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Novel contribution on the diagenetic physicochemical features of bone and teeth minerals, as substrates for ancient DNA typing

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Abstract

The extraction of DNA from skeletal remains is a major step in archeological or forensic contexts. However, diagenesis of mineralized tissues often compromises this task although bones and teeth may represent preservation niches allowing DNA to persist over a wide timescale. This exceptional persistence is not only explained on the basis of complex organo-mineral interactions through DNA adsorption on apatite crystals composing the mineral part of bones and teeth but is also linked to environmental factors such as low temperatures and/or a dry environment. The preservation of the apatite phase itself, as an adsorption substrate, is another crucial factor susceptible to significantly impact the retrieval of DNA. With the view to bring physicochemical evidence of the preservation or alteration of diagenetic biominerals, we developed here an analytical approach on various skeletal specimens (ranging from ancient archeological samples to recent forensic specimens), allowing us to highlight several diagenetic indices so as to better apprehend the complexity of bone diagenesis. Based on complementary techniques (X-ray diffraction (XRD), Fourier transform infrared (FTIR), calcium and phosphate titrations, SEM-EDX, and gravimetry), we have identified specific indices that allow differentiating 11 biological samples, primarily according to the crystallinity and maturation state of the apatite phase. A good correlation was found between FTIR results from the analysis of the v 3(PO4) and v 4(PO4) vibrational domains and XRD-based crystallinity features. A maximal amount of information has been sought from this analytical approach, by way of optimized posttreatment of the data (spectral subtraction and enhancement of curve-fitting parameters). The good overall agreement found between all techniques leads to a rather complete picture of the diagenetic changes undergone by these 11 skeletal specimens. Although the heterogeneity and scarcity of the studied samples did not allow us to seek direct correlations with DNA persistence, the physicochemical parameters described in this work permit a fine differentiation of key properties of apatite crystals among post mortem samples. As a perspective, this analytical approach could be extended to more numerous sets of specimens so as to draw statistical relationships between mineral and molecular conservation.

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References

  1. Tütken T, Vennemann TW (2011) Fossil bones and teeth: preservation or alteration of biogenic compositions? Palaeogeogr Palaeoclimatol Palaeoecol 310:1–8. doi:10.1016/j.palaeo.2011.06.020

    Article  Google Scholar 

  2. Price TD, Schoeninger MJ, Armelagos GJ (1985) Bone chemistry and past behavior: an overview. J Hum Evol 14:419–447

    Article  Google Scholar 

  3. Lee-Thorp JA (2008) On isotopes and old bones. Archaeometry 50:925–950. doi:10.1111/j.1475-4754.2008.00441.x

    Article  CAS  Google Scholar 

  4. Keyser-Tracqui C, Ludes B (2005) Methods for the study of ancient DNA. Methods Mol Biol 297:253–264

    CAS  Google Scholar 

  5. Rohland N, Hofreiter M (2007) Ancient DNA extraction from bones and teeth. Nat Protoc 2:1756–1762. doi:10.1038/nprot.2007.247

    Article  CAS  Google Scholar 

  6. Ostrom PH, Schall M, Gandhi H, Shen TL, Hauschka PV, Strahler JR, Gage DA (2000) New strategies for characterizing ancient proteins using matrix-assisted laser desorption ionization mass spectrometry. Geochim Cosmochim Acta 64:1043–1050. doi:10.1016/S0016-7037(99)00381-6

    Article  CAS  Google Scholar 

  7. Buckley M, Anderung C, Penkman K, Raney BJ, Gotherstrom A, Thomas-Oates J, Collins MJ (2008) Comparing the survival of osteocalcin and mtDNA in archaeological bone from four European sites. J Archaeol Sci 35:1756–1764. doi:10.1016/j.jas.2007.11.022

    Article  Google Scholar 

  8. Keyser C, Bouakaze C, Crubézy E, Nikolaev VG, Montagnon D, Reis T, Ludes B (2009) Ancient DNA provides new insights into the history of south Siberian Kurgan people. Hum Genet 126:395–410. doi:10.1007/s00439-009-0683-0

    Article  CAS  Google Scholar 

  9. Amory S, Huel R, Bilić A, Loreille O, Parsons TJ (2012) Automatable full demineralization DNA extraction procedure from degraded skeletal remains. Forensic Sci Int: Genet 6:398–406. doi:10.1016/j.fsigen.2011.08.004

    Article  CAS  Google Scholar 

  10. Orlando L, Ginolhac A, Zhang G et al (2013) Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499:74–78. doi:10.1038/nature12323

    Article  CAS  Google Scholar 

  11. Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38:645–679. doi:10.1146/annurev.genet.37.110801.143214

    Article  Google Scholar 

  12. Campos PF, Craig OE, Turner-Walker G, Peacock E, Willerslev E, Gilbert MTP (2012) DNA in ancient bone—where is it located and how should we extract it? Ann Anat-Anat Anz 194:7–16. doi:10.1016/j.aanat.2011.07.003

    Article  CAS  Google Scholar 

  13. Adler CJ, Haak W, Donlon D, Cooper A (2011) Survival and recovery of DNA from ancient teeth and bones. J Archaeol Sci 38:956–964. doi:10.1016/j.jas.2010.11.010

    Article  Google Scholar 

  14. Higgins D, Austin JJ (2013) Teeth as a source of DNA for forensic identification of human remains: a review. Sci Justice 53:433–441. doi:10.1016/j.scijus.2013.06.001

    Article  CAS  Google Scholar 

  15. Gilbert MTP, Willerslev E, Hansen AJ, Barnes I, Rudbeck L, Lynnerup N, Cooper A (2003) Distribution patterns of postmortem damage in human mitochondrial DNA. Am J Hum Genet 72:32–47

    Article  CAS  Google Scholar 

  16. Rollin-Martinet S, Navrotsky A, Champion E, Grossin D, Drouet C (2013) Thermodynamic basis for evolution of apatite in calcified tissues. Am Mineral 98:2037–2045. doi:10.2138/am.2013.4537

    Article  CAS  Google Scholar 

  17. Eanes ED, Meyer JL (1977) The maturation of crystalline calcium phosphates in aqueous suspensions at physiologic pH. Calc Tis Res 23:259–269. doi:10.1007/BF02012795

    Article  CAS  Google Scholar 

  18. Rey C, Hina A, Tofighi A, Glimcher MJ (1995) Maturation of poorly crystalline apatites: chemical and structural aspects in vivo and in vitro. Cells Mat 5:345–356

    CAS  Google Scholar 

  19. Rey C, Lian J, Grynpas M, Shapiro F, Zylberberg L, Glimcher MJ (1989) Non-apatitic environments in bone mineral: FT-IR detection, biological properties and changes in several disease states. Connect Tissue Res 21:267–273

    Article  CAS  Google Scholar 

  20. Combes C, Rey C, Eichert D, Drouet C (2005) Formation and evolution of hydrated surface layers of apatites. Key Eng Mater 284:3–6

    Google Scholar 

  21. Rey C, Shimizu M, Collins B, Glimcher MJ (1991) Resolution-enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ion in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age: 2. Investigations in the v 3 PO4 domain. Calcif Tissue Int 49:383–388

    Article  CAS  Google Scholar 

  22. Rey C, Shimizu M, Collins B, Glimcher MJ (1990) Resolution-enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ions in the early deposits of a solid phase of calcium-phosphate in bone and enamel, and their evolution with age. I. Investigations in the v 4 PO4 domain. Calcif Tissue Int 46:384–394

    Article  CAS  Google Scholar 

  23. Cazalbou S, Eichert D, Ranz X, Drouet C, Combes C, Harmand MF, Rey C (2005) Ion exchanges in apatites for biomedical application. J Mater Sci Mater Med 16:405–409. doi:10.1007/s10856-005-6979-2

    Article  CAS  Google Scholar 

  24. Errassifi F, Menbaoui A, Autefage H et al (2010) Adsorption on apatitic calcium phosphates: applications to drug delivery. In: Narayan R, McKittrick J (eds) Advances in bioceramics and biotechnologies. Amer Ceramic Soc, Westerville, pp 159–174

    Google Scholar 

  25. Ouizat S, Barroug A, Legrouri A, Rey C (1999) Adsorption of bovine serum albumin on poorly crystalline apatite: influence of maturation. Mater Res Bull 34:2279–2289. doi:10.1016/S0025-5408(00)00167-7

    Article  CAS  Google Scholar 

  26. Posner AS (1985) The structure of bone apatite surfaces. J Biomed Mater Res 19:241–250. doi:10.1002/jbm.820190307

    Article  CAS  Google Scholar 

  27. Drouet C, Carayon MT, Combes C, Rey C (2005) Exchange of biologically relevant ions on nanocrystalline apatites. Geochim Cosmochim Acta 69:A69–A69

    Google Scholar 

  28. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715. doi:10.1038/362709a0

    Article  CAS  Google Scholar 

  29. Grunenwald A, Keyser C, Sautereau A-M, Crubézy E, Ludes B, Drouet C (2014) Adsorption of DNA on biomimetic apatites: towards the understanding of the role of bone and tooth mineral on the preservation of ancient DNA. Appl Surf Sci 292:867–875. doi:10.1016/j.apsusc.2013.12.063

    Article  CAS  Google Scholar 

  30. Götherström A, Collins MJ, Angerbjörn A, Lidén K (2002) Bone preservation and DNA amplification. Archaeometry 44:395–404. doi:10.1111/1475-4754.00072

    Article  Google Scholar 

  31. Hagelberg E, Bell LS, Allen T, Boyde A, Jones SJ, Clegg JB (1991) Analysis of ancient bone DNA: techniques and applications [and discussion]. Philos Trans R Soc Lond Ser B Biol Sci 333:399–407

    Article  CAS  Google Scholar 

  32. Cazalbou S, Eichert D, Drouet C, Combes C, Rey C (2004) Minéralisations biologiques à base de phosphate de calcium. Comptes Rendus Palevol 3:563–572. doi:10.1016/j.crpv.2004.07.003

    Article  Google Scholar 

  33. Trueman CN, Palmer MR, Field J, Privat K, Ludgate N, Chavagnac V, Eberth DA, Cifelli R, Rogers RR (2008) Comparing rates of recrystallisation and the potential for preservation of biomolecules from the distribution of trace elements in fossil bones. Comptes Rendus Palevol 7:145–158. doi:10.1016/j.crpv.2008.02.006

    Article  Google Scholar 

  34. Yi H, Balan E, Gervais C et al (2013) A carbonate-fluoride defect model for carbonate-rich fluorapatite. Am Mineral 98:1066–1069. doi:10.2138/am.2013.4445

    Article  CAS  Google Scholar 

  35. Sosa C, Vispe E, Núñez C, Baeta M, Casalod Y, Bolea M, Hedges REM, Martinez-Jarreta B (2013) Association between ancient bone preservation and DNA yield: a multidisciplinary approach. Am J Phys Anthropol 151:102–109. doi:10.1002/ajpa.22262

    Article  CAS  Google Scholar 

  36. Vandecandelaere N, Rey C, Drouet C (2012) Biomimetic apatite-based biomaterials: on the critical impact of synthesis and post-synthesis parameters. J Mater Sci Mater Med 23:2593–2606. doi:10.1007/s10856-012-4719-y

    Article  CAS  Google Scholar 

  37. Mendisco F, Keyser C, Hollard C et al (2011) Application of the iPLEXTM Gold SNP genotyping method for the analysis of Amerindian ancient DNA samples: benefits for ancient population studies. Electrophoresis 32:386–393. doi:10.1002/elps.201000483

    Article  CAS  Google Scholar 

  38. Gee A, Deitz VR (1953) Determination of phosphate by differential spectrophotometry. Anal Chem 25:1320–1324. doi:10.1021/ac60081a006

    Article  CAS  Google Scholar 

  39. Charlot G (1963) L’analyse qualitative et les réactions en solution. Masson, 1963, Paris, France

  40. Kauppinen JK, Moffatt DJ, Mantsch HH, Cameron DG (1981) Fourier self-deconvolution: a method for resolving intrinsically overlapped bands. Appl Spectrosc 35:271–276

    Article  CAS  Google Scholar 

  41. Vandecandelaère N (2012) Élaboration et caractérisation de biomatériaux osseux innovants à base d’apatites phospho-calciques dopées. INPT

  42. Rowles S (1965) Studies on non-stoichiometric apatites. In: Stack MV, Fearnhead RW (eds) Tooth enamel: its composition, properties and fundamental structure. John Wright et Sons LTD, Bristol, Royaume-Uni, pp 23–25, 56–57

  43. Person A, Bocherens H, Saliège J-F, Paris F, Zeitoun V, Gerard M (1995) Early diagenetic evolution of bone phosphate: an X-ray diffractometry analysis. J Archaeol Sci 22:211–221. doi:10.1006/jasc.1995.0023

    Article  Google Scholar 

  44. Thompson TJU, Islam M, Piduru K, Marcel A (2011) An investigation into the internal and external variables acting on crystallinity index using Fourier transform infrared spectroscopy on unaltered and burned bone. Palaeogeogr Palaeoclimatol Palaeoecol 299:168–174. doi:10.1016/j.palaeo.2010.10.044

    Article  Google Scholar 

  45. Pucéat E, Reynard B, Lécuyer C (2004) Can crystallinity be used to determine the degree of chemical alteration of biogenic apatites? Chem Geol 205:83–97. doi:10.1016/j.chemgeo.2003.12.014

    Article  Google Scholar 

  46. Lebon M, Müller K, Bellot-Gurlet L, et al. (2012) Application des micro-spectrométries infrarouge et Raman à l’étude des processus diagénétiques altérant les ossements paléolithiques. ArchéoSciences no. 35:179–190

  47. McElderry J-DP, Zhu P, Mroue KH et al (2013) Crystallinity and compositional changes in carbonated apatites: evidence from 31P solid-state NMR, Raman, and AFM analysis. J Solid State Chem 206:192–198. doi:10.1016/j.jssc.2013.08.011

    Article  CAS  Google Scholar 

  48. Sader MS, Lewis K, Soares GA, LeGeros RZ (2013) Simultaneous incorporation of magnesium and carbonate in apatite: effect on physico-chemical properties. Mater Res 16:779–784. doi:10.1590/S1516-14392013005000046

    Article  CAS  Google Scholar 

  49. LeGeros RZ (1991) Calcium phosphates in oral biology and medicine. Monogr Oral Sci 15:1–201

    CAS  Google Scholar 

  50. Boskey AL, Mendelsohn R (2005) Infrared spectroscopic characterization of mineralized tissues. Vib Spectrosc 38:107–114. doi:10.1016/j.vibspec.2005.02.015

    Article  CAS  Google Scholar 

  51. Trueman CN, Privat K, Field J (2008) Why do crystallinity values fail to predict the extent of diagenetic alteration of bone mineral? Palaeogeogr Palaeoclimatol Palaeoecol 266:160–167. doi:10.1016/j.palaeo.2008.03.038

    Article  Google Scholar 

  52. Farlay D, Panczer G, Rey C, Delmas PD, Boivin G (2010) Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab 28:433–445. doi:10.1007/s00774-009-0146-7

    Article  Google Scholar 

  53. Trueman CN (2013) Chemical taphonomy of biomineralized tissues. Palaeontology 56:475–486. doi:10.1111/pala.12041

    Article  Google Scholar 

  54. Miller LM, Vairavamurthy V, Chance MR, Mendelsohn R, Paschalis EP, Betts F, Boskey AL (2001) In situ analysis of mineral content and crystallinity in bone using infrared micro-spectroscopy of the v(4) PO43-vibration. Biochimica et Biophysica Acta (BBA)-General Subjects 1527:11–19

  55. Smith CI, Chamberlain AT, Riley MS, Stringer C, Collins MJ (2003) The thermal history of human fossils and the likelihood of successful DNA amplification. J Hum Evol 45:203–217. doi:10.1016/S0047-2484(03)00106-4

    Article  Google Scholar 

  56. Legros R, Balmain N, Bonel G (1986) Structure and Composition of the Mineral Phase of Periosteal Bone. J Chem Res-S 8–9

  57. Cazalbou S (2000) Échanges cationiques impliquant des apatites nanocristallines analogues au minéral osseux. Thèse de doctorat, Institut national polytechnique

  58. Drouet C, Carayon M-T, Combes C, Rey C (2008) Surface enrichment of biomimetic apatites with biologically-active ions Mg2+ and Sr2+: a preamble to the activation of bone repair materials. Mater Sci Eng C-Biomimetic Supramol Syst 28:1544–1550. doi:10.1016/j.msec.2008.04.011

    Article  CAS  Google Scholar 

  59. Lefevre R, Frank RM, Voegel JC (1975) The study of human dentine with secondary ion microscopy and electron diffraction. Calcif Tissue Res 19:251–261

    Article  Google Scholar 

  60. Keyser-Tracqui C, Crubezy E, Ludes B (2003) Nuclear and mitochondrial DNA analysis of a 2,000-year-old necropolis in the Egyin Gol Valley of Mongolia. Am J Hum Genet 73:247–260

    Article  CAS  Google Scholar 

  61. Mendisco F (2011) Apports de la paléogénétique à l’histoire du peuplement précolombien des Andes méridionales (Vème–XVème siècles). Université de Toulouse, Université Toulouse III-Paul Sabatier

  62. Scherrer P (1981) Estimation of the size and internal structure of colloidal particles by means of Rontgen rays. Nachr. Ges. Wiss., Gotengen 2:96–100

  63. Paschalis EP et al. (1997) FTIR microspectroscopic analysis of normal human cortical and tribecular bone. Calcif. Tis. Int. 61(6):480–486

  64. Elliott JC (1994) Structure and chemistry of the apatites and other calcium orthophosphtes. Elsevier Science BV, Amsterdam

  65. Drouet C (2013) Apatite formation: why it may not work as planned, and how to conclusively identify apatite compounds. BioMed Res. Ins., p. 490946. Doi:10.1155/2013/490946

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Acknowledgments

This research was supported by the Institute of Ecology and Environment (INEE) and the Institute of Chemistry (INC) of the French National Center for Scientific Research (CNRS).

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Authors and Affiliations

  1. CIRIMAT Carnot Institute  –  Phosphates, Pharmacotechnics, Biomaterials, University of Toulouse, CNRS/INPT/UPS, ENSIACET, 4 allée Emile Monso, 31030, Toulouse Cedex 4, France

    A. Grunenwald, A. M. Sautereau & C. Drouet

  2. Institute of Legal Medicine, AMIS Laboratory, CNRS UMR 5288, University of Strasbourg, 11 rue Humann, 67085, Strasbourg Cedex, France

    A. Grunenwald & C. Keyser

  3. Molecular Anthropology and Image Synthesis Laboratory (AMIS), CNRS UMR 5288, University of Toulouse, 37 allées Jules Guesde, 31000, Toulouse, France

    E. Crubézy

  4. Institute of Legal Medicine, Paris Descartes Medicine Faculty, Paris Descartes University, 15 Rue de l’Ecole de Médecine, 75006, Paris, France

    B. Ludes

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  1. A. Grunenwald
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  2. C. Keyser
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  3. A. M. Sautereau
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Correspondence to C. Drouet.

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Grunenwald, A., Keyser, C., Sautereau, A.M. et al. Novel contribution on the diagenetic physicochemical features of bone and teeth minerals, as substrates for ancient DNA typing. Anal Bioanal Chem 406, 4691–4704 (2014). https://doi.org/10.1007/s00216-014-7863-z

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