Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Nalabothula, Narasimharao ^a   Xi, Liqun ^b   Bhattacharyya, Sucharita ^b   Widom, Jonathan ^b   Wang, Ji Ping ^b   Reeve, John N ^c   Santangelo, Thomas J ^c   Fondufe Mittendorf, Yvonne N ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Archaea; Chromatin evolution; Dinucleotide repeats; Histone deletions; Nucleosome positioning; RDNA expression

Indexed keywords

GENOMIC DNA; HISTONE; OLIGONUCLEOTIDE; RIBOSOME DNA; TRANSCRIPTOME;

ARCHAEAL GENOME; ARTICLE; AT RICH SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DINUCLEOTIDE REPEAT; DNA BINDING; DNA SEQUENCE; GENE EXPRESSION; GENETIC CONSERVATION; IN VITRO STUDY; IN VIVO STUDY; METHANOTHERMOBACTER THERMAUTOTROPHICUS; NONHUMAN; NUCLEOSOME; OPEN READING FRAME; OPERON; THERMOCOCCUS KODAKARENSIS; TRANSCRIPTION INITIATION;

ARCHAEA; BASE SEQUENCE; CONSERVED SEQUENCE; DNA, ARCHAEAL; DNA, INTERGENIC; EVOLUTION, MOLECULAR; GENES, ARCHAEAL; HISTONES; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; NUCLEOTIDE MOTIFS; TRANSCRIPTION, GENETIC;

ARCHAEA; EUKARYOTA; METHANOTHERMOBACTER THERMAUTOTROPHICUS; THERMOCOCCUS KODAKARENSIS;

EID: 84878692366     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-391     Document Type: Article

References (67)

1. 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, 2570626, 18989395.
2. 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, 2267817, 18351804.
3. Jiang C, Pugh BF. Nucleosome positioning and gene regulation: advances through genomics. Nature Rev Genet 2009, 10:161-172.
4. 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, 3209474, 21942931.
5. 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, 2623244, 16862119.
6. 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, 2658732, 19092803.
7. Yuan GC, Liu JS. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput Biol 2008, 4:e13. 10.1371/journal.pcbi.0040013, 2211532, 18225943.
8. Rapoport AE, Frenkel ZM, Trifonov EN. Nucleosome positioning pattern derived from oligonucleotide compositions of genomic sequences. J Biomol Struct Dynam 2011, 28:567-574.
9. 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, 16920388.
10. 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, 1196040, 16030242.
11. 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, 2632074, 19047349.
12. 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, 11021967.
13. 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, 3510624, 23065975.
14. 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, 54413, 2377617.
15. Samson R, Reeve JN. DNA binding proteins and chromatin. Archaea: Molecular and Cellular Biology 2007, 110-119. Washington, DC: ASM Press, Cavicchioli R.
16. 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, 25063, 9356501.
17. 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, 11751933.
18. 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, 12058041.
19. 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. author reply 920-922, 10.1038/nsmb0810-918, 2969171, 20683473.
20. 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, 3499251, 23166509.
21. Brogaard K, Xi L, Wang JP, Widom J. A map of nucleosome positions in yeast at base-pair resolution. Nature 2012, 486:496-501.
22. 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, 17873876.
23. 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, 2673466, 19208466.
24. 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. 398371, 7781610.
25. 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, 111049, 10684934.
26. 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.
27. 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, 16860337.
28. 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, 390927, 3909145.
29. 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, 3670410.
30. 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, 113125, 11058103.
31. 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, 87046, 11340174.
32. 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, 15949447.
33. Ioshikhes IP, Albert I, Zanton SJ, Pugh BF. Nucleosome positions predicted through comparative genomics. Nat Genet 2006, 38:1210-1215. 10.1038/ng1878, 16964265.
34. 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, 551561, 15710748.
35. 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, 21596617.
36. 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, 16305799.
37. 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, 3376729, 22724063.
38. 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, 1933512, 17620451.
39. Archaeal Genome Browser http://archaea.ucsc.edu.
40. 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, 2258858, 18192385.
41. 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. 179657, 9371463.
42. UCSC Genome Browser on Thermococcus kodakarensis May 2004 Assembly (therKoda1) http://archaea.ucsc.edu/lists/therKoda1/refSeq-list.html.
43. 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, 2515632, 18725940.
44. 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, 2823114, 19620965.
45. 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, 3205571, 21750105.
46. Tillo D, Hughes TR. G + C content dominates intrinsic nucleosome occupancy. BMC Bioinforma 2009, 10:442.
47. 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, 2779460, 19734899.
48. 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, 1303568, 14581192.
49. 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, 9305837.
50. 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.
51. 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, 11021968.
52. 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, 10704305.
53. 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, 17237472.
54. 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, 2872413, 20351259.
55. 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, 415759, 15150236.
56. 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, 15961632.
57. 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, 3510453, 23240084.
58. 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, 2841640, 20333302.
59. 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, 2735122, 18408708.
60. 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, 2744203, 19252487.
61. Rapoport AE, Trivonof EF. " Anticipated" nucleosome positioning pattern in prokaryotes. Gene 2011, 488:41-45. 10.1016/j.gene.2011.08.002, 21884764.
62. Reeve JN. Archaeal chromatin and transcription. Mol Microbiol 2003, 48:587-598. 10.1046/j.1365-2958.2003.03439.x, 12694606.
63. 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, 8347588.
64. Applied Biosystems protocol for SOLiD sequencing http://tools.invitrogen.com/content/sfs/manuals/SOLiD4_Library_Preparation_man.pdf.
65. 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.
66. Genome-database of Methanobacterium thermoautotrophicum and Thermococcus kodakarensis sequenced nucleosomal reads 2012 http://ncode.northwestern.edu.
67. UCSC Genome Browser on Methanobacterium thermoautotrophicum Aug 1997 Assembly (methTher1) http://archaea.ucsc.edu/lists/methTher1/refSeq-list.html.