True single-molecule DNA sequencing of a pleistocene horse bone.
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.
Publication Date: 2011-07-29 PubMed ID: 21803858PubMed Central: PMC3202287DOI: 10.1101/gr.122747.111Google Scholar: Lookup
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- Journal Article
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Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article presents the use of “true single molecule sequencing” for ancient DNA from a Pleistocene horse bone, showing it can provide a higher percentage of endogenous DNA sequences and offers an efficient way of studying ancient DNA extracts. The article also suggests that a combination of current second- and third-generation sequencing methods could enhance the sequencing of paleogenomes.
Introduction
- The research focuses on using second-generation sequencing platforms for studying ancient DNA.
- These platforms have been transformative in the study of past genomes, even from extinct species.
- However, the process relies heavily on constructing libraries and amplification steps, which might alter the original DNA template composition.
- This is especially an issue with ancient DNA, which has been subjected to significant damage over time.
Single Molecule Sequencing and its Application
- The researchers employed “true single molecule sequencing” to assess ancient DNA.
- DNA sequences from a Pleistocene horse bone, preserved in permafrost, were generated using the Helicos HeliScope and Illumina GAIIx platforms.
- The sequences derived from the horse (endogenous DNA sequences) were found more frequently in Helicos data than in Illumina data, showing a distinct advantage of using the “true single molecule sequencing”.
Limitations of Existing Tools and Improvement Suggestion
- Tools used for generating sequencing libraries often introduce biases, reducing the efficiency of the process and limiting the full exploration of the ancient DNA extracts’ molecular complexity.
- The researchers found that making simple modifications to the standard Helicos DNA template preparation protocol could increase the horse DNA proportion in their sample by three times.
Analyzing Biases and Sequence Errors
- The study compared Helicos-specific biases and sequence errors between modern and ancient DNA.
- It revealed extensive cytosine deamination damage at the ancient DNA templates’ 3′ ends, indicating the presence of 3′-sequence overhangs.
Future Recommendations
- The study concluded by suggesting a potential approach for sequencing paleogenomes using a combination of current second- and third-generation sequencing techniques.
- This method could revolutionize the sequencing process of paleogenomes.
Cite This Article
APA
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.
(2011).
True single-molecule DNA sequencing of a pleistocene horse bone.
Genome Res, 21(10), 1705-1719.
https://doi.org/10.1101/gr.122747.111 Publication
Researcher Affiliations
- Centre for GeoGenetics, Natural History Museum of Denmark, Copenhagen University, Copenhagen DK-1350, Denmark. Lorlando@snm.ku.dk
MeSH Terms
- Animals
- Bone and Bones / chemistry
- Chromosome Mapping
- DNA / chemistry
- DNA / isolation & purification
- DNA Damage
- DNA Fragmentation
- Fossils
- High-Throughput Nucleotide Sequencing / instrumentation
- High-Throughput Nucleotide Sequencing / methods
- Horses / genetics
- Sequence Analysis, DNA / instrumentation
- Sequence Analysis, DNA / methods
Grant Funding
- R44 HG005279 / NHGRI NIH HHS
- R44 HG005279-02 / NHGRI NIH HHS
References
This article includes 81 references
- Binladen J, Wiuf C, Gilbert MT, Bunce M, Barnett R, Larson G, Greenwood AD, Haile J, Ho SY, Hansen AJ, Willerslev E. Assessing the fidelity of ancient DNA sequences amplified from nuclear genes.. Genetics 2006 Feb;172(2):733-41.
- Bowers J, Mitchell J, Beer E, Buzby PR, Causey M, Efcavitch JW, Jarosz M, Krzymanska-Olejnik E, Kung L, Lipson D, Lowman GM, Marappan S, McInerney P, Platt A, Roy A, Siddiqi SM, Steinmann K, Thompson JF. Virtual terminator nucleotides for next-generation DNA sequencing.. Nat Methods 2009 Aug;6(8):593-5.
- Bramanti B, Thomas MG, Haak W, Unterlaender M, Jores P, Tambets K, Antanaitis-Jacobs I, Haidle MN, Jankauskas R, Kind CJ, Lueth F, Terberger T, Hiller J, Matsumura S, Forster P, Burger J. Genetic discontinuity between local hunter-gatherers and central Europe's first farmers.. Science 2009 Oct 2;326(5949):137-40.
- Briggs AW, Stenzel U, Johnson PL, Green RE, Kelso J, Prüfer K, Meyer M, Krause J, Ronan MT, Lachmann M, Pääbo S. Patterns of damage in genomic DNA sequences from a Neandertal.. Proc Natl Acad Sci U S A 2007 Sep 11;104(37):14616-21.
- Briggs AW, Good JM, Green RE, Krause J, Maricic T, Stenzel U, Lalueza-Fox C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Schmitz R, Doronichev VB, Golovanova LV, de la Rasilla M, Fortea J, Rosas A, Pääbo S. Targeted retrieval and analysis of five Neandertal mtDNA genomes.. Science 2009 Jul 17;325(5938):318-21.
- Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R, Austin J, Cooper A. 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.
- Burbano HA, Hodges E, Green RE, Briggs AW, Krause J, Meyer M, Good JM, Maricic T, Johnson PL, Xuan Z, Rooks M, Bhattacharjee A, Brizuela L, Albert FW, de la Rasilla M, Fortea J, Rosas A, Lachmann M, Hannon GJ, Pääbo S. Targeted investigation of the Neandertal genome by array-based sequence capture.. Science 2010 May 7;328(5979):723-5.
- Campos PF, Willerslev E, Sher A, Orlando L, Axelsson E, Tikhonov A, Aaris-Sørensen K, Greenwood AD, Kahlke RD, Kosintsev P, Krakhmalnaya T, Kuznetsova T, Lemey P, MacPhee R, Norris CA, Shepherd K, Suchard MA, Zazula GD, Shapiro B, Gilbert MT. 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.
- Cooper A, Poinar HN. Ancient DNA: do it right or not at all.. Science 2000 Aug 18;289(5482):1139.
- de Bruyn M, Hall BL, Chauke LF, Baroni C, Koch PL, Hoelzel AR. Rapid response of a marine mammal species to holocene climate and habitat change.. PLoS Genet 2009 Jul;5(7):e1000554.
- Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, Dewinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S. Real-time DNA sequencing from single polymerase molecules.. Science 2009 Jan 2;323(5910):133-8.
- Giladi E, Healy J, Myers G, Hart C, Kapranov P, Lipson D, Roels S, Thayer E, Letovsky S. Error tolerant indexing and alignment of short reads with covering template families.. J Comput Biol 2010 Oct;17(10):1397-1411.
- Gilbert MT, Hansen AJ, Willerslev E, Rí¯¬k L, Barnes I, Lynnerup N, Cooper A. Characterization of genetic miscoding lesions caused by postmortem damage.. Am J Hum Genet 2003 Jan;72(1):48-61.
- Gilbert MT, Bandelt HJ, Hofreiter M, Barnes I. Assessing ancient DNA studies.. Trends Ecol Evol 2005 Oct;20(10):541-4.
- Gilbert MT, Binladen J, Miller W, Wiuf C, Willerslev E, Poinar H, Carlson JE, Leebens-Mack JH, Schuster SC. Recharacterization of ancient DNA miscoding lesions: insights in the era of sequencing-by-synthesis.. Nucleic Acids Res 2007;35(1):1-10.
- Gilbert MT, Tomsho LP, Rendulic S, Packard M, Drautz DI, Sher A, Tikhonov A, Dalén L, Kuznetsova T, Kosintsev P, Campos PF, Higham T, Collins MJ, Wilson AS, Shidlovskiy F, Buigues B, Ericson PG, Germonpré M, Götherström A, Iacumin P, Nikolaev V, Nowak-Kemp M, Willerslev E, Knight JR, Irzyk GP, Perbost CS, Fredrikson KM, Harkins TT, Sheridan S, Miller W, Schuster SC. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts.. Science 2007 Sep 28;317(5846):1927-30.
- Gilbert MT, Kivisild T, Grønnow B, Andersen PK, Metspalu E, Reidla M, Tamm E, Axelsson E, Götherström A, Campos PF, Rasmussen M, Metspalu M, Higham TF, Schwenninger JL, Nathan R, De Hoog CJ, Koch A, Møller LN, Andreasen C, Meldgaard M, Villems R, Bendixen C, Willerslev E. Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland.. Science 2008 Jun 27;320(5884):1787-9.
- Ginolhac A, Rasmussen M, Gilbert MT, Willerslev E, Orlando L. mapDamage: testing for damage patterns in ancient DNA sequences.. Bioinformatics 2011 Aug 1;27(15):2153-5.
- Green RE, Krause J, Ptak SE, Briggs AW, Ronan MT, Simons JF, Du L, Egholm M, Rothberg JM, Paunovic M, Pääbo S. Analysis of one million base pairs of Neanderthal DNA.. Nature 2006 Nov 16;444(7117):330-6.
- Green RE, Malaspinas AS, Krause J, Briggs AW, Johnson PL, Uhler C, Meyer M, Good JM, Maricic T, Stenzel U, Prüfer K, Siebauer M, Burbano HA, Ronan M, Rothberg JM, Egholm M, Rudan P, Brajković D, Kućan Z, Gusić I, Wikström M, Laakkonen L, Kelso J, Slatkin M, Pääbo S. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing.. Cell 2008 Aug 8;134(3):416-26.
- Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Ž, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S. A draft sequence of the Neandertal genome.. Science 2010 May 7;328(5979):710-722.
- Haak W, Balanovsky O, Sanchez JJ, Koshel S, Zaporozhchenko V, Adler CJ, Der Sarkissian CS, Brandt G, Schwarz C, Nicklisch N, Dresely V, Fritsch B, Balanovska E, Villems R, Meller H, Alt KW, Cooper A. Ancient DNA from European early neolithic farmers reveals their near eastern affinities.. PLoS Biol 2010 Nov 9;8(11):e1000536.
- Hagelberg E, Sykes B, Hedges R. Ancient bone DNA amplified.. Nature 1989 Nov 30;342(6249):485.
- Haile J, Froese DG, Macphee RD, Roberts RG, Arnold LJ, Reyes AV, Rasmussen M, Nielsen R, Brook BW, Robinson S, Demuro M, Gilbert MT, Munch K, Austin JJ, Cooper A, Barnes I, Möller P, Willerslev E. 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.
- Hansen A, Willerslev E, Wiuf C, Mourier T, Arctander P. Statistical evidence for miscoding lesions in ancient DNA templates.. Mol Biol Evol 2001 Feb;18(2):262-5.
- Harris TD, Buzby PR, Babcock H, Beer E, Bowers J, Braslavsky I, Causey M, Colonell J, Dimeo J, Efcavitch JW, Giladi E, Gill J, Healy J, Jarosz M, Lapen D, Moulton K, Quake SR, Steinmann K, Thayer E, Tyurina A, Ward R, Weiss H, Xie Z. Single-molecule DNA sequencing of a viral genome.. Science 2008 Apr 4;320(5872):106-9.
- Hart C, Lipson D, Ozsolak F, Raz T, Steinmann K, Thompson J, Milos PM. Single-molecule sequencing: sequence methods to enable accurate quantitation.. Methods Enzymol 2010;472:407-30.
- Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC. DNA sequences from the quagga, an extinct member of the horse family.. Nature 1984 Nov 15-21;312(5991):282-4.
- Hillier LW, Marth GT, Quinlan AR, Dooling D, Fewell G, Barnett D, Fox P, Glasscock JI, Hickenbotham M, Huang W, Magrini VJ, Richt RJ, Sander SN, Stewart DA, Stromberg M, Tsung EF, Wylie T, Schedl T, Wilson RK, Mardis ER. Whole-genome sequencing and variant discovery in C. elegans.. Nat Methods 2008 Feb;5(2):183-8.
- Ho SY, Heupink TH, Rambaut A, Shapiro B. Bayesian estimation of sequence damage in ancient DNA.. Mol Biol Evol 2007 Jun;24(6):1416-22.
- Hofreiter M, Jaenicke V, Serre D, von Haeseler A, Pääbo S. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA.. Nucleic Acids Res 2001 Dec 1;29(23):4793-9.
- Höss M, Jaruga P, Zastawny TH, Dizdaroglu M, Pääbo S. DNA damage and DNA sequence retrieval from ancient tissues.. Nucleic Acids Res 1996 Apr 1;24(7):1304-7.
- Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data.. Genome Res 2007 Mar;17(3):377-86.
- Johnson DS, Mortazavi A, Myers RM, Wold B. Genome-wide mapping of in vivo protein-DNA interactions.. Science 2007 Jun 8;316(5830):1497-502.
- Kimbrel JA, Givan SA, Halgren AB, Creason AL, Mills DI, Banowetz GM, Armstrong DJ, Chang JH. An improved, high-quality draft genome sequence of the Germination-Arrest Factor-producing Pseudomonas fluorescens WH6.. BMC Genomics 2010 Sep 28;11:522.
- Krause J, Dear PH, Pollack JL, Slatkin M, Spriggs H, Barnes I, Lister AM, Ebersberger I, Pääbo S, Hofreiter M. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae.. Nature 2006 Feb 9;439(7077):724-7.
- Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Pääbo S. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia.. Nature 2010 Apr 8;464(7290):894-7.
- Krause J, Briggs AW, Kircher M, Maricic T, Zwyns N, Derevianko A, Pääbo S. A complete mtDNA genome of an early modern human from Kostenki, Russia.. Curr Biol 2010 Feb 9;20(3):231-6.
- Kuch M, Rohland N, Betancourt JL, Latorre C, Steppan S, Poinar HN. Molecular analysis of an 11,700-year-old rodent midden from the Atacama Desert, Chile.. Mol Ecol 2002 May;11(5):913-24.
- Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform.. Bioinformatics 2009 Jul 15;25(14):1754-60.
- Lindahl T. Instability and decay of the primary structure of DNA.. Nature 1993 Apr 22;362(6422):709-15.
- Lipson D, Raz T, Kieu A, Jones DR, Giladi E, Thayer E, Thompson JF, Letovsky S, Milos P, Causey M. Quantification of the yeast transcriptome by single-molecule sequencing.. Nat Biotechnol 2009 Jul;27(7):652-8.
- Malmström H, Gilbert MT, Thomas MG, Brandström M, Storå J, Molnar P, Andersen PK, Bendixen C, Holmlund G, Götherström A, Willerslev E. Ancient DNA reveals lack of continuity between neolithic hunter-gatherers and contemporary Scandinavians.. Curr Biol 2009 Nov 3;19(20):1758-62.
- Maricic T, Whitten M, Pääbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products.. PLoS One 2010 Nov 16;5(11):e14004.
- Metzker ML. Sequencing technologies - the next generation.. Nat Rev Genet 2010 Jan;11(1):31-46.
- Meyer M, Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing.. Cold Spring Harb Protoc 2010 Jun;2010(6):pdb.prot5448.
- Miller W, Drautz DI, Ratan A, Pusey B, Qi J, Lesk AM, Tomsho LP, Packard MD, Zhao F, Sher A, Tikhonov A, Raney B, Patterson N, Lindblad-Toh K, Lander ES, Knight JR, Irzyk GP, Fredrikson KM, Harkins TT, Sheridan S, Pringle T, Schuster SC. Sequencing the nuclear genome of the extinct woolly mammoth.. Nature 2008 Nov 20;456(7220):387-90.
- Mitchell D, Willerslev E, Hansen A. Damage and repair of ancient DNA.. Mutat Res 2005 Apr 1;571(1-2):265-76.
- Noonan JP, Hofreiter M, Smith D, Priest JR, Rohland N, Rabeder G, Krause J, Detter JC, Pääbo S, Rubin EM. Genomic sequencing of Pleistocene cave bears.. Science 2005 Jul 22;309(5734):597-9.
- Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, Chen F, Platt D, Pääbo S, Pritchard JK, Rubin EM. Sequencing and analysis of Neanderthal genomic DNA.. Science 2006 Nov 17;314(5802):1113-8.
- Oskam CL, Haile J, McLay E, Rigby P, Allentoft ME, Olsen ME, Bengtsson C, Miller GH, Schwenninger JL, Jacomb C, Walter R, Baynes A, Dortch J, Parker-Pearson M, Gilbert MT, Holdaway RN, Willerslev E, Bunce M. Fossil avian eggshell preserves ancient DNA.. Proc Biol Sci 2010 Jul 7;277(1690):1991-2000.
- Pääbo S. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification.. Proc Natl Acad Sci U S A 1989 Mar;86(6):1939-43.
- Pääbo S, Higuchi RG, Wilson AC. Ancient DNA and the polymerase chain reaction. The emerging field of molecular archaeology.. J Biol Chem 1989 Jun 15;264(17):9709-12.
- Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M. Genetic analyses from ancient DNA.. Annu Rev Genet 2004;38:645-79.
- Poinar H, Kuch M, McDonald G, Martin P, Pääbo S. Nuclear gene sequences from a late pleistocene sloth coprolite.. Curr Biol 2003 Jul 1;13(13):1150-2.
- Poinar HN, Schwarz C, Qi J, Shapiro B, Macphee RD, Buigues B, Tikhonov A, Huson DH, Tomsho LP, Auch A, Rampp M, Miller W, Schuster SC. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA.. Science 2006 Jan 20;311(5759):392-4.
- Pruvost M, Schwarz R, Correia VB, Champlot S, Braguier S, Morel N, Fernandez-Jalvo Y, Grange T, Geigl EM. 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.
- Pushkarev D, Neff NF, Quake SR. Single-molecule sequencing of an individual human genome.. Nat Biotechnol 2009 Sep;27(9):847-50.
- Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, Durbin R, Swerdlow H, Turner DJ. A large genome center's improvements to the Illumina sequencing system.. Nat Methods 2008 Dec;5(12):1005-10.
- R Development Core Team. R: A language and envionment for statistical computing. 2010.
- Ramírez O, Gigli E, Bover P, Alcover JA, Bertranpetit J, Castresana J, Lalueza-Fox C. Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean caprine.. PLoS One 2009 May 22;4(5):e5670.
- Rasmussen M, Li Y, Lindgreen S, Pedersen JS, Albrechtsen A, Moltke I, Metspalu M, Metspalu E, Kivisild T, Gupta R, Bertalan M, Nielsen K, Gilbert MT, Wang Y, Raghavan M, Campos PF, Kamp HM, Wilson AS, Gledhill A, Tridico S, Bunce M, Lorenzen ED, Binladen J, Guo X, Zhao J, Zhang X, Zhang H, Li Z, Chen M, Orlando L, Kristiansen K, Bak M, Tommerup N, Bendixen C, Pierre TL, Grønnow B, Meldgaard M, Andreasen C, Fedorova SA, Osipova LP, Higham TF, Ramsey CB, Hansen TV, Nielsen FC, Crawford MH, Brunak S, Sicheritz-Pontén T, Villems R, Nielsen R, Krogh A, Wang J, Willerslev E. Ancient human genome sequence of an extinct Palaeo-Eskimo.. Nature 2010 Feb 11;463(7282):757-62.
- Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL, Maricic T, Good JM, Marques-Bonet T, Alkan C, Fu Q, Mallick S, Li H, Meyer M, Eichler EE, Stoneking M, Richards M, Talamo S, Shunkov MV, Derevianko AP, Hublin JJ, Kelso J, Slatkin M, Pääbo S. Genetic history of an archaic hominin group from Denisova Cave in Siberia.. Nature 2010 Dec 23;468(7327):1053-60.
- Rohland N, Hofreiter M. Ancient DNA extraction from bones and teeth.. Nat Protoc 2007;2(7):1756-62.
- Rohland N, Malaspinas AS, Pollack JL, Slatkin M, Matheus P, Hofreiter M. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup.. PLoS Biol 2007 Aug;5(8):e207.
- Rohland N, Reich D, Mallick S, Meyer M, Green RE, Georgiadis NJ, Roca AL, Hofreiter M. Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants.. PLoS Biol 2010 Dec 21;8(12):e1000564.
- Römpler H, Rohland N, Lalueza-Fox C, Willerslev E, Kuznetsova T, Rabeder G, Bertranpetit J, Schöneberg T, Hofreiter M. Nuclear gene indicates coat-color polymorphism in mammoths.. Science 2006 Jul 7;313(5783):62.
- Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N. 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.
- Salamon M, Tuross N, Arensburg B, Weiner S. 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.
- Schwarz C, Debruyne R, Kuch M, McNally E, Schwarcz H, Aubrey AD, Bada J, Poinar H. New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains.. Nucleic Acids Res 2009 Jun;37(10):3215-29.
- Shapiro B, Drummond AJ, Rambaut A, Wilson MC, Matheus PE, Sher AV, Pybus OG, Gilbert MT, Barnes I, Binladen J, Willerslev E, Hansen AJ, Baryshnikov GF, Burns JA, Davydov S, Driver JC, Froese DG, Harington CR, Keddie G, Kosintsev P, Kunz ML, Martin LD, Stephenson RO, Storer J, Tedford R, Zimov S, Cooper A. Rise and fall of the Beringian steppe bison.. Science 2004 Nov 26;306(5701):1561-5.
- Shendure J, Ji H. Next-generation DNA sequencing.. Nat Biotechnol 2008 Oct;26(10):1135-45.
- Stiller M, Green RE, Ronan M, Simons JF, Du L, He W, Egholm M, Rothberg JM, Keates SG, Ovodov ND, Antipina EE, Baryshnikov GF, Kuzmin YV, Vasilevski AA, Wuenschell GE, Termini J, Hofreiter M, Jaenicke-Després V, Pääbo S. 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.
- Stiller M, Baryshnikov G, Bocherens H, Grandal d'Anglade A, Hilpert B, Münzel SC, Pinhasi R, Rabeder G, Rosendahl W, Trinkaus E, Hofreiter M, Knapp M. Withering away--25,000 years of genetic decline preceded cave bear extinction.. Mol Biol Evol 2010 May;27(5):975-8.
- Thompson JF, Steinmann KE. Single molecule sequencing with a HeliScope genetic analysis system.. Curr Protoc Mol Biol 2010 Oct;Chapter 7:Unit7.10.
- Wall JD, Kim SK. Inconsistencies in Neanderthal genomic DNA sequences.. PLoS Genet 2007 Oct;3(10):1862-6.
- Willerslev E, Cooper A. Ancient DNA.. Proc Biol Sci 2005 Jan 7;272(1558):3-16.
- Willerslev E, Hansen AJ, Binladen J, Brand TB, Gilbert MT, Shapiro B, Bunce M, Wiuf C, Gilichinsky DA, Cooper A. Diverse plant and animal genetic records from Holocene and Pleistocene sediments.. Science 2003 May 2;300(5620):791-5.
- Willerslev E, Hansen AJ, Rønn R, Brand TB, Barnes I, Wiuf C, Gilichinsky D, Mitchell D, Cooper A. Long-term persistence of bacterial DNA.. Curr Biol 2004 Jan 6;14(1):R9-10.
- Willerslev E, Cappellini E, Boomsma W, Nielsen R, Hebsgaard MB, Brand TB, Hofreiter M, Bunce M, Poinar HN, Dahl-Jensen D, Johnsen S, Steffensen JP, Bennike O, Schwenninger JL, Nathan R, Armitage S, de Hoog CJ, Alfimov V, Christl M, Beer J, Muscheler R, Barker J, Sharp M, Penkman KE, Haile J, Taberlet P, Gilbert MT, Casoli A, Campani E, Collins MJ. Ancient biomolecules from deep ice cores reveal a forested southern Greenland.. Science 2007 Jul 6;317(5834):111-4.
- Willerslev E, Gilbert MT, Binladen J, Ho SY, Campos PF, Ratan A, Tomsho LP, da Fonseca RR, Sher A, Kuznetsova TV, Nowak-Kemp M, Roth TL, Miller W, Schuster SC. Analysis of complete mitochondrial genomes from extinct and extant rhinoceroses reveals lack of phylogenetic resolution.. BMC Evol Biol 2009 May 11;9:95.
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This article has been cited 50 times.- Sharko F, Slobodova N, Boulygina E, Cheprasov M, Gladysheva-Azgari M, Tsygankova S, Rastorguev S, Novgorodov G, Boeskorov G, Grigorieva L, Hwang WS, Tikhonov A, Nedoluzhko A. Ancient DNA of the Don-Hares Assumes the Existence of Two Distinct Mitochondrial Clades in Northeast Asia.. Genes (Basel) 2023 Mar 12;14(3).
- Gao L, Xu W, Xin T, Song J. Application of third-generation sequencing to herbal genomics.. Front Plant Sci 2023;14:1124536.
- Boulygina E, Sharko F, Cheprasov M, Gladysheva-Azgari M, Slobodova N, Tsygankova S, Rastorguev S, Grigorieva L, Kopp M, Fernandes JMO, Novgorodov G, Boeskorov G, Protopopov A, Hwang WS, Tikhonov A, Nedoluzhko A. Ancient DNA Reveals Maternal Philopatry of the Northeast Eurasian Brown Bear (Ursus arctos) Population during the Holocene.. Genes (Basel) 2022 Oct 27;13(11).
- Zacho CM, Bager MA, Margaryan A, Gravlund P, Galatius A, Rasmussen AR, Allentoft ME. Uncovering the genomic and metagenomic research potential in old ethanol-preserved snakes.. PLoS One 2021;16(8):e0256353.
- Zhang M, Cao P, Dai Q, Wang Y, Feng X, Wang H, Wu H, Ko AM, Mao X, Liu Y, Yu L, Roos C, Nadler T, Xiao W, Bennett EA, Fu Q. Comparative analysis of DNA extraction protocols for ancient soft tissue museum samples.. Zool Res 2021 May 18;42(3):280-286.
- Xavier C, Eduardoff M, Bertoglio B, Amory C, Berger C, Casas-Vargas A, Pallua J, Parson W. Evaluation of DNA Extraction Methods Developed for Forensic and Ancient DNA Applications Using Bone Samples of Different Age.. Genes (Basel) 2021 Jan 22;12(2).
- Mubemba B, Gogarten JF, Schuenemann VJ, Düx A, Lang A, Nowak K, Pléh K, Reiter E, Ulrich M, Agbor A, Brazzola G, Deschner T, Dieguez P, Granjon AC, Jones S, Junker J, Wessling E, Arandjelovic M, Kuehl H, Wittig RM, Leendertz FH, Calvignac-Spencer S. Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue.. Microb Genom 2020 Nov;6(11).
- Gakuhari T, Nakagome S, Rasmussen S, Allentoft ME, Sato T, Korneliussen T, Chuinneagáin BN, Matsumae H, Koganebuchi K, Schmidt R, Mizushima S, Kondo O, Shigehara N, Yoneda M, Kimura R, Ishida H, Masuyama T, Yamada Y, Tajima A, Shibata H, Toyoda A, Tsurumoto T, Wakebe T, Shitara H, Hanihara T, Willerslev E, Sikora M, Oota H. Ancient Jomon genome sequence analysis sheds light on migration patterns of early East Asian populations.. Commun Biol 2020 Aug 25;3(1):437.
- Bailleul AM, O'Connor J, Schweitzer MH. Dinosaur paleohistology: review, trends and new avenues of investigation.. PeerJ 2019;7:e7764.
- Raudsepp T, Finno CJ, Bellone RR, Petersen JL. Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era.. Anim Genet 2019 Dec;50(6):569-597.
- Lan TM, Lin Y, Njaramba-Ngatia J, Guo XS, Li RG, Li HM, Kumar-Sahu S, Wang X, Yang XJ, Guo HB, Xu WH, Kristiansen K, Liu H, Xu YC. Improving Species Identification of Ancient Mammals Based on Next-Generation Sequencing Data.. Genes (Basel) 2019 Jul 5;10(7).
- Peyrégne S, Slon V, Mafessoni F, de Filippo C, Hajdinjak M, Nagel S, Nickel B, Essel E, Le Cabec A, Wehrberger K, Conard NJ, Kind CJ, Posth C, Krause J, Abrams G, Bonjean D, Di Modica K, Toussaint M, Kelso J, Meyer M, Pääbo S, Prüfer K. Nuclear DNA from two early Neandertals reveals 80,000 years of genetic continuity in Europe.. Sci Adv 2019 Jun;5(6):eaaw5873.
- Honka J, Heino MT, Kvist L, Askeyev IV, Shaymuratova DN, Askeyev OV, Askeyev AO, Heikkinen ME, Searle JB, Aspi J. Over a Thousand Years of Evolutionary History of Domestic Geese from Russian Archaeological Sites, Analysed Using Ancient DNA.. Genes (Basel) 2018 Jul 20;9(7).
- Hahn A, Bendall ML, Gibson KM, Chaney H, Sami I, Perez GF, Koumbourlis AC, McCaffrey TA, Freishtat RJ, Crandall KA. Benchmark Evaluation of True Single Molecular Sequencing to Determine Cystic Fibrosis Airway Microbiome Diversity.. Front Microbiol 2018;9:1069.
- Mak SST, Gopalakrishnan S, Carøe C, Geng C, Liu S, Sinding MS, Kuderna LFK, Zhang W, Fu S, Vieira FG, Germonpré M, Bocherens H, Fedorov S, Petersen B, Sicheritz-Pontén T, Marques-Bonet T, Zhang G, Jiang H, Gilbert MTP. Comparative performance of the BGISEQ-500 vs Illumina HiSeq2500 sequencing platforms for palaeogenomic sequencing.. Gigascience 2017 Aug 1;6(8):1-13.
- Zaucha J, Heddle JG. Resurrecting the Dead (Molecules).. Comput Struct Biotechnol J 2017;15:351-358.
- Philips A, Stolarek I, Kuczkowska B, Juras A, Handschuh L, Piontek J, Kozlowski P, Figlerowicz M. Comprehensive analysis of microorganisms accompanying human archaeological remains.. Gigascience 2017 Jul 1;6(7):1-13.
- Mizuno F, Kumagai M, Kurosaki K, Hayashi M, Sugiyama S, Ueda S, Wang L. Imputation approach for deducing a complete mitogenome sequence from low-depth-coverage next-generation sequencing data: application to ancient remains from the Moon Pyramid, Mexico.. J Hum Genet 2017 Jun;62(6):631-635.
- Nistelberger HM, Smith O, Wales N, Star B, Boessenkool S. The efficacy of high-throughput sequencing and target enrichment on charred archaeobotanical remains.. Sci Rep 2016 Nov 24;6:37347.
- Mohandesan E, Speller CF, Peters J, Uerpmann HP, Uerpmann M, De Cupere B, Hofreiter M, Burger PA. Combined hybridization capture and shotgun sequencing for ancient DNA analysis of extinct wild and domestic dromedary camel.. Mol Ecol Resour 2017 Mar;17(2):300-313.
- Kanda K, Pflug JM, Sproul JS, Dasenko MA, Maddison DR. Successful Recovery of Nuclear Protein-Coding Genes from Small Insects in Museums Using Illumina Sequencing.. PLoS One 2015;10(12):e0143929.
- Duchemin W, Daubin V, Tannier E. Reconstruction of an ancestral Yersinia pestis genome and comparison with an ancient sequence.. BMC Genomics 2015;16 Suppl 10(Suppl 10):S9.
- Olalde I, Schroeder H, Sandoval-Velasco M, Vinner L, Lobón I, Ramirez O, Civit S, García Borja P, Salazar-García DC, Talamo S, María Fullola J, Xavier Oms F, Pedro M, Martínez P, Sanz M, Daura J, Zilhão J, Marquès-Bonet T, Gilbert MT, Lalueza-Fox C. A Common Genetic Origin for Early Farmers from Mediterranean Cardial and Central European LBK Cultures.. Mol Biol Evol 2015 Dec;32(12):3132-42.
- Damgaard PB, Margaryan A, Schroeder H, Orlando L, Willerslev E, Allentoft ME. Improving access to endogenous DNA in ancient bones and teeth.. Sci Rep 2015 Jun 17;5:11184.
- Allentoft ME, Sikora M, Sjögren KG, Rasmussen S, Rasmussen M, Stenderup J, Damgaard PB, Schroeder H, Ahlström T, Vinner L, Malaspinas AS, Margaryan A, Higham T, Chivall D, Lynnerup N, Harvig L, Baron J, Della Casa P, Dąbrowski P, Duffy PR, Ebel AV, Epimakhov A, Frei K, Furmanek M, Gralak T, Gromov A, Gronkiewicz S, Grupe G, Hajdu T, Jarysz R, Khartanovich V, Khokhlov A, Kiss V, Kolář J, Kriiska A, Lasak I, Longhi C, McGlynn G, Merkevicius A, Merkyte I, Metspalu M, Mkrtchyan R, Moiseyev V, Paja L, Pálfi G, Pokutta D, Pospieszny Ł, Price TD, Saag L, Sablin M, Shishlina N, Smrčka V, Soenov VI, Szeverényi V, Tóth G, Trifanova SV, Varul L, Vicze M, Yepiskoposyan L, Zhitenev V, Orlando L, Sicheritz-Pontén T, Brunak S, Nielsen R, Kristiansen K, Willerslev E. Population genomics of Bronze Age Eurasia.. Nature 2015 Jun 11;522(7555):167-72.
- Orlando L, Gilbert MT, Willerslev E. Reconstructing ancient genomes and epigenomes.. Nat Rev Genet 2015 Jul;16(7):395-408.
- Parks M, Lambert D. Impacts of low coverage depths and post-mortem DNA damage on variant calling: a simulation study.. BMC Genomics 2015 Jan 23;16(1):19.
- Der Sarkissian C, Allentoft ME, Ávila-Arcos MC, Barnett R, Campos PF, Cappellini E, Ermini L, Fernández R, da Fonseca R, Ginolhac A, Hansen AJ, Jónsson H, Korneliussen T, Margaryan A, Martin MD, Moreno-Mayar JV, Raghavan M, Rasmussen M, Velasco MS, Schroeder H, Schubert M, Seguin-Orlando A, Wales N, Gilbert MT, Willerslev E, Orlando L. Ancient genomics.. Philos Trans R Soc Lond B Biol Sci 2015 Jan 19;370(1660):20130387.
- Turki T, Roshan U. MaxSSmap: a GPU program for mapping divergent short reads to genomes with the maximum scoring subsequence.. BMC Genomics 2014 Nov 15;15(1):969.
- Lindgreen S, Krogh A, Pedersen JS. SNPest: a probabilistic graphical model for estimating genotypes.. BMC Res Notes 2014 Oct 7;7:698.
- Ramos-Onsins SE, Burgos-Paz W, Manunza A, Amills M. Mining the pig genome to investigate the domestication process.. Heredity (Edinb) 2014 Dec;113(6):471-84.
- Finno CJ, Bannasch DL. Applied equine genetics.. Equine Vet J 2014 Sep;46(5):538-44.
- Kerpedjiev P, Frellsen J, Lindgreen S, Krogh A. Adaptable probabilistic mapping of short reads using position specific scoring matrices.. BMC Bioinformatics 2014 Apr 9;15:100.
- Star B, Nederbragt AJ, Hansen MH, Skage M, Gilfillan GD, Bradbury IR, Pampoulie C, Stenseth NC, Jakobsen KS, Jentoft S. Palindromic sequence artifacts generated during next generation sequencing library preparation from historic and ancient DNA.. PLoS One 2014;9(3):e89676.
- Campana MG, Robles García N, Rühli FJ, Tuross N. False positives complicate ancient pathogen identifications using high-throughput shotgun sequencing.. BMC Res Notes 2014 Feb 25;7:111.
- Overballe-Petersen S, Harms K, Orlando LA, Mayar JV, Rasmussen S, Dahl TW, Rosing MT, Poole AM, Sicheritz-Ponten T, Brunak S, Inselmann S, de Vries J, Wackernagel W, Pybus OG, Nielsen R, Johnsen PJ, Nielsen KM, Willerslev E. Bacterial natural transformation by highly fragmented and damaged DNA.. Proc Natl Acad Sci U S A 2013 Dec 3;110(49):19860-5.
- Seguin-Orlando A, Schubert M, Clary J, Stagegaard J, Alberdi MT, Prado JL, Prieto A, Willerslev E, Orlando L. Ligation bias in illumina next-generation DNA libraries: implications for sequencing ancient genomes.. PLoS One 2013;8(10):e78575.
- Meyer JB, Cartier LE, Pinto-Figueroa EA, Krzemnicki MS, Hänni HA, McDonald BA. DNA fingerprinting of pearls to determine their origins.. PLoS One 2013;8(10):e75606.
- Dabney J, Knapp M, Glocke I, Gansauge MT, Weihmann A, Nickel B, Valdiosera C, García N, Pääbo S, Arsuaga JL, Meyer M. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments.. Proc Natl Acad Sci U S A 2013 Sep 24;110(39):15758-63.
- Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
- Dabney J, Meyer M, Pääbo S. Ancient DNA damage.. Cold Spring Harb Perspect Biol 2013 Jul 1;5(7).
- Allentoft ME, Collins M, Harker D, Haile J, Oskam CL, Hale ML, Campos PF, Samaniego JA, Gilbert MT, Willerslev E, Zhang G, Scofield RP, Holdaway RN, Bunce M. The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils.. Proc Biol Sci 2012 Dec 7;279(1748):4724-33.
- Meyer M, Kircher M, Gansauge MT, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prüfer K, de Filippo C, Sudmant PH, Alkan C, Fu Q, Do R, Rohland N, Tandon A, Siebauer M, Green RE, Bryc K, Briggs AW, Stenzel U, Dabney J, Shendure J, Kitzman J, Hammer MF, Shunkov MV, Derevianko AP, Patterson N, Andrés AM, Eichler EE, Slatkin M, Reich D, Kelso J, Pääbo S. A high-coverage genome sequence from an archaic Denisovan individual.. Science 2012 Oct 12;338(6104):222-6.
- Lindgreen S. AdapterRemoval: easy cleaning of next-generation sequencing reads.. BMC Res Notes 2012 Jul 2;5:337.
- Rizzi E, Lari M, Gigli E, De Bellis G, Caramelli D. Ancient DNA studies: new perspectives on old samples.. Genet Sel Evol 2012 Jul 6;44(1):21.
- Schubert M, Ginolhac A, Lindgreen S, Thompson JF, Al-Rasheid KA, Willerslev E, Krogh A, Orlando L. Improving ancient DNA read mapping against modern reference genomes.. BMC Genomics 2012 May 10;13:178.
- Ginolhac A, Vilstrup J, Stenderup J, Rasmussen M, Stiller M, Shapiro B, Zazula G, Froese D, Steinmann KE, Thompson JF, Al-Rasheid KA, Gilbert TM, Willerslev E, Orlando L. Improving the performance of true single molecule sequencing for ancient DNA.. BMC Genomics 2012 May 10;13:177.
- Ozsolak F. Third-generation sequencing techniques and applications to drug discovery.. Expert Opin Drug Discov 2012 Mar;7(3):231-43.
- Achilli A, Olivieri A, Soares P, Lancioni H, Hooshiar Kashani B, Perego UA, Nergadze SG, Carossa V, Santagostino M, Capomaccio S, Felicetti M, Al-Achkar W, Penedo MC, Verini-Supplizi A, Houshmand M, Woodward SR, Semino O, Silvestrelli M, Giulotto E, Pereira L, Bandelt HJ, Torroni A. Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication.. Proc Natl Acad Sci U S A 2012 Feb 14;109(7):2449-54.
- García-Garcerà M, Gigli E, Sanchez-Quinto F, Ramirez O, Calafell F, Civit S, Lalueza-Fox C. Fragmentation of contaminant and endogenous DNA in ancient samples determined by shotgun sequencing; prospects for human palaeogenomics.. PLoS One 2011;6(8):e24161.
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