Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution
Identifieur interne : 001F49 ( Istex/Corpus ); précédent : 001F48; suivant : 001F50Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution
Auteurs : Kathryn A. Bailey ; Suzette L. Pereira ; Jonathan Widom ; John N. ReeveSource :
- Journal of Molecular Biology [ 0022-2836 ] ; 2000.
English descriptors
- KwdEn :
- Teeft :
- Acad, Archaeal, Archaeal histone, Archaeal histones, Archaeal nucleosome, Archaeal nucleosome assembly, Archaeal nucleosomes, Biol, Complete genome sequence, Crothers, Digestion, Dinucleotide, Dinucleotides, Eucaryal, Fervidus, Gene expression, Genome, Genome sequence evolution, Genome sequences, Genomic, Histone, Kawarabayashi, Lateral gene transfer, Lowary, Lowary widom, Luger, Methanococcus jannaschii, Methanothermus, Methanothermus fervidus, Micrococcal nuclease, Molecule, Natl, Natl acad, Nucleosome, Nucleosome assembly, Nucleosome core, Nucleosomes, Pereira, Pereira reeve, Power spectra, Proc, Reaction mixtures, Reeve, Restriction fragments, Rhmfb, Sandman reeve, Sequencing, Shrader, Shrader crothers, Thastrom, Thermoautotrophicum, Widlund, Widom, Woese.
Abstract
Abstract: Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones have almost identical histone folds. Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from Methanothermus fervidus) into archaeal nucleosomes from a mixture of ∼1014 random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN3AA or TA)n]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of Eucarya and the histone-containing Euryarchaeota, but not in the genomes of Bacteria and Crenarchaeota, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarchaeota. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.
Url:
DOI: 10.1006/jmbi.2000.4128
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ISTEX:A579D5A93A4D6039E7699E68A910DC4948907066Le document en format XML
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Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from Methanothermus fervidus) into archaeal nucleosomes from a mixture of ∼1014 random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN3AA or TA)n]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of Eucarya and the histone-containing Euryarchaeota, but not in the genomes of Bacteria and Crenarchaeota, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarchaeota. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.</div></front></TEI><istex><corpusName>elsevier</corpusName><keywords><teeft><json:string>histone</json:string><json:string>archaeal</json:string><json:string>genome</json:string><json:string>nucleosome</json:string><json:string>nucleosomes</json:string><json:string>reeve</json:string><json:string>widom</json:string><json:string>archaeal nucleosomes</json:string><json:string>eucaryal</json:string><json:string>biol</json:string><json:string>rhmfb</json:string><json:string>dinucleotide</json:string><json:string>dinucleotides</json:string><json:string>pereira</json:string><json:string>lowary</json:string><json:string>proc</json:string><json:string>archaeal histone</json:string><json:string>fervidus</json:string><json:string>thermoautotrophicum</json:string><json:string>natl acad</json:string><json:string>natl</json:string><json:string>acad</json:string><json:string>digestion</json:string><json:string>thastrom</json:string><json:string>pereira reeve</json:string><json:string>lowary widom</json:string><json:string>crothers</json:string><json:string>widlund</json:string><json:string>methanothermus</json:string><json:string>kawarabayashi</json:string><json:string>sequencing</json:string><json:string>genomic</json:string><json:string>woese</json:string><json:string>shrader</json:string><json:string>complete genome sequence</json:string><json:string>archaeal nucleosome</json:string><json:string>sandman reeve</json:string><json:string>shrader crothers</json:string><json:string>genome sequences</json:string><json:string>molecule</json:string><json:string>archaeal nucleosome assembly</json:string><json:string>methanothermus fervidus</json:string><json:string>power spectra</json:string><json:string>reaction mixtures</json:string><json:string>luger</json:string><json:string>methanococcus jannaschii</json:string><json:string>restriction fragments</json:string><json:string>micrococcal nuclease</json:string><json:string>nucleosome core</json:string><json:string>genome sequence evolution</json:string><json:string>lateral gene transfer</json:string><json:string>nucleosome assembly</json:string><json:string>archaeal histones</json:string><json:string>gene expression</json:string></teeft></keywords><author><json:item><name>Kathryn A Bailey</name><affiliations><json:string>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</json:string></affiliations></json:item><json:item><name>Suzette L Pereira</name><affiliations><json:string>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</json:string></affiliations></json:item><json:item><name>Jonathan Widom</name><affiliations><json:string>Department of Biochemistry Molecular Biology and Cell Biology, Northwestern University, Evanston IL 60208-3500, USA</json:string></affiliations></json:item><json:item><name>John N Reeve</name><affiliations><json:string>E-mail: reeve.2@osu.edu</json:string><json:string>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</json:string></affiliations></json:item></author><subject><json:item><lang><json:string>eng</json:string></lang><value>Regular article</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>Archaea</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>SELEX</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>nucleosome positioning</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>genome evolution</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>HMfB</value></json:item></subject><arkIstex>ark:/67375/6H6-CG6PZT6G-9</arkIstex><language><json:string>eng</json:string></language><originalGenre><json:string>Full-length article</json:string></originalGenre><abstract>Abstract: Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones have almost identical histone folds. Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from Methanothermus fervidus) into archaeal nucleosomes from a mixture of ∼1014 random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN3AA or TA)n]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of Eucarya and the histone-containing Euryarchaeota, but not in the genomes of Bacteria and Crenarchaeota, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarchaeota. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.</abstract><qualityIndicators><refBibsNative>true</refBibsNative><abstractWordCount>271</abstractWordCount><abstractCharCount>1930</abstractCharCount><keywordCount>6</keywordCount><score>10</score><pdfWordCount>6498</pdfWordCount><pdfCharCount>40563</pdfCharCount><pdfVersion>1.3</pdfVersion><pdfPageCount>10</pdfPageCount><pdfPageSize>612 x 792 pts (letter)</pdfPageSize></qualityIndicators><title>Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution</title><pmid><json:string>11021967</json:string></pmid><pii><json:string>S0022-2836(00)94128-7</json:string></pii><genre><json:string>research-article</json:string></genre><host><title>Journal of Molecular Biology</title><language><json:string>unknown</json:string></language><publicationDate>2000</publicationDate><issn><json:string>0022-2836</json:string></issn><pii><json:string>S0022-2836(00)X0206-9</json:string></pii><volume>303</volume><issue>1</issue><pages><first>25</first><last>34</last></pages><genre><json:string>journal</json:string></genre></host><namedEntities><unitex><date><json:string>2000</json:string></date><geogName></geogName><orgName><json:string>Northwestern University</json:string><json:string>Promega Corp</json:string><json:string>Integrated DNA Technologies</json:string><json:string>Promega Corp., Madison</json:string><json:string>Department of Biochemistry Molecular Biology and Cell Biology</json:string><json:string>NIH</json:string></orgName><orgName_funder><json:string>NIH</json:string></orgName_funder><orgName_provider></orgName_provider><persName><json:string>Kathryn A. Bailey</json:string><json:string>John N. Reeve</json:string><json:string>Jonathan Widom</json:string><json:string>Suzette L. Pereira</json:string></persName><placeName><json:string>Foster City</json:string><json:string>IA</json:string><json:string>Madison</json:string><json:string>CA</json:string><json:string>WI</json:string></placeName><ref_url><json:string>http://www.biosci.ohio-state.edu/</json:string><json:string>http://niji.imb.nrc.ca/sulfhome</json:string><json:string>http://www.biosci.ohiostate.edu/</json:string><json:string>http://www.idealibrary.com</json:string></ref_url><ref_bibl><json:string>Lowary & Ê È Widom, 1998</json:string><json:string>Tuerk & Gold, 1990</json:string><json:string>Musgrave et al., 1991</json:string><json:string>Bolshoy, 1995</json:string><json:string>Woese et al., 1990, 2000</json:string><json:string>Svaren & Horz, 1996</json:string><json:string>Bult et al., 1996</json:string><json:string>Fleishmann et al., 1995</json:string><json:string>Widlund et al., 1999</json:string><json:string>Soares et al., 2000</json:string><json:string>Bult et al, 1996</json:string><json:string>Ê È Bolshoy, 1995</json:string><json:string>Sandman & Reeve, 1999</json:string><json:string>Pereira & Reeve, 1999</json:string><json:string>Zhu et al., 1998</json:string><json:string>Stevens et al., 1998</json:string><json:string>Lowary & Widom, 1998</json:string><json:string>Cole et al., 1998</json:string><json:string>Kunst et al., 1997</json:string><json:string>Hayes & Wolffe, 1993</json:string><json:string>Hayes et al., 1991</json:string><json:string>Klenk et al., 1997</json:string><json:string>Deckert et al, 1998</json:string><json:string>Satchwell et al., 1986</json:string><json:string>Sandman & Reeve, 1998</json:string><json:string>Nelson et al., 1999</json:string><json:string>Press et al., 1986</json:string><json:string>Herzel et al., 1999</json:string><json:string>Klenk et al. 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(1995)</json:string><json:string>Pereira et al., 1997</json:string><json:string>Pihl et al., 1994</json:string><json:string>Ph, Kawarabayashi et al., 1998</json:string><json:string>Bailey, 2000</json:string><json:string>Widom, 1996</json:string><json:string>Widlund et al.</json:string><json:string>Kawarabayashi et al., 1999</json:string><json:string>Stephens et al., 1998</json:string><json:string>Ioshikhes et al., 1992, 1996</json:string><json:string>Alilat et al., 1999</json:string><json:string>Bina, 1994</json:string><json:string>Luger et al., 1997</json:string><json:string>Widlund et al., 1997, 1999</json:string><json:string>Mt, Smith et al., 1997</json:string><json:string>Deckert et al., 1998</json:string><json:string>Minsky et al., 1997</json:string><json:string>Sandman et al., 1990, 1998</json:string><json:string>Kawarabayashi et al., 1998</json:string><json:string>Hamiche et al., 1996</json:string></ref_bibl><bibl></bibl></unitex></namedEntities><ark><json:string>ark:/67375/6H6-CG6PZT6G-9</json:string></ark><categories><wos><json:string>1 - science</json:string><json:string>2 - biochemistry & molecular biology</json:string></wos><scienceMetrix><json:string>1 - health sciences</json:string><json:string>2 - biomedical research</json:string><json:string>3 - biochemistry & molecular biology</json:string></scienceMetrix><scopus><json:string>1 - Life Sciences</json:string><json:string>2 - Biochemistry, Genetics and Molecular Biology</json:string><json:string>3 - Molecular Biology</json:string></scopus><inist><json:string>1 - sciences appliquees, technologies et medecines</json:string><json:string>2 - sciences biologiques et medicales</json:string><json:string>3 - sciences biologiques fondamentales et appliquees. psychologie</json:string><json:string>4 - biochimie analytique, structurale et metabolique</json:string></inist></categories><publicationDate>2000</publicationDate><copyrightDate>2000</copyrightDate><doi><json:string>10.1006/jmbi.2000.4128</json:string></doi><id>A579D5A93A4D6039E7699E68A910DC4948907066</id><score>1</score><fulltext><json:item><extension>pdf</extension><original>true</original><mimetype>application/pdf</mimetype><uri>https://api.istex.fr/ark:/67375/6H6-CG6PZT6G-9/fulltext.pdf</uri></json:item><json:item><extension>zip</extension><original>false</original><mimetype>application/zip</mimetype><uri>https://api.istex.fr/ark:/67375/6H6-CG6PZT6G-9/bundle.zip</uri></json:item><istex:fulltextTEI uri="https://api.istex.fr/ark:/67375/6H6-CG6PZT6G-9/fulltext.tei"><teiHeader><fileDesc><titleStmt><title level="a" type="main" xml:lang="en">Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution</title></titleStmt><publicationStmt><authority>ISTEX</authority><publisher scheme="https://scientific-publisher.data.istex.fr">ELSEVIER</publisher><availability><licence><p>©2000 Academic Press</p></licence><p scheme="https://loaded-corpus.data.istex.fr/ark:/67375/XBH-HKKZVM7B-M">elsevier</p></availability><date>2000</date></publicationStmt><notesStmt><note type="research-article" scheme="https://content-type.data.istex.fr/ark:/67375/XTP-1JC4F85T-7">research-article</note><note type="journal" scheme="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</note><note>Edited by T. Richmond</note><note type="content">Section title: Regular article</note><note type="content">Figure 1: Structure of cycle 0 DNA molecules, rHMfB affinities and consensus of cycle 8 sequences. (a) Each cycle 0 molecule had a 60 bp region of random-sequence (N60) flanked by the 25 bp fixed sequences (25L and 25R) shown. (b) Electrophoretic separation of cycle 0 DNA from archaeal nucleosomes (rHMfB-DNA) assembled at increasing rHMfB to DNA ratios. (c) Comparison of the affinities of cycle 0 DNA, cycle 8 clones 5 and 9, M. fervidus 7 S RNA encoding sequence (Pereira & Reeve, 1999) and (CTG)6 repeat sequence (Sandman & Reeve, 1999) for rHMfB. (d) The sequences show by relative font size the frequency with which A, C, G or T occurred at each location in the 89 different 60 bp cycle 8 N60 sequences. The most to least prevalent nucleotide at each location, relative to 25L, are shown in the sequences from top to bottom. The font size equivalent to 80 % occupancy of a site by only one nucleotide is indicated.</note><note type="content">Figure 2: Micrococcal nuclease (MN) digestion and cycle 8 DNA positioning of an archaeal nucleosome. (a) Archaeal nucleosomes, assembled using the cycle 8 molecule with the sequence shown in panel (b), were exposed to MN for 0, 1, 5, 15 and 45 minutes. DNA fragments protected from MN digestion were separated by PAGE and visualized by autoradiography. Control (C) exposure of the DNA to MN for two minutes in the absence of rHMfB resulted in complete digestion. High-resolution electrophoresis through DNA sequencing gels demonstrated that the DNA fragments that accumulated after extended MN digestion were 58 bp. (b) None of the 58 bp MN protected DNA fragments retained the Bam H1 and Eco RI cleavage sites, and Alu I digestion generated only discrete 10(±1) bp and 48(±1) bp restriction fragments. Archaeal nucleosome assembly therefore either occurred at three overlapping sites, displaced by 1 bp as indicated by the ovals, or more likely at one site with the ±1 bp difference reflecting MN nicking of histone-bound DNA near the entry and exit sites of the nucleosome (Hayes & Wolffe, 1993). The vertical arrows identify the sites of fusion of the N60 sequence with 25L and 25R.</note><note type="content">Figure 3: Fourier-transform analysis of dinucleotides in the cycle 8 sequences. As shown, strong signals were present for AA (=TT), TA and GC and a weaker signal for CG at an ∼0.10 bp−1 (∼10 bp) periodicity in the non-redundant database of 111 cycle 8 sequences with subsidiary maxima in the TA and GC transforms reflecting higher harmonics of the ∼0.10 bp−1 signal. The continuous lines with (o) data points are the experimental results, and the lines with error bars are the mean and standard deviation values, respectively, of 100 identical analyses performed on computer-randomized versions of the cycle 8 sequences.</note><note type="content">Figure 4: Real-space correlation analyses of the spatial relationships between dinucleotides in cycle 8 sequences. The spatial relationships between all pairs of dinucleotides in the non-redundant database of cycle 8 sequences were determined for all distances from 1 to 55 bp (Lowary & Widom, 1998). The most-strongly correlated dinucleotide pairs, plotted as a function of the distance (in bp) of the second dinucleotide from the first, are shown. Namely, AA, TA and GC repeated at distances of ∼10, 20 and 30 bp, AA followed by TA at distances of ∼10, 20 and 30 bp, and GC followed by AA or TA at distances of ∼5, 15 and 25 bp. Also shown as lines with error bars are the mean and standard deviations of random expectation (generated from randomized sequences as in Figure 3).</note><note type="content">Figure 5: Power spectra for the AA dinucleotide in archaeal and bacterial genome sequences. The results show data from analyses of the complete euryarchaeal genome sequences of the histone containing (+) Archaeoglobus fulgidus (Af; (Klenk et al. (1997)), Methanococcus jannaschii (Mj, Bult et al. (1996), M. thermoautotrophicum (Mt, Smith et al., 1997), Pyrococcus abyssi (Pa, (http://www.genoscope.cns.fr/Pab)) and Pyrococcus horikoshii (Ph, Kawarabayashi et al., 1998), and of the crenarchaeal and bacterial genomes of Aeropyrum pernix (Ap, Kawarabayashi et al., 1999) and Thermotoga maritima (Tm, Nelson et al., 1999), respectively, that do not (−) contain histones. Analyses of genome sequences from Sulfolobus solfataricus P2 (http://niji.imb.nrc.ca/sulfhome), and additional bacterial genome sequences (Kunst et al., 1997; Cole et al., 1998; Deckert et al., 1998; Stevens et al., 1998) confirmed the presence of a spatial periodicity peak at 0.09 bp−1 (∼11 bp repeat), but absence of the peak at 0.1 bp−1 (∼10.1 bp repeat) that is present in the euryarchaeal genomes. A difference in AA spatial periodicities in bacterial versus archaeal genomes was noted previously (Herzel et al., 1999) but crenarchaeal genome sequences were not then available. Power spectra are shown on a relative scale with a small constant increment added to space the curves for visual clarity.</note></notesStmt><sourceDesc><biblStruct type="inbook"><analytic><title level="a" type="main" xml:lang="en">Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution</title><author xml:id="author-0000"><persName><forename type="first">Kathryn A</forename><surname>Bailey</surname></persName><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation></author><author xml:id="author-0001"><persName><forename type="first">Suzette L</forename><surname>Pereira</surname></persName><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation></author><author xml:id="author-0002"><persName><forename type="first">Jonathan</forename><surname>Widom</surname></persName><affiliation>Department of Biochemistry Molecular Biology and Cell Biology, Northwestern University, Evanston IL 60208-3500, USA</affiliation></author><author xml:id="author-0003"><persName><forename type="first">John N</forename><surname>Reeve</surname></persName><email>reeve.2@osu.edu</email><note type="correspondence"><p>Corresponding author</p></note><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation></author><idno type="istex">A579D5A93A4D6039E7699E68A910DC4948907066</idno><idno type="ark">ark:/67375/6H6-CG6PZT6G-9</idno><idno type="DOI">10.1006/jmbi.2000.4128</idno><idno type="PII">S0022-2836(00)94128-7</idno></analytic><monogr><title level="j">Journal of Molecular Biology</title><title level="j" type="abbrev">YJMBI</title><idno type="pISSN">0022-2836</idno><idno type="PII">S0022-2836(00)X0206-9</idno><imprint><publisher>ELSEVIER</publisher><date type="published" when="2000"></date><biblScope unit="volume">303</biblScope><biblScope unit="issue">1</biblScope><biblScope unit="page" from="25">25</biblScope><biblScope unit="page" to="34">34</biblScope></imprint></monogr></biblStruct></sourceDesc></fileDesc><profileDesc><creation><date>2000</date></creation><langUsage><language ident="en">en</language></langUsage><abstract xml:lang="en"><p>Abstract: Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones have almost identical histone folds. Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from Methanothermus fervidus) into archaeal nucleosomes from a mixture of ∼1014 random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN3AA or TA)n]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of Eucarya and the histone-containing Euryarchaeota, but not in the genomes of Bacteria and Crenarchaeota, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarchaeota. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.</p></abstract><textClass><keywords scheme="keyword"><list><head>article-category</head><item><term>Regular article</term></item></list></keywords></textClass><textClass xml:lang="en"><keywords scheme="keyword"><list><head>Keywords</head><item><term>Archaea</term></item><item><term>SELEX</term></item><item><term>nucleosome positioning</term></item><item><term>genome evolution</term></item><item><term>HMfB</term></item></list></keywords></textClass></profileDesc><revisionDesc><change when="2000-08-17">Modified</change><change when="2000">Published</change></revisionDesc></teiHeader></istex:fulltextTEI><json:item><extension>txt</extension><original>false</original><mimetype>text/plain</mimetype><uri>https://api.istex.fr/ark:/67375/6H6-CG6PZT6G-9/fulltext.txt</uri></json:item></fulltext><metadata><istex:metadataXml wicri:clean="Elsevier, elements deleted: ce:floats; body; tail"><istex:xmlDeclaration>version="1.0" encoding="utf-8"</istex:xmlDeclaration><istex:docType PUBLIC="-//ES//DTD journal article DTD version 4.5.2//EN//XML" URI="art452.dtd" name="istex:docType"><istex:entity SYSTEM="gr1a" NDATA="IMAGE" name="GR1a"></istex:entity><istex:entity SYSTEM="gr1b" NDATA="IMAGE" name="GR1b"></istex:entity><istex:entity SYSTEM="gr2" NDATA="IMAGE" name="GR2"></istex:entity><istex:entity SYSTEM="gr3" NDATA="IMAGE" name="GR3"></istex:entity><istex:entity SYSTEM="gr4" NDATA="IMAGE" name="GR4"></istex:entity><istex:entity SYSTEM="gr5" NDATA="IMAGE" name="GR5"></istex:entity></istex:docType><istex:document><converted-article version="4.5.2" docsubtype="fla" xml:lang="en"><item-info><jid>YJMBI</jid><aid>94128</aid><ce:pii>S0022-2836(00)94128-7</ce:pii><ce:doi>10.1006/jmbi.2000.4128</ce:doi><ce:copyright type="full-transfer" year="2000">Academic Press</ce:copyright><ce:doctopics><ce:doctopic><ce:text>Regular article</ce:text></ce:doctopic></ce:doctopics></item-info><head><ce:dochead><ce:textfn>Regular article</ce:textfn></ce:dochead><ce:title>Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution<ce:cross-ref refid="FN1"><ce:sup>1</ce:sup></ce:cross-ref><ce:footnote id="FN1"><ce:label>1</ce:label><ce:note-para><ce:bold><ce:italic>Edited by T. Richmond</ce:italic></ce:bold></ce:note-para></ce:footnote></ce:title><ce:author-group><ce:author><ce:given-name>Kathryn A</ce:given-name><ce:surname>Bailey</ce:surname><ce:cross-ref refid="AFF1"><ce:sup>1</ce:sup></ce:cross-ref></ce:author><ce:author><ce:given-name>Suzette L</ce:given-name><ce:surname>Pereira</ce:surname><ce:cross-ref refid="AFF1"><ce:sup>1</ce:sup></ce:cross-ref></ce:author><ce:author><ce:given-name>Jonathan</ce:given-name><ce:surname>Widom</ce:surname><ce:cross-ref refid="AFF2"><ce:sup>2</ce:sup></ce:cross-ref></ce:author><ce:author><ce:given-name>John N</ce:given-name><ce:surname>Reeve</ce:surname><ce:cross-ref refid="AFF1"><ce:sup>1</ce:sup></ce:cross-ref><ce:cross-ref refid="COR1">*</ce:cross-ref><ce:e-address>reeve.2@osu.edu</ce:e-address></ce:author><ce:affiliation id="AFF1"><ce:label>1</ce:label><ce:textfn>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</ce:textfn></ce:affiliation><ce:affiliation id="AFF2"><ce:label>2</ce:label><ce:textfn>Department of Biochemistry Molecular Biology and Cell Biology, Northwestern University, Evanston IL 60208-3500, USA</ce:textfn></ce:affiliation><ce:correspondence id="COR1"><ce:label>*</ce:label><ce:text>Corresponding author</ce:text></ce:correspondence></ce:author-group><ce:date-received day="15" month="5" year="2000"></ce:date-received><ce:date-revised day="17" month="8" year="2000"></ce:date-revised><ce:date-accepted day="23" month="8" year="2000"></ce:date-accepted><ce:abstract><ce:section-title>Abstract</ce:section-title><ce:abstract-sec><ce:simple-para>Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones have almost identical histone folds. Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from <ce:italic>Methanothermus fervidus</ce:italic>) into archaeal nucleosomes from a mixture of ∼10<ce:sup>14</ce:sup> random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN<ce:inf>3</ce:inf>AA or TA)<ce:inf>n</ce:inf>]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of <ce:italic>Eucarya</ce:italic> and the histone-containing <ce:italic>Euryarchaeota</ce:italic>, but not in the genomes of <ce:italic>Bacteria</ce:italic> and <ce:italic>Crenarchaeota</ce:italic>, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the <ce:italic>Crenarchaeota</ce:italic>. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.</ce:simple-para></ce:abstract-sec></ce:abstract><ce:keywords><ce:section-title>Keywords</ce:section-title><ce:keyword><ce:text><ce:italic>Archaea</ce:italic></ce:text></ce:keyword><ce:keyword><ce:text>SELEX</ce:text></ce:keyword><ce:keyword><ce:text>nucleosome positioning</ce:text></ce:keyword><ce:keyword><ce:text>genome evolution</ce:text></ce:keyword><ce:keyword><ce:text>HMfB</ce:text></ce:keyword></ce:keywords></head></converted-article></istex:document></istex:metadataXml><mods version="3.6"><titleInfo lang="en"><title>Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution</title></titleInfo><titleInfo type="alternative" lang="en" contentType="CDATA"><title>Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution</title></titleInfo><name type="personal"><namePart type="given">Kathryn A</namePart><namePart type="family">Bailey</namePart><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Suzette L</namePart><namePart type="family">Pereira</namePart><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Jonathan</namePart><namePart type="family">Widom</namePart><affiliation>Department of Biochemistry Molecular Biology and Cell Biology, Northwestern University, Evanston IL 60208-3500, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">John N</namePart><namePart type="family">Reeve</namePart><affiliation>E-mail: reeve.2@osu.edu</affiliation><affiliation>Department of Microbiology The Ohio State University, Columbus OH 43210-1292, USA</affiliation><description>Corresponding author</description><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="research-article" displayLabel="Full-length article" authority="ISTEX" authorityURI="https://content-type.data.istex.fr" valueURI="https://content-type.data.istex.fr/ark:/67375/XTP-1JC4F85T-7">research-article</genre><originInfo><publisher>ELSEVIER</publisher><dateIssued encoding="w3cdtf">2000</dateIssued><dateModified encoding="w3cdtf">2000-08-17</dateModified><copyrightDate encoding="w3cdtf">2000</copyrightDate></originInfo><language><languageTerm type="code" authority="iso639-2b">eng</languageTerm><languageTerm type="code" authority="rfc3066">en</languageTerm></language><abstract lang="en">Abstract: Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones have almost identical histone folds. Here, we show that DNA molecules selectively incorporated by rHMfB (recombinant archaeal histone B from Methanothermus fervidus) into archaeal nucleosomes from a mixture of ∼1014 random sequence molecules contain sequence motifs shown previously to direct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA are repeated at ∼10 bp intervals, with the GC harmonic displaced ∼5 bp from the AA and TA harmonics [(GCN3AA or TA)n]. AT and CG were not strongly selected, indicating that TA≠AT and GC≠CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from ∼9 to 18-fold higher than the level of affinity of the starting population, and direct the positioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at ∼10.1 bp intervals, the helical repeat of DNA wrapped around a nucleosome, in the genomes of Eucarya and the histone-containing Euryarchaeota, but not in the genomes of Bacteria and Crenarchaeota, procaryotes that do not have histones. Facilitating histone packaging of genomic DNA has apparently therefore imposed constraints on genome sequence evolution, and since archaeal histones have no structure in addition to the histone fold, these constraints must result predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolution most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarchaeota. However, with lateral gene transfer, the first histone fold could alternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages.</abstract><note type="footnote">Edited by T. Richmond</note><note type="content">Section title: Regular article</note><note type="content">Figure 1: Structure of cycle 0 DNA molecules, rHMfB affinities and consensus of cycle 8 sequences. (a) Each cycle 0 molecule had a 60 bp region of random-sequence (N60) flanked by the 25 bp fixed sequences (25L and 25R) shown. (b) Electrophoretic separation of cycle 0 DNA from archaeal nucleosomes (rHMfB-DNA) assembled at increasing rHMfB to DNA ratios. (c) Comparison of the affinities of cycle 0 DNA, cycle 8 clones 5 and 9, M. fervidus 7 S RNA encoding sequence (Pereira & Reeve, 1999) and (CTG)6 repeat sequence (Sandman & Reeve, 1999) for rHMfB. (d) The sequences show by relative font size the frequency with which A, C, G or T occurred at each location in the 89 different 60 bp cycle 8 N60 sequences. The most to least prevalent nucleotide at each location, relative to 25L, are shown in the sequences from top to bottom. The font size equivalent to 80 % occupancy of a site by only one nucleotide is indicated.</note><note type="content">Figure 2: Micrococcal nuclease (MN) digestion and cycle 8 DNA positioning of an archaeal nucleosome. (a) Archaeal nucleosomes, assembled using the cycle 8 molecule with the sequence shown in panel (b), were exposed to MN for 0, 1, 5, 15 and 45 minutes. DNA fragments protected from MN digestion were separated by PAGE and visualized by autoradiography. Control (C) exposure of the DNA to MN for two minutes in the absence of rHMfB resulted in complete digestion. High-resolution electrophoresis through DNA sequencing gels demonstrated that the DNA fragments that accumulated after extended MN digestion were 58 bp. (b) None of the 58 bp MN protected DNA fragments retained the Bam H1 and Eco RI cleavage sites, and Alu I digestion generated only discrete 10(±1) bp and 48(±1) bp restriction fragments. Archaeal nucleosome assembly therefore either occurred at three overlapping sites, displaced by 1 bp as indicated by the ovals, or more likely at one site with the ±1 bp difference reflecting MN nicking of histone-bound DNA near the entry and exit sites of the nucleosome (Hayes & Wolffe, 1993). The vertical arrows identify the sites of fusion of the N60 sequence with 25L and 25R.</note><note type="content">Figure 3: Fourier-transform analysis of dinucleotides in the cycle 8 sequences. As shown, strong signals were present for AA (=TT), TA and GC and a weaker signal for CG at an ∼0.10 bp−1 (∼10 bp) periodicity in the non-redundant database of 111 cycle 8 sequences with subsidiary maxima in the TA and GC transforms reflecting higher harmonics of the ∼0.10 bp−1 signal. The continuous lines with (o) data points are the experimental results, and the lines with error bars are the mean and standard deviation values, respectively, of 100 identical analyses performed on computer-randomized versions of the cycle 8 sequences.</note><note type="content">Figure 4: Real-space correlation analyses of the spatial relationships between dinucleotides in cycle 8 sequences. The spatial relationships between all pairs of dinucleotides in the non-redundant database of cycle 8 sequences were determined for all distances from 1 to 55 bp (Lowary & Widom, 1998). The most-strongly correlated dinucleotide pairs, plotted as a function of the distance (in bp) of the second dinucleotide from the first, are shown. Namely, AA, TA and GC repeated at distances of ∼10, 20 and 30 bp, AA followed by TA at distances of ∼10, 20 and 30 bp, and GC followed by AA or TA at distances of ∼5, 15 and 25 bp. Also shown as lines with error bars are the mean and standard deviations of random expectation (generated from randomized sequences as in Figure 3).</note><note type="content">Figure 5: Power spectra for the AA dinucleotide in archaeal and bacterial genome sequences. The results show data from analyses of the complete euryarchaeal genome sequences of the histone containing (+) Archaeoglobus fulgidus (Af; (Klenk et al. (1997)), Methanococcus jannaschii (Mj, Bult et al. (1996), M. thermoautotrophicum (Mt, Smith et al., 1997), Pyrococcus abyssi (Pa, (http://www.genoscope.cns.fr/Pab)) and Pyrococcus horikoshii (Ph, Kawarabayashi et al., 1998), and of the crenarchaeal and bacterial genomes of Aeropyrum pernix (Ap, Kawarabayashi et al., 1999) and Thermotoga maritima (Tm, Nelson et al., 1999), respectively, that do not (−) contain histones. Analyses of genome sequences from Sulfolobus solfataricus P2 (http://niji.imb.nrc.ca/sulfhome), and additional bacterial genome sequences (Kunst et al., 1997; Cole et al., 1998; Deckert et al., 1998; Stevens et al., 1998) confirmed the presence of a spatial periodicity peak at 0.09 bp−1 (∼11 bp repeat), but absence of the peak at 0.1 bp−1 (∼10.1 bp repeat) that is present in the euryarchaeal genomes. A difference in AA spatial periodicities in bacterial versus archaeal genomes was noted previously (Herzel et al., 1999) but crenarchaeal genome sequences were not then available. Power spectra are shown on a relative scale with a small constant increment added to space the curves for visual clarity.</note><subject><genre>article-category</genre><topic>Regular article</topic></subject><subject lang="en"><genre>Keywords</genre><topic>Archaea</topic><topic>SELEX</topic><topic>nucleosome positioning</topic><topic>genome evolution</topic><topic>HMfB</topic></subject><relatedItem type="host"><titleInfo><title>Journal of Molecular Biology</title></titleInfo><titleInfo type="abbreviated"><title>YJMBI</title></titleInfo><genre type="journal" authority="ISTEX" authorityURI="https://publication-type.data.istex.fr" valueURI="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</genre><originInfo><publisher>ELSEVIER</publisher><dateIssued encoding="w3cdtf">2000</dateIssued></originInfo><identifier type="ISSN">0022-2836</identifier><identifier type="PII">S0022-2836(00)X0206-9</identifier><part><date>2000</date><detail type="volume"><number>303</number><caption>vol.</caption></detail><detail type="issue"><number>1</number><caption>no.</caption></detail><extent unit="issue-pages"><start>1</start><end>113</end></extent><extent unit="pages"><start>25</start><end>34</end></extent></part></relatedItem><identifier type="istex">A579D5A93A4D6039E7699E68A910DC4948907066</identifier><identifier type="ark">ark:/67375/6H6-CG6PZT6G-9</identifier><identifier type="DOI">10.1006/jmbi.2000.4128</identifier><identifier type="PII">S0022-2836(00)94128-7</identifier><accessCondition type="use and reproduction" contentType="copyright">©2000 Academic Press</accessCondition><recordInfo><recordContentSource authority="ISTEX" authorityURI="https://loaded-corpus.data.istex.fr" valueURI="https://loaded-corpus.data.istex.fr/ark:/67375/XBH-HKKZVM7B-M">elsevier</recordContentSource><recordOrigin>Academic Press, ©2000</recordOrigin></recordInfo></mods><json:item><extension>json</extension><original>false</original><mimetype>application/json</mimetype><uri>https://api.istex.fr/ark:/67375/6H6-CG6PZT6G-9/record.json</uri></json:item></metadata><serie></serie></istex></record>Pour manipuler ce document sous Unix (Dilib)
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