期刊论文详细信息
BMC Research Notes
False positives complicate ancient pathogen identifications using high-throughput shotgun sequencing
Noreen Tuross1  Frank J Rühli3  Nelly Robles García2  Michael G Campana3 
[1] Department of Human Evolutionary Biology, Harvard University, Peabody Museum, 11 Divinity Avenue, Cambridge, MA 02138, USA;Instituto Nacional de Antropología e Historia, Mexico City, Mexico;Centre for Evolutionary Medicine, Anatomy Institute, University of Zurich, 190 Winterthurerstrasse, Zurich 8057, Switzerland
关键词: False positive;    Ancient DNA;    Pathogen;    High-throughput sequencing;    True single molecule sequencing;   
Others  :  1134415
DOI  :  10.1186/1756-0500-7-111
 received in 2014-02-19, accepted in 2014-02-20,  发布年份 2014
PDF
【 摘 要 】

Background

Identification of historic pathogens is challenging since false positives and negatives are a serious risk. Environmental non-pathogenic contaminants are ubiquitous. Furthermore, public genetic databases contain limited information regarding these species. High-throughput sequencing may help reliably detect and identify historic pathogens.

Results

We shotgun-sequenced 8 16th-century Mixtec individuals from the site of Teposcolula Yucundaa (Oaxaca, Mexico) who are reported to have died from the huey cocoliztli (‘Great Pestilence’ in Nahautl), an unknown disease that decimated native Mexican populations during the Spanish colonial period, in order to identify the pathogen. Comparison of these sequences with those deriving from the surrounding soil and from 4 precontact individuals from the site found a wide variety of contaminant organisms that confounded analyses. Without the comparative sequence data from the precontact individuals and soil, false positives for Yersinia pestis and rickettsiosis could have been reported.

Conclusions

False positives and negatives remain problematic in ancient DNA analyses despite the application of high-throughput sequencing. Our results suggest that several studies claiming the discovery of ancient pathogens may need further verification. Additionally, true single molecule sequencing’s short read lengths, inability to sequence through DNA lesions, and limited ancient-DNA-specific technical development hinder its application to palaeopathology.

【 授权许可】

   
2014 Campana et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150305202756420.pdf 288KB PDF download
【 参考文献 】
  • [1]Papagrigorakis MJ, Yapijakis C, Synodinos PN, Baziotopoulou-Valavani E: DNA examination of ancient dental pulp incriminates typhoid fever as a probable cause of the Plague of Athens. Int J Infect Dis 2006, 10:206-214.
  • [2]Shapiro B, Rambaut A, Gilbert MTP: No proof that typhoid caused the Plague of Athens (a reply to Papagrigorakis et al.). Int J Infect Dis 2006, 10:334-335.
  • [3]Drancourt M, Aboudharam G, Signoli M, Dutour O, Raoult D: Detection of 400-year-old Yersinia pestis DNA in human dental pulp: an approach to the diagnosis of ancient septicemia. Proc Natl Acad Sci USA 1998, 95:12637-12640.
  • [4]Zink AR, Sola C, Reischl U, Grabner W, Rastogi N, Wolf H, Nerlich AG: Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J Clin Microbiol 2003, 41:359-367.
  • [5]Nguyen-Hieu T, Aboudharam G, Signoli M, Rigeade C, Drancourt M, Raoult D: Evidence of a louse-born outbreak involving typhus in Douai, 1710–1712 during the War of Spanish Succession. PLoS One 2010, 5:e15405.
  • [6]Gernaey AM, Minnikin DE, Copley MS, Dixon RA, Middleton JC, Roberts CA: Mycolic acids and ancient DNA confirm an osteological diagnosis of tuberculosis. Tuberculosis 2001, 81:259-265.
  • [7]Kolman CJ, Centurion-Lara A, Lukehart SA, Owsley DA, Tuross N: Identification of Treponema pallidum subspecies pallidum in a 200-year-old skeletal specimen. J Infect Dis 2060–2063, 1999:180.
  • [8]Bianucci R, Rahalison L, Ferroglio E, Massa ER, Signoli M: Détection de l’antigène F1 de Yersinia pestis dans les restes humains anciens à l’aide d’un test de diagnostic rapide. C R Biol 2007, 330:747-754.
  • [9]Bianucci R, Rahalison L, Massa ER, Peluso A, Ferroglio E, Signoli M: Technical note: a rapid diagnostic test detects plague in ancient human remains: an example of the interaction between archaeological and biological approaches (Southeastern France, 16th‒18th centuries). Am J Phys Anthropol 2008, 136:361-367.
  • [10]Bianucci R, Rahalison L, Peluso A, Massa ER, Ferroglio E, Signoli M, Langlois J-Y, Gallien V: Plague immunodetection in remains of religious exhumed from burial sites in central France. J Arch Sci 2009, 36:616-621.
  • [11]Haensch S, Bianucci R, Signoli M, Rajerison M, Schultz M, Kacki S, Vermunt M, Weston DA, Hurst D, Achtman M, Carniel E, Bramanti B: Distinct clones of Yersinia pestis caused the Black Death. PLoS Pathog 2010, 6:e1001134.
  • [12]Kacki S, Rahalison L, Rajerison M, Ferroglio E, Bianucci R: Black Death in the rural cemetery of Saint-Laurent-de-la-Cabrerisse Aude-Languedoc, southern France, 14th century: immunological evidence. J Arch Sci 2011, 38:581-587.
  • [13]Schuenemann VJ, Bos K, DeWitte S, Schmedes S, Jamieson J, Mittnik A, Forrest S, Coombes BK, Wood JW, Earn DJD, White W, Krause J, Poinar HN: Targeted enrichment of ancient pathogens yielding the pPCP1 plasmid of Yersinia pestis from victims of the Black Death. Proc Natl Acad Sci USA 2011, 108:E746-E752.
  • [14]Bos KI, Schuenemann VJ, Golding GB, Burbano HA, Waglechner N, Coombes BK, McPhee JB, DeWitte SN, Meyer M, Schmedes S, Wood J, Earn DJD, Herring DA, Bauer P, Poinar HN, Krause J: A draft genome of Yersinia pestis from victims of the Black Death. Nature 2011, 478:506-510.
  • [15]Barnes I, Thomas MG: Evaluating bacterial pathogen DNA preservation in museum osteological collections. P Roy Soc B 2006, 273:645-653.
  • [16]Bouwman AS, Brown TA: The limits of biomolecular palaeopathology: ancient DNA cannot be used to study venereal syphilis. J Arch Sci 2005, 32:703-713.
  • [17]Gilbert MTP, Cuccui J, White W, Lynnerup N, Titball RW, Cooper A, Prentice MB: Absence of Yersinia pestis-specific DNA in human teeth from five European excavations of putative plague victims. Microbiology 2004, 150:341-354.
  • [18]Gilbert MTP, Rudbeck L, Willerslev E, Hansen AJ, Smith C, Penkman KEH, Prangenberg K, Nielsen-Marsh CM, Jans ME, Arthur P, Lynnerup N, Turner-Walker G, Biddle M, Kjølbye-Biddle B, Collins MJ: Biochemical and physical correlates of DNA contamination in archaeological human bones and teeth excavated at Matera, Italy. J Arch Sci 2005, 32:785-793.
  • [19]Gilbert MTP, Hansen AJ, Willerslev E, Turner-Walker G, Collins M: Insights into the processes behind the contamination of degraded human teeth and bone samples with exogenous sources of DNA. Int J Osteoarchaeol 2006, 16:156-164.
  • [20]Pääbo S, Poinar H, Serre D, Jaenicke-Després V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M: Genetic analyses from ancient DNA. Annu Rev Genet 2004, 38:645-679.
  • [21]Drancourt M, Raoult DR: Palaeomicrobiology: current issues and perspectives. Nat Rev Microbiol 2005, 3:23-35.
  • [22]Roberts C, Ingham S: Using ancient DNA analysis in palaeopathology: a critical analysis of published papers and recommendations for future work. Int J Osteoarchaeol 2008, 18:600-613.
  • [23]Tsangaras K, Greenwood AD: Museums and disease: using tissue archive and museum samples to study pathogens. Ann Anat 2012, 194:58-73.
  • [24]Thèves C, Senescau A, Vanin S, Keyser C, Ricaut FX, Alekseev AN, Dabernat H, Ludes B, Fabre R, Crubézy : Molecular identification of bacteria by total sequence screening: determining the cause of death in ancient human subjects. PLoS One 2011, 6:e21733.
  • [25]Knapp M, Hofreiter M: Next generation sequencing of ancient DNA: requirements, strategies and perspectives. Genes 2010, 1:227-243.
  • [26]Acuna-Soto R, Stahle DW, Therrell MD, Griffin RD, Cleaveland MK: When half of the population died: the epidemic of hemorrhagic fevers of 1576 in Mexico. FEMS Microbiol Lett 2004, 240:1-5.
  • [27]Warinner C, Robles García N, Spores R, Tuross N: Disease, demography, and diet in early colonial New Spain: investigation of a sixteenth-century Mixtec cemetery at Teposcolula Yucundaa. Lat Am Antiq 2012, 23:467-489.
  • [28]Marr JS, Kiracofe JB: Was the huey cocoliztli a haemorrhagic fever? Med Hist 2000, 44:341-362.
  • [29]Warinner CG: Life and Death at Teposcolula Yucundaa: Mortuary, Archaeogenetic, and Isotopic Investigations of the Early Colonial Period in Mexico. Harvard University, Human Evolutionary Biology Department; 2010. [PhD thesis]
  • [30]Cooper A, Poinar HN: Ancient DNA: do it right or not at all. Science 2000, 289:1139.
  • [31]Debruyne R, Schwarz C, Poinar H: Comment on ‘Whole-genome shotgun sequencing of mitochondria from ancient hair shafts”. Science 2008, 322:857a.
  • [32]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 KAS, Gilbert MTP, Willerslev E: True single-molecule DNA sequencing of a pleistocene horse bone. Genome Res 2011, 21:1705-1719.
  • [33]Ginolhac A, Vilstrup J, Stenderup J, Rasmussen M, Stiller M, Shapiro B, Zazula G, Froese D, Steinmann KE, Thompson JF, Al-Rasheid KAS, Gilbert TMP, Willerslev E, Orlando L: Improving the performance of true single molecule sequencing for ancient DNA. BMC Genomics 2012, 13:177. BioMed Central Full Text
  • [34]Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD: PANDAseq: PAired-eND Assembler for Illumina sequences. BMC Bioinformatics 2012, 13:31. BioMed Central Full Text
  • [35]Lassman T, Hayashizaki Y, Daub CO: TagDust—a program to eliminate artifacts from next generation sequencing data. Bioinformatics 2009, 25:2839-2840.
  • [36]Li W, Fu L, Niu B, Wu S, Wooley J: Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 2012, 13:656-668.
  • [37]Andrews S: Fastqc: A Quality Control Tool For High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ webcite
  • [38]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup: The sequence alignment/map format and SAMtools. Bioinformatics 2078–2079, 2009:25.
  • [39]Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
  • [40]Li H, Durbin R: Fast and accurate long read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26:589-595.
  • [41]Schubert M, Ginolhac A, Lindgreen S, Thompson JF, Al-Rasheid KAS, Willerslev E, Krogh A, Orlando L: Improving ancient DNA read mapping against modern reference genomes. BMC Genomics 2012, 13:178. BioMed Central Full Text
  • [42]Zhang Z, Schwartz S, Wagner L, Miller W: A greedy algorithm for aligning DNA sequences. J Comput Biol 2000, 7:203-214.
  • [43]Huson D, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC: Integrative analysis of environmental sequences using MEGAN4. Genome Res 2011, 2011(21):1552-1560.
  • [44]R Core Team: R: A Language And Environment For Statistical Computing. Vienna: R Foundation for Statistical Computing; 2013.
  • [45]Hansen MA, Oey H, Fernandez-Valverde S, Jung C-H, Mattick JS: Biopieces: A Bioinformatics Toolset and Framework. http://www.biopieces.org webcite
  • [46]Jónsson H, Ginolhac A, Schubert M, Johnson P, Orlando L: mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 2013, 29(13):1682-1684.
  • [47]Briggs AW, Stenzel U, Johnson PLF, 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 USA 2007, 104:14616-14621.
  • [48]Acuna-Soto R, Calderon Romero L, Maguire JH: Large epidemics of hemorrhagic fevers in Mexico 1545–1815. Am J Trop Med Hyg 2000, 62:733-739.
  • [49]Acuna-Soto R, Stahle DW, Cleaveland MK, Therrell MD: Megadrought and megadeath in 16th century Mexico. Emerg Infect Dis 2002, 8:360-362.
  • [50]Gilbert MTP, Rambaut A, Wlasiuk G, Spira TJ, Pitchenik AE, Worobey M: The emergence of HIV/AIDS in the Americas and beyond. Proc Natl Acad Sci USA 2007, 104:18566-18570.
  • [51]Fordyce SL, Ávila-Arcos MC, Rasmussen M, Cappellini E, Romero-Navarro JA, Wales N, Alquezar-Planas DE, Penfield S, Brown TA, Vielle-Calzada J-P, Montiel R, Jørgensen T, Odegaard N, Jacobs M, Arriaza B, Higham TFG, Bronk Ramsey C, Willerslev E, Gilbert MTP: Deep sequencing of RNA from ancient maize kernels. PLoS One 2013, 8:e50961.
  • [52]Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, Bunce M, Muyembe J-J, Kabongo J-MM, Kalengayi RM, Van Marck E, Gilbert MTP, Wolinksy SM: Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 2008, 455:661-664.
  • [53]Khairat R, Ball M, Chang C-CH, Bianucci R, Nerlich AG, Trautmann M, Ismail S, Shanab GML, Karim AM, Gad YZ, Pusch CM: First insights into the metagenome of Egyptian mummies using next-generation sequencing. J Appl Genetics 2013, 54:309-325.
  • [54]Chan JZ-M, Sergeant MJ, Lee OY-C, Minnikin DE, Besra GS, Pap I, Spigelman M, Donoghue HD: Metagenomic analysis of tuberculosis in a mummy. N Engl J Med 2013, 369:289-290.
  • [55]Adler CJ, Dobney K, Weyrich LS, Kaidonis J, Walker AW, Haak W, Bradshaw CJA, Townsend G, Sołtysiak A, Alt KW, Parkhill J, Cooper A: Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet 2013, 45:450-455.
  • [56]Malmström H, Svensson EM, Gilbert MTP, Willerslev E, Götherström A, Holmlund G: More on contamination: the use of asymmetric molecular behavior to identify authentic ancient human DNA. Mol Biol Evol 2007, 24:998-1004.
  • [57]Costello M, Pugh TJ, Fennell TJ, Stewart C, Lichtenstein L, Meldrim JC, Fostel JF, Friedrich DC, Perrin D, Dionne D, Kim S, Gabriel SB, Lander ES, Fisher S, Getz G: Discovery and characterization of artifactual mutations in deep coverage targeted capture sequencing data due to oxidative DNA damage during sample preparation. Nucleic Acids Res 2013, 41:e67.
  文献评价指标  
  下载次数:11次 浏览次数:10次