Selection for ancient periodic motifs that do not impart DNA bending
Autoři:
Aletheia Atzinger aff001; Jeffrey G. Lawrence aff001
Působiště autorů:
University of Pittsburgh, Department of Biological Sciences, Pittsburgh, United States of America
aff001
Vyšlo v časopise:
Selection for ancient periodic motifs that do not impart DNA bending. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009042
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009042
Souhrn
A ~10–11 bp periodicity in dinucleotides imparting DNA bending, with shorter periods found in organisms with positively-supercoiled DNA and longer periods found in organisms with negatively-supercoiled DNA, was previously suggested to assist in DNA compaction. However, when measured with more robust methods, variation in the observed periods between organisms with different growth temperatures is not consistent with that hypothesis. We demonstrate that dinucleotide periodicity does not arise solely by mutational biases but is under selection. We found variation between genomes in both the period and the suite of dinucleotides that are periodic. Whereas organisms with similar growth temperatures have highly variable periods, differences in periods increase with phylogenetic distance between organisms. In addition, while the suites of dinucleotides under selection for periodicity become more dissimilar among more distantly-related organisms, there is a core set of dinucleotides that are strongly periodic among genomes in all domains of life. Notably, this core set of periodic motifs are not involved in DNA bending. These data indicate that dinucleotide periodicity is an ancient genomic architecture which may play a role in shaping the evolution of genes and genomes.
Klíčová slova:
Archaea – Bacterial genomics – Curve fitting – Distribution curves – Genome analysis – Genomics – Paleogenetics – Autocorrelation
Zdroje
1. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000;405(6784):299–304. Epub 2000/06/01. doi: 10.1038/35012500 10830951.
2. Polz MF, Alm EJ, Hanage WP. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 2013;29(3):170–5. Epub 2013/01/22. doi: 10.1016/j.tig.2012.12.006 23332119; PubMed Central PMCID: PMC3760709.
3. Beiko RG, Harlow TJ, Ragan MA. Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A. 2005;102(40):14332–7. Epub 2005/09/24. doi: 10.1073/pnas.0504068102 16176988; PubMed Central PMCID: PMC1242295.
4. Lawrence JG, Ochman H. Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A. 1998;95(16):9413–7. Epub 1998/08/05. doi: 10.1073/pnas.95.16.9413 9689094; PubMed Central PMCID: PMC21352.
5. Obar R, Green J. Molecular archaeology of the mitochondrial genome. J Mol Evol. 1985;22(3):243–51. Epub 1985/01/01. doi: 10.1007/BF02099754 3935805.
6. Baltrus DA. Exploring the costs of horizontal gene transfer. Trends Ecol Evol. 2013;28(8):489–95. Epub 2013/05/28. doi: 10.1016/j.tree.2013.04.002 23706556.
7. Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol. 2005;3(9):711–21. Epub 2005/09/03. doi: 10.1038/nrmicro1234 16138099.
8. Hendrickson H, Lawrence JG. Selection for chromosome architecture in bacteria. J Mol Evol. 2006;62(5):615–29. Epub 2006/04/14. doi: 10.1007/s00239-005-0192-2 16612541.
9. Hendrickson HL, Barbeau D, Ceschin R, Lawrence JG. Chromosome architecture constrains horizontal gene transfer in bacteria. PLoS Genet. 2018;14(5):e1007421. Epub 2018/05/31. doi: 10.1371/journal.pgen.1007421 29813058; PubMed Central PMCID: PMC5993296.
10. Griffith JD. Visualization of prokaryotic DNA in a regularly condensed chromatin-like fiber. Proc Natl Acad Sci U S A. 1976;73(2):563–7. Epub 1976/02/01. doi: 10.1073/pnas.73.2.563 1108025; PubMed Central PMCID: PMC335950.
11. Cairns J. The bacterial chromosome and its manner of replication as seen by autoradiography. J Mol Biol. 1963;6:208–13. Epub 1963/03/01. doi: 10.1016/s0022-2836(63)80070-4 14017761.
12. Bohrer CH, Roberts E. A biophysical model of supercoiling dependent transcription predicts a structural aspect to gene regulation. BMC Biophys. 2015;9:2. Epub 2016/02/09. doi: 10.1186/s13628-016-0027-0 26855771; PubMed Central PMCID: PMC4744432.
13. Bigot S, Saleh OA, Cornet F, Allemand JF, Barre FX. Oriented loading of FtsK on KOPS. Nat Struct Mol Biol. 2006;13(11):1026–8. Epub 2006/10/17. doi: 10.1038/nsmb1159 17041597.
14. Tomita M, Wada M, Kawashima Y. ApA dinucleotide periodicity in prokaryote, eukaryote, and organelle genomes. J Mol Evol. 1999;49(2):182–92. Epub 1999/08/12. doi: 10.1007/pl00006541 10441670.
15. Calladine CR, Drew HR, McCall MJ. The intrinsic curvature of DNA in solution. J Mol Biol. 1988;201(1):127–37. Epub 1988/05/05. doi: 10.1016/0022-2836(88)90444-5 3418695.
16. Hayes JJ, Clark DJ, Wolffe AP. Histone contributions to the structure of DNA in the nucleosome. Proc Natl Acad Sci U S A. 1991;88(15):6829–33. Epub 1991/08/01. doi: 10.1073/pnas.88.15.6829 1650485; PubMed Central PMCID: PMC52182.
17. Wang JC. Helical repeat of DNA in solution. Proc Natl Acad Sci U S A. 1979;76(1):200–3. Epub 1979/01/01. doi: 10.1073/pnas.76.1.200 284332; PubMed Central PMCID: PMC382905.
18. Shrader TE, Crothers DM. Effects of DNA sequence and histone-histone interactions on nucleosome placement. J Mol Biol. 1990;216(1):69–84. Epub 1990/11/05. doi: 10.1016/S0022-2836(05)80061-0 2172553.
19. Herzel H, Weiss O, Trifonov EN. 10–11 bp periodicities in complete genomes reflect protein structure and DNA folding. Bioinformatics. 1999;15(3):187–93. Epub 1999/05/01. doi: 10.1093/bioinformatics/15.3.187 10222405.
20. Pruss GJ, Drlica K. DNA supercoiling and prokaryotic transcription. Cell. 1989;56(4):521–3. Epub 1989/02/24. doi: 10.1016/0092-8674(89)90574-6 2645054.
21. Kikuchi A, Asai K. Reverse gyrase—a topoisomerase which introduces positive superhelical turns into DNA. Nature. 1984;309(5970):677–81. Epub 1984/06/21. doi: 10.1038/309677a0 6328327.
22. Mrázek J. Comparative analysis of sequence periodicity among prokaryotic genomes points to differences in nucleoid structure and a relationship to gene expression. J Bacteriol. 2010;192(14):3763–72. Epub 2010/05/25. doi: 10.1128/JB.00149-10 20494989; PubMed Central PMCID: PMC2897355.
23. Harris FJ. On the use of windows for harmonic analysis with the discrete Fourier transform. P IEEE. 1978;66:51–83. doi: 10.1109/proc.1978.10837
24. Goldstein E, Drlica K. Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A. 1984;81(13):4046–50. Epub 1984/07/01. doi: 10.1073/pnas.81.13.4046 6377307; PubMed Central PMCID: PMC345365.
25. Novembre JA. Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol. 2002;19(8):1390–4. Epub 2002/07/26. doi: 10.1093/oxfordjournals.molbev.a004201 12140252.
26. Retchless AC, Lawrence JG. Quantification of codon selection for comparative bacterial genomics. BMC Genomics. 2011;12:374. Epub 2011/07/27. doi: 10.1186/1471-2164-12-374 21787402; PubMed Central PMCID: PMC3162537.
27. Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res. 2005;33(4):1141–53. Epub 2005/02/25. doi: 10.1093/nar/gki242 15728743; PubMed Central PMCID: PMC549432.
28. Schieg P, Herzel H. Periodicities of 10-11bp as indicators of the supercoiled state of genomic DNA. J Mol Biol. 2004;343(4):891–901. Epub 2004/10/13. doi: 10.1016/j.jmb.2004.08.068 15476808.
29. Tolstorukov MY, Virnik KM, Adhya S, Zhurkin VB. A-tract clusters may facilitate DNA packaging in bacterial nucleoid. Nucleic Acids Res. 2005;33(12):3907–18. Epub 2005/07/19. doi: 10.1093/nar/gki699 16024741; PubMed Central PMCID: PMC1176013.
30. Swinger KK, Rice PA. Structure-based analysis of HU-DNA binding. J Mol Biol. 2007;365(4):1005–16. Epub 2006/11/14. doi: 10.1016/j.jmb.2006.10.024 17097674; PubMed Central PMCID: PMC1945228.
31. Riccardi E, van Mastbergen EC, Navarre WW, Vreede J. Predicting the mechanism and rate of H-NS binding to AT-rich DNA. PLoS Comput Biol. 2019;15(3):e1006845. Epub 2019/03/08. doi: 10.1371/journal.pcbi.1006845 30845209; PubMed Central PMCID: PMC6424460.
32. Sharma R, Pielstick BA, Bell KA, Nieman TB, Stubbs OA, Yeates EL, et al. A novel, highly related jumbo family of bacteriophages that were isolated against Erwinia. Front Microbiol. 2019;10:1533. Epub 2019/08/21. doi: 10.3389/fmicb.2019.01533 31428059; PubMed Central PMCID: PMC6690015.
33. Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol Biol Evol. 2002;19(12):2226–38. Epub 2002/11/26. doi: 10.1093/oxfordjournals.molbev.a004046 12446813.
34. Abel J, Mrázek J. Differences in DNA curvature-related sequence periodicity between prokaryotic chromosomes and phages, and relationship to chromosomal prophage content. BMC Genomics. 2012;13:188. Epub 2012/05/17. doi: 10.1186/1471-2164-13-188 22587570; PubMed Central PMCID: PMC3431218.
35. Herzel H, Weiss O, Trifonov EN. Sequence periodicity in complete genomes of archaea suggests positive supercoiling. J Biomol Struct Dyn. 1998;16(2):341–5. Epub 1998/12/02. doi: 10.1080/07391102.1998.10508251 9833672.
36. Lehmann R, Machne R, Herzel H. The structural code of cyanobacterial genomes. Nucleic Acids Res. 2014;42(14):8873–83. Epub 2014/07/25. doi: 10.1093/nar/gku641 25056315; PubMed Central PMCID: PMC4132750.
37. Trifonov EN, Sussman JL. The pitch of chromatin DNA is reflected in its nucleotide sequence. Proc Natl Acad Sci U S A. 1980;77(7):3816–20. Epub 1980/07/01. doi: 10.1073/pnas.77.7.3816 6933438; PubMed Central PMCID: PMC349717.
38. Bachmann BJ, Low KB. Linkage map of Escherichia coli K-12, edition 6. Microbiol Rev. 1980;44(1):1–56. Epub 1980/03/01. 6997720; PubMed Central PMCID: PMC373233.
39. Buhk HJ, Messer W. The replication origin region of Escherichia coli: nucleotide sequence and functional units. Gene. 1983;24(2–3):265–79. Epub 1983/10/01. doi: 10.1016/0378-1119(83)90087-2 6357950.
40. Carnoy C, Roten CA. The dif/Xer recombination systems in proteobacteria. PLoS One. 2009;4(9):e6531. Epub 2009/09/04. doi: 10.1371/journal.pone.0006531 19727445; PubMed Central PMCID: PMC2731167.
41. Kono N, Arakawa K, Tomita M. Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics. 2011;12:19. Epub 2011/01/13. doi: 10.1186/1471-2164-12-19 21223577; PubMed Central PMCID: PMC3025954.
42. Efron B. Bootstrap methods: another look at the jackknife. Annals Stat. 1979;7:1–26. doi: 10.1214/aos/1176344552
43. Li WH. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol. 1993;36(1):96–9. Epub 1993/01/01. doi: 10.1007/BF02407308 8433381.
44. Atzinger A, Lawrence JG. 2020. Data from: Selection for Ancient Periodic Motifs That Do Not Impart DNA Bending. Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.0p2ngf1zf
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 10
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Raději si zajděte na oční! Jak souvisí citlivost zraku s rozvojem demence?
- Co způsobuje pooperační infekce? Na vině může být i naše vlastní mikrobiota
- Čeká nás průlom v diagnostice karcinomu pankreatu?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
Nejčtenější v tomto čísle
- Evaluation of both exonic and intronic variants for effects on RNA splicing allows for accurate assessment of the effectiveness of precision therapies
- RNA-directed DNA Methylation
- The DNA methylome of human sperm is distinct from blood with little evidence for tissue-consistent obesity associations
- Correction: Molecular predictors of brain metastasis-related microRNAs in lung adenocarcinoma