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PMID: 21803858 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

True single-molecule DNA sequencing of a pleistocene horse bone.

Genome research ·Vol. 21 ·No. 10 ·2011-10-00 ·Pages 1705-19

Orlando L, Ginolhac A, Raghavan M, Vilstrup J, Rasmussen M, Magnussen K, Steinmann KE, Kapranov P, Thompson JF, Zazula G, Froese D, Moltke I, Shapiro B, Hofreiter M, Al-Rasheid KA, Gilbert MT, Willerslev E

Abstract

Second-generation sequencing platforms have revolutionized the field of ancient DNA, opening access to complete genomes of past individuals and extinct species. However, these platforms are dependent on library construction and amplification steps that may result in sequences that do not reflect the original DNA template composition. This is particularly true for ancient DNA, where templates have undergone extensive damage post-mortem. Here, we report the results of the first "true single molecule sequencing" of ancient DNA. We generated 115.9 Mb and 76.9 Mb of DNA sequences from a permafrost-preserved Pleistocene horse bone using the Helicos HeliScope and Illumina GAIIx platforms, respectively. We find that the percentage of endogenous DNA sequences derived from the horse is higher among the Helicos data than Illumina data. This result indicates that the molecular biology tools used to generate sequencing libraries of ancient DNA molecules, as required for second-generation sequencing, introduce biases into the data that reduce the efficiency of the sequencing process and limit our ability to fully explore the molecular complexity of ancient DNA extracts. We demonstrate that simple modifications to the standard Helicos DNA template preparation protocol further increase the proportion of horse DNA for this sample by threefold. Comparison of Helicos-specific biases and sequence errors in modern DNA with those in ancient DNA also reveals extensive cytosine deamination damage at the 3' ends of ancient templates, indicating the presence of 3'-sequence overhangs. Our results suggest that paleogenomes could be sequenced in an unprecedented manner by combining current second- and third-generation sequencing approaches.

MeSH Terms
Animals Bone and Bones/chemistry Chromosome Mapping DNA/chemistry,isolation & purification DNA Damage DNA Fragmentation Fossils High-Throughput Nucleotide Sequencing/instrumentation,methods Horses/genetics Sequence Analysis, DNA/instrumentation,methods
Chemicals
DNA
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Orlando Ludovic
Centre for GeoGenetics, Natural History Museum of Denmark, Copenhagen University, Copenhagen DK-1350, Denmark. [email protected]
Ginolhac Aurelien
Raghavan Maanasa
Vilstrup Julia
Rasmussen Morten
Magnussen Kim
Steinmann Kathleen E
Kapranov Philipp
Thompson John F
Zazula Grant
Froese Duane
Moltke Ida
Shapiro Beth
Hofreiter Michael
Al-Rasheid Khaled A S
Gilbert M Thomas P
Willerslev Eske
References (80)
80 references, click to expand
  1. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae.
    Nature. 2006 Feb 9;439(7077):724-7 PMID: 16362058
  2. Sequencing the nuclear genome of the extinct woolly mammoth.
    Nature. 2008 Nov 20;456(7220):387-90 PMID: 19020620
  3. Rise and fall of the Beringian steppe bison.
    Science. 2004 Nov 26;306(5701):1561-5 PMID: 15567864
  4. Quantification of the yeast transcriptome by single-molecule sequencing.
    Nat Biotechnol. 2009 Jul;27(7):652-8 PMID: 19581875
  5. Genome-wide mapping of in vivo protein-DNA interactions.
    Science. 2007 Jun 8;316(5830):1497-502 PMID: 17540862
  6. Targeted retrieval and analysis of five Neandertal mtDNA genomes.
    Science. 2009 Jul 17;325(5938):318-21 PMID: 19608918
  7. Whole-genome sequencing and variant discovery in C. elegans.
    Nat Methods. 2008 Feb;5(2):183-8 PMID: 18204455
  8. Inconsistencies in Neanderthal genomic DNA sequences.
    PLoS Genet. 2007 Oct;3(10):1862-6 PMID: 17937503
  9. Virtual terminator nucleotides for next-generation DNA sequencing.
    Nat Methods. 2009 Aug;6(8):593-5 PMID: 19620973
  10. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts.
    Science. 2007 Sep 28;317(5846):1927-30 PMID: 17901335
  11. Single-molecule sequencing: sequence methods to enable accurate quantitation.
    Methods Enzymol. 2010;472:407-30 PMID: 20580974
  12. Fast and accurate short read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2009 Jul 15;25(14):1754-60 PMID: 19451168
  13. Genetic discontinuity between local hunter-gatherers and central Europe's first farmers.
    Science. 2009 Oct 2;326(5949):137-40 PMID: 19729620
  14. Analysis of complete mitochondrial genomes from extinct and extant rhinoceroses reveals lack of phylogenetic resolution.
    BMC Evol Biol. 2009 May 11;9:95 PMID: 19432984
  15. Genetic analyses from ancient DNA.
    Annu Rev Genet. 2004;38:645-79 PMID: 15568989
  16. Ancient human genome sequence of an extinct Palaeo-Eskimo.
    Nature. 2010 Feb 11;463(7282):757-62 PMID: 20148029
  17. Freshly excavated fossil bones are best for amplification of ancient DNA.
    Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):739-44 PMID: 17210911
  18. Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland.
    Science. 2008 Jun 27;320(5884):1787-9 PMID: 18511654
  19. A large genome center's improvements to the Illumina sequencing system.
    Nat Methods. 2008 Dec;5(12):1005-10 PMID: 19034268
  20. Recharacterization of ancient DNA miscoding lesions: insights in the era of sequencing-by-synthesis.
    Nucleic Acids Res. 2007;35(1):1-10 PMID: 16920744
  21. Sequencing technologies - the next generation.
    Nat Rev Genet. 2010 Jan;11(1):31-46 PMID: 19997069
  22. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA.
    Nucleic Acids Res. 2001 Dec 1;29(23):4793-9 PMID: 11726688
  23. Assessing ancient DNA studies.
    Trends Ecol Evol. 2005 Oct;20(10):541-4 PMID: 16701432
  24. Genomic sequencing of Pleistocene cave bears.
    Science. 2005 Jul 22;309(5734):597-9 PMID: 15933159
  25. Ancient bone DNA amplified.
    Nature. 1989 Nov 30;342(6249):485 PMID: 2586623
  26. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing.
    Cell. 2008 Aug 8;134(3):416-26 PMID: 18692465
  27. Ancient DNA reveals late survival of mammoth and horse in interior Alaska.
    Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22352-7 PMID: 20018740
  28. Illumina sequencing library preparation for highly multiplexed target capture and sequencing.
    Cold Spring Harb Protoc. 2010 Jun;2010(6):pdb.prot5448 PMID: 20516186
  29. Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics.
    Proc Natl Acad Sci U S A. 2010 Mar 23;107(12):5675-80 PMID: 20212118
  30. Withering away--25,000 years of genetic decline preceded cave bear extinction.
    Mol Biol Evol. 2010 May;27(5):975-8 PMID: 20335279
  31. Characterization of genetic miscoding lesions caused by postmortem damage.
    Am J Hum Genet. 2003 Jan;72(1):48-61 PMID: 12489042
  32. Bayesian estimation of sequence damage in ancient DNA.
    Mol Biol Evol. 2007 Jun;24(6):1416-22 PMID: 17395598
  33. Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants.
    PLoS Biol. 2010 Dec 21;8(12):e1000564 PMID: 21203580
  34. Statistical evidence for miscoding lesions in ancient DNA templates.
    Mol Biol Evol. 2001 Feb;18(2):262-5 PMID: 11158385
  35. Next-generation DNA sequencing.
    Nat Biotechnol. 2008 Oct;26(10):1135-45 PMID: 18846087
  36. Damage and repair of ancient DNA.
    Mutat Res. 2005 Apr 1;571(1-2):265-76 PMID: 15748652
  37. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products.
    PLoS One. 2010 Nov 16;5(11):e14004 PMID: 21103372
  38. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup.
    PLoS Biol. 2007 Aug;5(8):e207 PMID: 17676977
  39. Diverse plant and animal genetic records from Holocene and Pleistocene sediments.
    Science. 2003 May 2;300(5620):791-5 PMID: 12702808
  40. New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains.
    Nucleic Acids Res. 2009 Jun;37(10):3215-29 PMID: 19321502
  41. Single molecule sequencing with a HeliScope genetic analysis system.
    Curr Protoc Mol Biol. 2010 Oct;Chapter 7:Unit7.10 PMID: 20890904
  42. Nuclear gene indicates coat-color polymorphism in mammoths.
    Science. 2006 Jul 7;313(5783):62 PMID: 16825562
  43. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia.
    Science. 1985 Dec 20;230(4732):1350-4 PMID: 2999980
  44. Assessing the fidelity of ancient DNA sequences amplified from nuclear genes.
    Genetics. 2006 Feb;172(2):733-41 PMID: 16299392
  45. Genetic history of an archaic hominin group from Denisova Cave in Siberia.
    Nature. 2010 Dec 23;468(7327):1053-60 PMID: 21179161
  46. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA.
    Science. 2006 Jan 20;311(5759):392-4 PMID: 16368896
  47. Sequencing and analysis of Neanderthal genomic DNA.
    Science. 2006 Nov 17;314(5802):1113-8 PMID: 17110569
  48. Nuclear gene sequences from a late pleistocene sloth coprolite.
    Curr Biol. 2003 Jul 1;13(13):1150-2 PMID: 12842016
  49. Ancient DNA extraction from bones and teeth.
    Nat Protoc. 2007;2(7):1756-62 PMID: 17641642
  50. A complete mtDNA genome of an early modern human from Kostenki, Russia.
    Curr Biol. 2010 Feb 9;20(3):231-6 PMID: 20045327
  51. Long-term persistence of bacterial DNA.
    Curr Biol. 2004 Jan 6;14(1):R9-10 PMID: 14711425
  52. An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6.
    BMC Genomics. 2010 Sep 28;11:522 PMID: 20920191
  53. Targeted investigation of the Neandertal genome by array-based sequence capture.
    Science. 2010 May 7;328(5979):723-5 PMID: 20448179
  54. Single-molecule DNA sequencing of a viral genome.
    Science. 2008 Apr 4;320(5872):106-9 PMID: 18388294
  55. mapDamage: testing for damage patterns in ancient DNA sequences.
    Bioinformatics. 2011 Aug 1;27(15):2153-5 PMID: 21659319
  56. Molecular analysis of an 11,700-year-old rodent midden from the Atacama Desert, Chile.
    Mol Ecol. 2002 May;11(5):913-24 PMID: 11975707
  57. A draft sequence of the Neandertal genome.
    Science. 2010 May 7;328(5979):710-722 PMID: 20448178
  58. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification.
    Proc Natl Acad Sci U S A. 1989 Mar;86(6):1939-43 PMID: 2928314
  59. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia.
    Nature. 2010 Apr 8;464(7290):894-7 PMID: 20336068
  60. Ancient DNA reveals lack of continuity between neolithic hunter-gatherers and contemporary Scandinavians.
    Curr Biol. 2009 Nov 3;19(20):1758-62 PMID: 19781941
  61. MEGAN analysis of metagenomic data.
    Genome Res. 2007 Mar;17(3):377-86 PMID: 17255551
  62. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions.
    Nucleic Acids Res. 2007;35(17):5717-28 PMID: 17715147
  63. Ancient DNA.
    Proc Biol Sci. 2005 Jan 7;272(1558):3-16 PMID: 15875564
  64. Ancient DNA from European early neolithic farmers reveals their near eastern affinities.
    PLoS Biol. 2010 Nov 09;8(11):e1000536 PMID: 21085689
  65. Error tolerant indexing and alignment of short reads with covering template families.
    J Comput Biol. 2010 Oct;17(10):1397-1411 PMID: 20937014
  66. Patterns of nucleotide misincorporations during enzymatic amplification and direct large-scale sequencing of ancient DNA.
    Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13578-84 PMID: 16938852
  67. Rapid response of a marine mammal species to holocene climate and habitat change.
    PLoS Genet. 2009 Jul;5(7):e1000554 PMID: 19593366
  68. Fossil avian eggshell preserves ancient DNA.
    Proc Biol Sci. 2010 Jul 7;277(1690):1991-2000 PMID: 20219731
  69. DNA damage and DNA sequence retrieval from ancient tissues.
    Nucleic Acids Res. 1996 Apr 1;24(7):1304-7 PMID: 8614634
  70. Single-molecule sequencing of an individual human genome.
    Nat Biotechnol. 2009 Sep;27(9):847-50 PMID: 19668243
  71. Patterns of damage in genomic DNA sequences from a Neandertal.
    Proc Natl Acad Sci U S A. 2007 Sep 11;104(37):14616-21 PMID: 17715061
  72. Ancient biomolecules from deep ice cores reveal a forested southern Greenland.
    Science. 2007 Jul 6;317(5834):111-4 PMID: 17615355
  73. Relatively well preserved DNA is present in the crystal aggregates of fossil bones.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13783-8 PMID: 16162675
  74. Ancient DNA and the polymerase chain reaction. The emerging field of molecular archaeology.
    J Biol Chem. 1989 Jun 15;264(17):9709-12 PMID: 2656708
  75. Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean caprine.
    PLoS One. 2009 May 22;4(5):e5670 PMID: 19461892
  76. DNA sequences from the quagga, an extinct member of the horse family.
    Nature. 1984 Nov 15-21;312(5991):282-4 PMID: 6504142
  77. Real-time DNA sequencing from single polymerase molecules.
    Science. 2009 Jan 2;323(5910):133-8 PMID: 19023044
  78. Analysis of one million base pairs of Neanderthal DNA.
    Nature. 2006 Nov 16;444(7117):330-6 PMID: 17108958
  79. Instability and decay of the primary structure of DNA.
    Nature. 1993 Apr 22;362(6422):709-15 PMID: 8469282
  80. Ancient DNA: do it right or not at all.
    Science. 2000 Aug 18;289(5482):1139 PMID: 10970224
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1549-5469
Published
2011-10-00
Epub
2011-00-29
Pages
1705-19
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC3202287
Subset
IM
Grants
NHGRI NIH HHS · R44 HG005279 · United States
NHGRI NIH HHS · R44 HG005279-02 · United States
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