at each site where the minor groove faces outwards and so away from the nucleosome core [3, 49, 50]. To date, despite a significant effort, there is no high resolution structure of an archaeal nucleosome available but, given that the archaeal and eukaryotic histone folds are virtually identical [9, 51] and that DNA-histone interactions are almost entirely mediated by histone fold residues , it seems highly likely that the same wrapping mechanism is employed and so DNA distortion is required to assemble archaeal nucleosomes. Given this conservation, the nucleosome positioning code almost certainly predates the Eukaryotes, and co-evolved with histones and the histone-fold based mechanism of DNA compaction early in the archaeal lineage, before the divergence of Euryarchaea, Nanoarchaea and Thaumarchaea[9–11].
Archaeal nucleosome positioning and gene expression
As in Bacteria, many archaeal genes are organized into operons and so are co-transcribed from a single promoter and, in the absence of a nuclear membrane; transcription and translation are coupled . However, archaeal promoters and the transcription machinery are substantially more similar to their eukaryotic than bacterial counterparts. Archaeal transcription initiation requires that both transcription factors and RNA polymerase be recruited to the promoter  and archaeal histone binding to promoter regions has been shown, alternatively, to inhibit or to stimulate transcription in vitro [54, 55]. Without a transcriptome, we chose to determine the locations at which HTkA and HTkB assembled into nucleosomes on T. kodakarensis genomic DNA, both in vivo and in vitro, relative to translation start codons. This is a reasonable proxy for transcription initiation sites as most archaeal promoters are located within short intergenic regions and so are close to a start codon. As the results revealed, on a genome wide basis, archaeal nucleosomes are excluded from the DNA immediately upstream of open reading frames, and these nucleosome depleted regions (NDRs) are flanked by regions with above average nucleosome occupancy (Figure 4b). This is very similar to the pattern of nucleosome occupancy established in promoter regions and around the downstream transcription start sites in the yeast genome [1, 3, 26, 56]. The conservation of this nucleosome organization argues strongly for a participatory role in gene expression. Possibly, avoiding nucleosome assembly in the promoter region coupled with the presence of a nucleosome at the transcription start site evolved as a generic system to facilitate pre-transcription complex assembly while preventing immediate transcription initiation. If so, a mechanism would then also be needed to remove the inhibitory nucleosome when transcription should occur. In Eukaryotes, many complexes have evolved that catalyze histone modifications, nucleosome remodeling, repositioning and/or eviction that relieve transcription inhibition  but, to date, there is no evidence for archaeal histone modifications nor for archaeal nucleosome remodeling complexes.
Consistent with the presence of an archaeal nucleosome impeding transcription , presumably to maximize rRNA synthesis, archaeal nucleosome assembly was strongly deterred by the rDNA operon sequences, in vivo and in vitro, in both T. kodakarensis (Figure 6) and in M. thermautotrophicus (Additional file 3: Figure S3). To test the prediction that the presence of an archaeal nucleosome in a promoter region was sufficient to prevent downstream transcription, we compared the archaeal nucleosomes profiles upstream of genes whose transcription was known to increase or decrease in response to the absence of HTkA or HTkB . There were substantial differences in these profiles, in both the abundance and positioning of archaeal nucleosomes, when compared with the parental strain with both histones (Figure 7) but there was no consistent correlation. An increase or decrease in transcription did not simply result from the absence or presence of an archaeal nucleosome in a promoter region.
The results of a similar and complementary investigation were published  while this report was being finalized. Ammar et al.  determined the locations of archaeal nucleosomes assembled in vivo in Haloferax volcanii, also a euryarchaeon, but a species with a relatively high 65% G + C content, and one with a single atypical archaeal histone that has two histone folds fused into one polypeptide [9, 15, 58]. Both positioning investigations established that G/C-rich sequences predominate at the center of an archaeal nucleosome but a 10 bp periodicity of AA/AT/TA/TT dinucleotides was not detected in the DNA incorporated into nucleosomes in Hlf. volcanii. In both studies, a NDR flanked by increased nucleosome assembly was documented in intergenic regions but, with a transcriptome available, Ammar et al.  were able to define the location of the NDR relative to the sites of transcription initiation rather than, as here, to translation start codons. They did not report confirmatory in vitro positioning studies, but the nucleosome positioning in vivo in Hlf. volcanii was, as established here both in vivo and in vitro, almost certainly directed primarily by the Hlf. volcanii genome sequence.
The results reported establish that an archaeal histone and genome sequence are sufficient for positioned archaeal nucleosome assembly. They confirm that the primary sequence motifs known to facilitate and direct histone assembly into eukaryotic nucleosomes [5–8] also direct nucleosome assembly in Archaea and that this positioning mechanism therefore almost certainly originated in a common ancestor of Archaea and Eukaryotes. DNA compaction is often described as the primary function of nucleosomes but positioned nucleosomes clearly also participate in regulating eukaryotic gene expression [3, 59, 60] and nucleosome positioning, as a regulatory mechanism, likely predates nucleosome assembly for DNA compaction and archiving. When compared with eukaryotic genomes, archaeal (and bacterial) genomes are very small, and many different proteins have been described that participate both in gene expression and prokaryotic genome compaction . The first histone may have evolved as a protein that bound preferentially to sequences that encoded amphipathic peptide helices  with this sequence-directed binding participating in gene regulation. But, given that the histone fold mechanism of DNA binding results in DNA wrapping, this would have also inherently resulted in DNA compaction. When evaluated in terms of the length of DNA compacted per unit of protein, histone wrapping is very efficient, and it is possible that it was the availability of this mechanism, employed by all Eukaryotes, that allowed the massive genome expansion needed for eukaryotic evolution . It remains to be determined if archaeal histones still function primarily as regulators, as suggested by their depletion in intergenic regions , or if genome compaction is their primary function consistent with their observed assembly here throughout the full length of the T. kodakarensis and M. thermautotrophicus genomes.
Isolation of genomic DNA and archaeal nucleosomes assembled in vivo
Cells from exponentially growing cultures of M. thermautotrophicus, T. kodakarensis TS517 (ΔpyrF; Δ trpE::pyrF; Δ TK0664), LC124 (Δ pyrF; ΔtrpE::pyrF; Δ TK0664; Δ TK1413) and LC125 (Δ pyrF; Δ trpE::pyrF; ΔTK0664; ΔTK2289)  were harvested by centrifugation, flash frozen and genomic DNA preparations isolated from aliquots of these cells as previously described [36, 40]. The remainder were ruptured by grinding in frozen micrococcal nuclease (MN) buffer [50 mM Tris (pH 8), 1 mM CaCl2, 100 mM NaCl], and the lysates allowed to thaw at 4°C. Aliquots were incubated with MN (1 U/μl) at 37°C, and the nuclease digestion then terminated, after increasing periods of digestion, by addition of 250 mM EDTA, 1% SDS, 200 mM NaCl. Following incubation with RNase A (10 mg/ml) for 60 min at 42°C, the DNA molecules that remained were purified by phenol:chloroform extraction, concentrated by ethanol precipitation, and separated by electrophoresis through 3.5% NuSieve agarose gels (Fisher Molecular Biology, Trevose, PA) or 6% polyacrylamide gels. Gel fragments that contained DNA molecules with ~60 bp lengths were excised, crushed and the DNA molecules eluted by incubation overnight at 37°C in 300 mM sodium acetate, 1 mM EDTA (pH 8), 0.1% SDS. The DNA molecules were concentrated by ethanol precipitation, and prepared for sequencing (see below).
Archaeal histone gene cloning, expression and purification of recombinant HTkA and HTkB
The genes, TK1413 and TK2289, that encode HTkA and HTkB respectively in T. kodakarensis TS517 , were PCR-amplified and cloned into plasmid pQE-80 (Qiagen, Valencia, CA) generating plasmids pTS600 (TK1413) and pTS601 (TK2289) that were transformed into Escherichia coli Rosetta 2 (EMD-Millipore, Billerica, MA). Cultures of the transformants were grown to the late exponential phase in LB medium that contained 100 μg ampicillin/ml and 30 μg chloramphenicol/ml at 37°C, and recombinant HTkA or HTkB synthesis was then induced by adding isopropyl β-D-1-thiogalacto-pyranoside (500 μM final concentration) and continued incubation for 3 h at 37°C. The cells were harvested by centrifugation, resuspended (0.33 g wet cell pellet/ml) in 25 mM Tris–HCl (pH 7), 0.1 mM EDTA, 50 mM NaCl, lysozyme (100 μg/ml) added and the mixtures held ice for 30 min. Phenylmethanesulfonyl fluoride (Sigma, St. Louis, MO) was added (100 μg/ml) and cells were ruptured by repeated passage through a French press. The lysates were clarified by centrifugation at 4°C (60,000 g, 20 min), MgCl2 (5 mM) and DNase I (40 μg/ml) added, the mixtures incubated for 1 h at 37°C and then at 85°C for 20 min. Following further centrifugation (60,000 g, 30 min, 4°C), the supernatants generated were loaded onto 5 ml Hi-Trap heparin columns (GE Healthcare; Pataskala, OH). Recombinant HTkA and HTkB were eluted by passage of 10 column volumes of linear 50 to 500 mM, and 200 to 700 mM gradients of NaCl, respectively, dissolved in 25 mM Tris–HCl (pH 7). The eluate fractions that contained HTkA or HTkB were identified by Commassie-staining of the proteins in samples of the fractions separated by electrophoresis through 22% (w/v) denaturing polyacrylamide gels. These fractions were combined and the protein solution concentrated (final volume of ~0.5 ml) by centrifugation through a pre-rinsed Vivaspin 6 centrifugal concentrator (5 K molecular weight cut off; Sartorious AG, Bohemia, NY). The solutions were adjusted to contain 600 mM NaCl in 25 mM Tris–HCl (pH 7) and then passaged through Sephacryl S-100 HR 16/40 column (GE Healthcare) at a flow rate of 0.5 ml/min. Fractions that contained HTkA or HTkB, identified by Commassie-blue staining after electrophoresis of aliquots through 22% denaturing polyacrylamide gels, were pooled and concentrated (final volume of ~2 ml) by centrifugation again through pre-rinsed Vivaspin 6 centrifugal concentrators (5 K molecular weight cut off). These proteins solution, >99% purified archaeal histone, were dialyzed against in 25 mM Tris–HCl (pH 7), 500 mM NaCl, 50% (v/v) glycerol, and stored at −20°C.
Purification of eukaryotic histones
Chicken histone octamers were purified from erythrocytes by salt extraction and by hydroxyapatite column chromatography as previously described .
Archaeal and eukaryotic nucleosome assembly in vitro
Eukaryotic nucleosomes were assembled in vitro by salt dialysis in 200 μl reaction mixtures that contained 50 μg of genomic DNA and 30 μg of chicken histone octamers . Archaeal nucleosomes were reconstituted by mixing 50 μg of genomic DNA with 30 μg archaeal histone tetramers. The complexes formed were dialyzed into MN digestion buffer, and aliquots containing ~2.5 μg of DNA were incubated with 0.1 U MN/ μl for 5 min at 37°C. The MN digestions were stopped by addition of 125 mM EDTA, 200 mM NaCl, and the DNA molecules remaining were isolated by phenol:chloroform extraction, concentrated by ethanol precipitation and separated by electrophoresis through 6% polyacrylamide or 3.5% NuSieve agarose gels. Gel fragments that contained the ~60 bp, or ~147 bp, DNA molecules protected from MN digestion by incorporation into archaeal or eukaryotic nucleosomes, respectively, were excised and the DNA molecules extracted, purified and prepared for DNA sequencing as described above.
ABI SOLiD sequencing of DNA fragments
The ends of the ~60 bp and ~147 bp DNA fragments were repaired and 5’-phosphorylated by incubation in DNATerminator end-repair kits, as recommended by the manufacturer (Lucigen Corp., Middleton, WI). SOLiD adapters were ligated and the DNA molecules PCR amplified (very low cycle number) and sequenced by using the Applied Biosystems protocol for SOLiD fragment paired-end sequencing . Sequencing generated from 2 to 12 million unique reads which, depending on the experiment, equated to 60- to 800-fold coverage per 60 bp or 147 bp nucleosome footprint.
Analysis of DNA reads generated by pair-end sequencing
We first selected reads of length 55–65 bp (nucleosome of 60 bp lengths) to construct the center-weighted nucleosome occupancy scores. If a read length was odd, a Gaussian weight of exp(−0.5 * (d/10)2) was assigned to a position d bp away from the center of the read for d ≤ 25. If a read length was even, then positions i − 1 and i were treated as the possible nucleosome centers. For example, for a 60 nucleotide sequence i = 31, and so the two potential centers were at positions 30 and 31. Each center in an even read was, in turn, assigned a weight of 0.5 * exp(−0.5 * (d/10)2) for a position d bp away from the center and the values for both positions were then divided by 2. The center-weighted occupancy score for any given position was defined as the aggregation of the weighted scores from all reads. We identified well-defined peaks on the reads occupancy-curve as putative nucleosome centers by controlling the peak height and steepness simultaneously. To generate AA/AT/TA/TT frequency plots, after defining the nucleosome center positions based on the peaks of center-weighted occupancy score, dinucleotide frequency scores were computed as described by Segal et al.. We searched for a sequencing tag of length 60 bp nearest to the peak position in the +/−5 bp region. If no such read existed, we further searched for reads of lengths 61, 59, 62 and 58 bp sequentially within +/− 5 bp region of the peak until the first read was identified. The center of the identified read was treated as the nucleosome center to generate the AA/TT/TA/AT frequency plot. If no such read was identified in the +/−5 bp region, the peak position was treated as the true nucleosome center to generate the alignment. For paired-end MNase sequencing data for 147 bp long nucleosomes, read lengths of 137–157 bp were used. We followed a similar approach as described above and also employed by Brogaard et al. [21, 65] to identify the nucleosome centers.
Analyses of the DNA reads generated by single-end sequencing
For the single-end reads with known start position on the Watson strand, their end positions are unknown. However, since the DNA inserts are mapping nucleosomes, their length must be subject to the constraint of being around one nucleosome repeat length. Thus, if we observe a single-end read on the Watson strand at position i, we could practically assume that its end position should be within a region, say [i + a, i + b], and follows some distribution. For practical purpose, we let a = 51, b = 68. We further assumed that the start and end positions of the DNA inserts are independently distributed around the two edges of the nucleosome they map. Let ci + 51, …, ci + 68 be the Crick strand tag numbers in this region. Then the relative frequency defined as can be used to estimate the probability of a DNA insert ending at position i + k for k = 51, …, 68. Thus, if we observe w i single-end tags at position i from the Watson strand, then we could regard that we had observed w i paired-end tags ending at i + k for k = 51, …, 68 with respective frequency . Likewise, if we observe c i single-end tags at position i from the Crick strand, we would regard that there were c i paired-end tags ending at i − k for k = 51, …, 68 with respective frequency . By this calculation the observed data with single-end tags are converted approximately to a pseudo data set consisting of paired-end tags. The approach defined above for paired-end data was then used to define the center-weighted reads occupancy score and the nucleosome centers.
The sequences obtained and detailed descriptions of the computational analyses are available . The M. thermoautotrophicus and T. kodakarensis genome coordinates and RefSeq transcript annotations used were from the methTher1 and therkoda1 genome assemblies available on the Archaeal Genome Browser web site .
We gratefully acknowledge the life and achievements of Jonathan Widom. He was a mentor, colleague and friend who played a major role in the initial stages of this project. Sadly, he passed away before its completion.
We thank the staff of the Northwestern University Genomic Core for all the DNA sequencing. This research was supported by NIH grants GM075313 (WJ-P), GM098176 (JNR; TJS), GM100329 (TJS) and 2P20 RR020171 (YNF-M).
- Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E: Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol. 2008, 4: e1000216-10.1371/journal.pcbi.1000216.PubMed CentralView ArticlePubMed
- Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, Iyer VR: Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 2008, 6: e65-10.1371/journal.pbio.0060065.PubMed CentralView ArticlePubMed
- Jiang C, Pugh BF: Nucleosome positioning and gene regulation: advances through genomics. Nature Rev Genet. 2009, 10: 161-172.View ArticlePubMed
- Guan Y, Yao V, Tsui K, Gebbia M, Dunham MJ, Nislow C, Troyanskaya OG: Nucleosome-coupled expression differences in closely-related species. BMC Genomics. 2011, 12: 466-10.1186/1471-2164-12-466.PubMed CentralView ArticlePubMed
- Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J: A genomic code for nucleosome positioning. Nature. 2006, 442: 772-778. 10.1038/nature04979.PubMed CentralView ArticlePubMed
- Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, Segal E: The DNA-encoded nucleosome organization of a eukaryotic genome. Nature. 2009, 458: 362-366. 10.1038/nature07667.PubMed CentralView ArticlePubMed
- Yuan GC, Liu JS: Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput Biol. 2008, 4: e13-10.1371/journal.pcbi.0040013.PubMed CentralView ArticlePubMed
- Rapoport AE, Frenkel ZM, Trifonov EN: Nucleosome positioning pattern derived from oligonucleotide compositions of genomic sequences. J Biomol Struct Dynam. 2011, 28: 567-574. 10.1080/07391102.2011.10531243.View Article
- Sandman K, Reeve JN: Archaeal histones and the origin of the histone fold. Curr Opin Microbiol. 2006, 9: 520-525. 10.1016/j.mib.2006.08.003.View ArticlePubMed
- Cubonova L, Sandman K, Hallam SJ, Delong EF, Reeve JN: Histones in Crenarchaea. J Bacteriol. 2005, 187: 5482-5485. 10.1128/JB.187.15.5482-5485.2005.PubMed CentralView ArticlePubMed
- Friedrich-Jahn U, Aigner J, Langst G, Reeve JN, Huber H: Nanoarchaeal origin of histone H3?. J Bacteriol. 2009, 191: 1092-1096. 10.1128/JB.01431-08.PubMed CentralView ArticlePubMed
- Bailey KA, Pereira SL, Widom J, Reeve JN: Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. J Mol Biol. 2000, 303: 25-34. 10.1006/jmbi.2000.4128.View ArticlePubMed
- Cubonova L, Katano M, Kanai T, Atomi H, Reeve JN, Santangelo TJ: An archaeal histone is required for transformation of Thermococcus kodakarensis. J Bacteriol. 2012, 194: 6864-6874. 10.1128/JB.01523-12.PubMed CentralView Article
- Sandman K, Krzycki JA, Dobrinski B, Lurz R, Reeve JN: HMf, a DNA-binding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc Natl Acad Sci USA. 1990, 87: 5788-5791. 10.1073/pnas.87.15.5788.PubMed CentralView ArticlePubMed
- Samson R, Reeve JN: DNA binding proteins and chromatin. Archaea: Molecular and Cellular Biology. Edited by: Cavicchioli R. 2007, Washington, DC: ASM Press, 110-119.View Article
- Pereira SL, Grayling RA, Lurz R, Reeve JN: Archaeal nucleosomes. Proc Natl Acad Sci USA. 1997, 94: 12633-12637. 10.1073/pnas.94.23.12633.PubMed CentralView ArticlePubMed
- Bailey KA, Marc F, Sandman K, Reeve JN: Both DNA and histone fold sequences contribute to archaeal nucleosome stability. J Biol Chem. 2002, 277: 9293-9301. 10.1074/jbc.M110029200.View ArticlePubMed
- Marc F, Sandman K, Lurz R, Reeve JN: Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J Biol Chem. 2002, 277: 30879-30886. 10.1074/jbc.M203674200.View ArticlePubMed
- Kaplan N, Moore I, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, Hughes TR, Lieb JD, Widom J, Segal E: Nucleosome sequence preferences influence in vivo nucleosome organization. Nat Struct Mol Biol. 2010, 17: 918-920. 10.1038/nsmb0810-918. author reply 920–922PubMed CentralView ArticlePubMed
- Gaffney DJ, McVicker G, Pai AA, Fondufe-Mittendorf YN, Lewellen N, Michelini K, Widom J, Gilad Y, Pritchard JK: Controls of nucleosome positioning in the human genome. PLoS Genet. 2012, 8: e1003036-10.1371/journal.pgen.1003036.PubMed CentralView ArticlePubMed
- Brogaard K, Xi L, Wang JP, Widom J: A map of nucleosome positions in yeast at base-pair resolution. Nature. 2012, 486: 496-501.PubMed CentralPubMed
- Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C: A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet. 2007, 39: 1235-1244. 10.1038/ng2117.View ArticlePubMed
- Segal E, Widom J: Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol. 2009, 19: 65-71. 10.1016/j.sbi.2009.01.004.PubMed CentralView ArticlePubMed
- Iyer V, Struhl K: Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995, 14: 2570-2579.PubMed CentralPubMed
- Lascaris RF, Groot E, Hoen PB, Mager WH, Planta RJ: Different roles for abf1p and a T-rich promoter element in nucleosome organization of the yeast RPS28A gene. Nucl Acids Res. 2000, 28: 1390-1396. 10.1093/nar/28.6.1390.PubMed CentralView ArticlePubMed
- Morohashi N, Yamamoto Y, Kuwana S, Morita W, Shindo H, Mitchell AP, Shimizu M: Effect of sequence-directed nucleosome disruption on cell-type-specific repression by alpha2/Mcm1 in the yeast genome. Euk Cell. 2006, 5: 1925-1933. 10.1128/EC.00105-06.View Article
- Bao Y, White CL, Luger K: Nucleosome core particles containing a poly(dA.dT) sequence element exhibit a locally distorted DNA structure. J Mol Biol. 2006, 361: 617-624. 10.1016/j.jmb.2006.06.051.View ArticlePubMed
- Struhl K: Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast. Proc Natl Acad Sci USA. 1985, 82: 8419-8423. 10.1073/pnas.82.24.8419.PubMed CentralView ArticlePubMed
- Nelson HC, Finch JT, Luisi BF, Klug A: The structure of an oligo(dA)-oligo(dT) tract and its biological implications. Nature. 1987, 330: 221-226. 10.1038/330221a0.View ArticlePubMed
- Suter B, Schnappauf G, Thoma F: Poly(dA.dT) sequences exist as rigid DNA structures in nucleosome-free yeast promoters in vivo. Nucl Acids Res. 2000, 28: 4083-4089. 10.1093/nar/28.21.4083.PubMed CentralView ArticlePubMed
- Anderson JD, Widom J: Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol Cell Biol. 2001, 21: 3830-3839. 10.1128/MCB.21.11.3830-3839.2001.PubMed CentralView ArticlePubMed
- Sekinger EA, Moqtaderi Z, Struhl K: Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol Cell. 2005, 18: 735-748. 10.1016/j.molcel.2005.05.003.View ArticlePubMed
- Ioshikhes IP, Albert I, Zanton SJ, Pugh BF: Nucleosome positions predicted through comparative genomics. Nat Genet. 2006, 38: 1210-1215. 10.1038/ng1878.View ArticlePubMed
- Fukui T, Atomi H, Kanai T, Matsumi R, Fujiwara S, Imanaka T: Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res. 2005, 15: 352-363. 10.1101/gr.3003105.PubMed CentralView ArticlePubMed
- Grohmann D, Werner F: Recent advances in the understanding of archaeal transcription. Curr Opin Microbiol. 2011, 14: 328-334. 10.1016/j.mib.2011.04.012.View ArticlePubMed
- Santangelo TJ, Reeve JN: Archaeal RNA polymerase is sensitive to intrinsic termination directed by transcribed and remote sequences. J Mol Biol. 2006, 355: 196-210. 10.1016/j.jmb.2005.10.062.View ArticlePubMed
- Nishida H, Kondo S, Matsumoto T, Suzuki Y, Yoshikawa H, Taylor TD, Sugiyama J: Characteristics of nucleosomes and linker DNA regions on the genome of the basidiomycete Mixia osmundae revealed by mono- and dinucleosome mapping. Open Biol. 2012, 2: 120043-10.1098/rsob.120043.PubMed CentralView ArticlePubMed
- Peckham HE, Thurman RE, Fu Y, Stamatoyannopoulos JA, Noble WS, Struhl K, Weng Z: Nucleosome positioning signals in genomic DNA. Genome Res. 2007, 17: 1170-1177. 10.1101/gr.6101007.PubMed CentralView ArticlePubMed
- Archaeal Genome Browser. http://archaea.ucsc.edu,
- Santangelo TJ, Cubonova L, Matsumi R, Atomi H, Imanaka T, Reeve JN: Polarity in archaeal operon transcription in Thermococcus kodakaraensis. J Bacteriol. 2008, 190: 2244-2248. 10.1128/JB.01811-07.PubMed CentralView ArticlePubMed
- Smith DR, Doucette-Stamm LA, Deloughery C, Lee H, Dubois J, Aldredge T, Bashirzadeh R, Blakely D, Cook R, Gilbert K, Harrison D, Hoang L, Keagle P, Lumm W, Pothier B, Qiu D, Spadafora R, Vicaire R, Wang Y, Wierzbowski J, Gibson R, Jiwani N, Caruso A, Bush D, Reeve JN: Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics. J Bacteriol. 1997, 179: 7135-7155.PubMed CentralPubMed
- UCSC Genome Browser on Thermococcus kodakarensis May 2004 Assembly (therKoda1). 2004, http://archaea.ucsc.edu/lists/therKoda1/refSeq-list.html, May Assembly (therKoda1),
- Gupta S, Dennis J, Thurman RE, Kingston R, Stamatoyannopoulos JA, Noble WS: Predicting human nucleosome occupancy from primary sequence. PLoS Comput Biol. 2008, 4: e1000134-10.1371/journal.pcbi.1000134.PubMed CentralView ArticlePubMed
- Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, Liu XS, Struhl K: Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol. 2009, 16: 847-852. 10.1038/nsmb.1636.PubMed CentralView ArticlePubMed
- Ioshikhes I, Hosid S, Pugh BF: Variety of genomic DNA patterns for nucleosome positioning. Genome Res. 2011, 21: 1863-1871. 10.1101/gr.116228.110.PubMed CentralView ArticlePubMed
- Tillo D, Hughes TR: G + C content dominates intrinsic nucleosome occupancy. BMC Bioinforma. 2009, 10: 442-10.1186/1471-2105-10-442.View Article
- Visnapuu ML, Greene EC: Single-molecule imaging of DNA curtains reveals intrinsic energy landscapes for nucleosome deposition. Nat Struct Mol Biol. 2009, 16: 1056-1062. 10.1038/nsmb.1655.PubMed CentralView ArticlePubMed
- Lankas F, Sponer J, Langowski J, Cheatham TE: DNA basepair step deformability inferred from molecular dynamics simulations. Biophys J. 2003, 85: 2872-2883. 10.1016/S0006-3495(03)74710-9.PubMed CentralView ArticlePubMed
- Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ: Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997, 389: 251-260. 10.1038/38444.View ArticlePubMed
- Luger K, Mader A, Sargent DF, Richmond TJ: The atomic structure of the nucleosome core particle. J Biomol Struct Dyn. 2000, 17 (Suppl 1): 185-188.View ArticlePubMed
- Decanniere K, Babu AM, Sandman K, Reeve JN, Heinemann U: Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. J Mol Biol. 2000, 303: 35-47. 10.1006/jmbi.2000.4104.View ArticlePubMed
- Soares DJ, Sandman K, Reeve JN: Mutational analysis of archaeal histone-DNA interactions. J Mol Biol. 2000, 297: 39-47. 10.1006/jmbi.2000.3546.View ArticlePubMed
- French SL, Santangelo TJ, Beyer AL, Reeve JN: Transcription and translation are coupled in Archaea. Mol Biol Evol. 2007, 24: 893-895. 10.1093/molbev/msm007.View ArticlePubMed
- Wilkinson SP, Ouhammouch M, Geiduschek EP: Transcriptional activation in the context of repression mediated by archaeal histones. Proc Natl Acad Sci USA. 2010, 107: 6777-6781. 10.1073/pnas.1002360107.PubMed CentralView ArticlePubMed
- Xie Y, Reeve JN: Transcription by an archaeal RNA polymerase is slowed but not blocked by an archaeal nucleosome. J Bacteriol. 2004, 186: 3492-3498. 10.1128/JB.186.11.3492-3498.2004.PubMed CentralView ArticlePubMed
- Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ: Genome-scale identification of nucleosome positions in S. cerevisiae. Science. 2005, 309: 626-630. 10.1126/science.1112178.View ArticlePubMed
- Ammar R, Torti D, Tsui K, Gebbia M, Durbic T, Bader GD, Giaever G, Nislow C: Chromatin is an ancient innovation conserved between Archaea and Eukarya. Elife. 2012, 1: e00078-10.7554/eLife.00078.PubMed CentralView ArticlePubMed
- Hartman AL, Norais C, Badger JH, Delmas S, Haldenby S, Madupu R, Robinson J, Khouri H, Ren Q, Lowe TM, Maupin-Furlow J, Pohlschroder M, Daniels C, Pfeiffer F, Allers T, Eisen JA: The complete genome sequence of Haloferax volcanii DS2, a model archaeon. PLoS One. 2010, 5: e9605-10.1371/journal.pone.0009605.PubMed CentralView ArticlePubMed
- Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF: Nucleosome organization in the Drosophila genome. Nature. 2008, 453: 358-362. 10.1038/nature06929.PubMed CentralView ArticlePubMed
- Field Y, Fondufe-Mittendorf Y, Moore IK, Mieczkowski P, Kaplan N, Lubling Y, Lieb JD, Widom J, Segal E: Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nat Genet. 2009, 41: 438-445. 10.1038/ng.324.PubMed CentralView ArticlePubMed
- Rapoport AE, Trivonof EF: “Anticipated” nucleosome positioning pattern in prokaryotes. Gene. 2011, 488: 41-45. 10.1016/j.gene.2011.08.002.View ArticlePubMed
- Reeve JN: Archaeal chromatin and transcription. Mol Microbiol. 2003, 48: 587-598. 10.1046/j.1365-2958.2003.03439.x.View ArticlePubMed
- Feng HP, Scherl DS, Widom J: Lifetime of the histone octamer studied by continuous-flow quasielastic light scattering: test of a model for nucleosome transcription. Biochemistry. 1993, 32: 7824-7831. 10.1021/bi00081a030.View ArticlePubMed
- Applied Biosystems protocol for SOLiD sequencing. http://tools.invitrogen.com/content/sfs/manuals/SOLiD4_Library_Preparation_man.pdf,
- Brogaard KR, Xi L, Wang JP, Widom J: A chemical approach to mapping nucleosomes at base pair resolution in yeast. Meth Enzymol. 2012, 513: 315-334.View ArticlePubMed
- Genome-database of Methanobacterium thermoautotrophicum and Thermococcus kodakarensis sequenced nucleosomal reads. 2012, http://ncode.northwestern.edu,
- UCSC Genome Browser on Methanobacterium thermoautotrophicum Aug 1997 Assembly (methTher1). 1997, http://archaea.ucsc.edu/lists/methTher1/refSeq-list.html, Aug Assembly (methTher1),
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