Molecular analysis of ancient caries

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1790, 2014, Pages

  Simón, Marc ^a   Montiel, Rafael ^b   Smerling, Andrea ^a   Solórzano, Eduvigis ^a,c   Díaz, Nancy ^a,c   Álvarez Sandoval, Brenda A ^b   Jiménez Marín, Andrea R ^b   Malgosa, Assumpció ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b Laboratorio Nacional de Genómica para la Biodiversidad Unidad de Genómica Avanzada   (Mexico)

^c UNIVERSIDAD DE LOS ANDES   (Venezuela)

Author keywords

Dextranase; Neutral evolution; Positive selection; Streptococcus mutans

Indexed keywords

DEXTRANASE;

AMINO ACID SEQUENCE; DENTAL CARIES; GENETICS; HAPLOTYPE; HISTORY; HUMAN; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; STREPTOCOCCUS MUTANS;

AMINO ACID SEQUENCE; BASE SEQUENCE; DENTAL CARIES; DEXTRANASE; HAPLOTYPES; HISTORY, 15TH CENTURY; HISTORY, 20TH CENTURY; HISTORY, ANCIENT; HISTORY, MEDIEVAL; HUMANS; MOLECULAR SEQUENCE DATA; STREPTOCOCCUS MUTANS;

EID: 84904664746     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0586     Document Type: Article

References (81)

1. Donoghue HD. 2011 Insights gained from palaeomicrobiology into ancient and modern tuberculosis. Clin. Microbiol. Infect. 17, 821-829. (doi: 10. 1111/j. 1469-0691. 2011. 03554. x)
2. Müller R, Roberts CA, Brown TA. 2014 Biomolecular identification of ancient Mycobacterium tuberculosis complex DNA in human remains from Britain and continental Europe. Am. J. Phys. Anthropol. 153, 178-189. (doi: 10. 1002/ajpa. 22417)
3. Bos KIet al. 2011 A draft genome of Yersinia pestisfrom victims of the Black Death. Nature478, 506-510. (doi: 10. 1038/nature10675)
4. Wagner DMet al. 2014 Yersinia pestisand the Plague of Justinian 541-543 AD: a genomic analysis. Lancet Infect Dis. 14, 319-326. (doi: 10. 1016/S1473-3099(13)70323-2)
5. Montiel R, GarcíaC, Cañadas MP, Isidro A, Guijo JM, Malgosa A. 2003 DNA sequences ofMycobacterium leprae recovered from ancient bones. FEMS. Microbiol. Lett. 226, 413-414. (doi: 10. 1016/S0378-1097(03) 00617-7)
6. Suzuki Ket al. 2010 Detection of Mycobacterium leprae DNA from archaeological skeletal remains in Japan using whole genome amplification and polymerase chain reaction. PLoS ONE5, e12422. (doi: 10. 1371/journal. pone. 0012422)
7. Kolman CJ, Centurion-Lara A, Lukehart SA, Owsley DW, Tuross N. 1999 Identification ofTreponema pallidumsubspecies pallidum in a 200-year-old skeletal specimen. J. Infect. Dis. 180, 2060-2063. (doi: 10. 1086/315151)
8. MontielR, Solórzano E, Díaz N, Álvarez-Sandoval BA, González-Ruiz M, Cañadas MP, Simoes N, Isidro A, Malgosa A. 2012 Neonate human remains: a window of opportunity to the molecular study of ancient syphilis. PLoS ONE7, e36371. (doi: 10. 1371/journal. pone. 0036371)
9. Donoghue HD. 2007 Molecular palaeopathology of human infectious disease. InAdvances in human palaeopathology(eds R Pinhasi, S Mays), pp. 147-176. Chichester, UK: Wiley & Sons Ltd.
10. Wilbur AK, Stone AC. Using ancient DNA techniques to study human disease. In The global history of paleopathology: pioneers and prospects(eds JE Buikstra, CA Roberts), pp. 703-717. New York, NY: Oxford University Press.
11. Malgosa A, Montiel R, DíazN, Solórzano E, Smerling A, Isidro A, García C, Simon M. 2005 Ancient DNA: a modern look at the infections of the past. InRecent research developments in microbiology (ed. SG Pandalai), pp. 213-236. Trivandrum, India: Research Signpost.
12. Bäumler AJ, Hargis BM, Tsolis RM. 2000 Tracing the origins of Salmonellaoutbreaks. Science 287, 50-52. (doi: 10. 1126/science. 287. 5450. 50)
13. Szpara ML, Gatherer D, Ochoa A, Greenbaum B, Dolan A, Bowden RJ, Enquist LW, Legendre M, Davison AJ. 2014 Evolution and diversity in human herpes simplex virus genomes. J. Virol. 88, 1209-1227. (doi: 10. 1128/JVI. 01987-13)
14. Liu Wet al. 2010 Origin of the human malaria parasitePlasmodium falciparumin gorillas. Nature 467, 420-425. (doi: 10. 1038/nature09442)
15. Bourhy Het al. 2008 The origin and phylogeography of dog rabies virus. J. Gen. Virol. 89, 2673-2681. (doi: 10. 1099/vir. 0. 2008/ 003913-0)
16. Trueba G, Dunthorn M. 2012 Many neglected diseases may have originated in the Paleolithic or before: new insights from genetics. PLoS Negl. Trop. Dis. 6, e1393. (doi: 10. 1371/journal. pntd. 0001393)
17. Grine FE, Gwinnett AJ, Oaks JH. 1990 Early hominid dental pathology: interproximal caries in 1. 5 million-year-oldParanthropus robustusfrom Swartkrans. Arch. Oral. Biol. 35, 381-386. (doi: 10. 1016/0003-9969(90)90185-D)
18. Pezo-Lanfranco L, Eggers S. 2010 The usefulness of caries frequency, depth, and location in determining cariogenicity and past subsistence: a test on early and later agriculturalists from the Peruvian coast. Am. J. Phys. Anthropol. 143, 75-91. (doi: 10. 1002/ajpa. 21296)
19. Da-Gloria P, Larsen CS. 2014 Oral health of the Paleoamericans of Lagoa Santa, central Brazil. Am. J. Phys. Anthropol. 154, 11-26. (doi: 10. 1002/ ajpa. 22467)
20. Gómez S, Romero A, de Juan J. 2009 'Patrónde subsistencia o modo de producción: caries y desgaste dental en poblaciones del Valle Alto del río Vinalopó(Alicante)'. In Investigaciones históricomédicas sobre salud y enfermedad en el pasado' (eds P Cerda, G Prósper), pp. 659-664. Valencia, Spain: Grupo Paleolab y Sociedad Española de Paleopatologia.
21. Halcrow SE, Harris NJ, Tayles N, Ikehara-Quebral R, Pietrusewsky M. 2013 From the mouths of babes: dental caries in infants and children and the intensification of agriculture in mainland Southeast Asia. Am. J. Phys. Anthropol. 150, 409-420. (doi: 10. 1002/ajpa. 22215)
22. Janket S-J, Baird AE, Chuang S-K, Jones JA. 2003 Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 95, 559-569. (doi: 10. 1067/moe. 2003. 107)
23. Grau AJet al. 2004 Periodontal disease as a risk Factor for ischemic stroke. Stroke 35, 496-501. (doi: 10. 1161/01. STR. 0000110789. 20526. 9D)
24. Jagelaviciene E, Kubilius R. 2006 The relationship between general osteoporosis of the organism and periodontal diseases. Medicina(Kaunas) 42, 613-618.
25. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R, Romero H, Simón-Soro A, Pignatelli M, Mira A. 2012 The oral metagenome in health and disease. ISME J. 6, 46-56. (doi: 10. 1038/ismej. 2011. 85)
26. Forssten SD, Björklund M, Ouwehand AC. 2010 Streptococcus mutans, caries and simulation models. Nutrients2, 290-298. (doi: 10. 3390/nu2030290)
27. Smerling A, Solórzano E, Díaz N, Montiel R, Chimenos E, Malgosa A. 2007 Análisis de ADN de Streptococcus mutansrecuperado en restos antiguos. In Enfermedad, muerte y cultura en las sociedades del pasado. Importancia de la contextualizaciónen los estudios paleopatológicos(eds J Barca Durán, J Jiménez Ávila), pp. 554-566. Fundación Academia Europea de Yuste.
28. Solórzano E, Díaz N, Smerling A, Montiel R, Malgosa A. 2011 Rastreo genético del Streptococcus mutans. Acta Odontológica Venezolana49,2.
29. Yang Z, Wong WSW, Nielsen R. 2005 Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22, 1107-1118. (doi: 10. 1093/molbev/msi097)
30. Zhang J, Nielsen R, Yang Z. 2004 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479. (doi: 10. 1093/ molbev/msi237)
31. Morisaki H, Igarashi T, Yamamoto A, Goto N. 2002 Analysis of dextran-binding domain of the dextranase ofStreptococcus mutans. Lett. Appl. Microbiol. 35, 223-227. (doi: 10. 1046/j. 1472-765X. 2002. 01160. x)
32. Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997 Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (doi: 10. 1093/nar/25. 17. 3389)
33. Nei M, Kumar S. 2000Molecular evolution and phylogenetics. New York, NY: Oxford University Press.
34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011 MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. (doi: 10. 1093/molbev/msr121)
35. Excoffier L, Laval G, Schneider S. 2005 ARLEQUIN v. 3. 0: an integrated software package for population genetics data analysis. Evol. Bioinform. 1, 47-50.
36. Yang Z. 2007 PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. (doi: 10. 1093/molbev/ msm088)
37. Pond SLK, Frost SDW, Muse SV. 2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics21, 676-679. (doi: 10. 1093/ bioinformatics/bti079)
38. Guindon S, Gascuel O. 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. (doi: 10. 1080/10635150390235520)
39. Yang Z. 1998 Likelihood ratio tests for detecting positive selection and application to primate lysozime evolution. Mol. Biol. Evol. 15, 568-573. (doi: 10. 1093/oxfordjournals. molbev. a025957)
40. Nei M, Gojobori T. 1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426.
41. Mann HB, Whitney DR. 1947 On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50-60. (doi: 10. 1214/aoms/1177730491)
42. Kimura M. 1980 A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. (doi: 10. 1007/BF01731581)
43. Preus HR, Marvik OJ, Selvig KA, Bennike P. 2011 Ancient bacterial DNA (aDNA) in dental calculus from archaeological human remains. J. Archaeol. Sci. 8, 1827-1831. (doi: 10. 1016/j. jas. 2011. 03. 020)
44. De la Fuente C, Flores S, Moraga M. 2013 DNA from human ancient bacteria: a novel source of genetic evidence from archaeological dental calculus. Archaeometry55, 767-778. (doi: 10. 1111/j. 1475-4754. 2012. 00707. x)
45. Binladen Jet al. 2006 Assessing the fidelity of ancient DNA sequences amplified from nuclear genes. Genetics172, 733-741. (doi: 10. 1534/ genetics. 105. 049718)
46. Gilbert MTP, Binladen J, Miller W, Wiuf C, Willerslev E, Poinar H, Carlson JE, Leebens-Mack JH, Schuster SC. 2007 Recharacterization of ancient DNA miscoding lesions: insights in the era of sequencing-by-synthesis. Nucleic Acids Res. 35, 1-10. (doi: 10. 1093/nar/gkl483)
47. Montiel R, Francalacci P, Malgosa A. 2007 Ancient DNA and biological anthropology: believers vs. skeptics. In Recent advances in molecular biology and evolution: applications to biological anthropology(eds C Santos, M Lima), pp. 209-250. Kerala, India: Research Signpost.
48. King CE, Debruyne R, Kuch M, Schwarz C, Poinar HN. 2009 A quantitative approach to detect and overcome PCR inhibition in ancient DNA extracts. BioTechniques 47, 941-949. (doi: 10. 2144/000113244)
49. Igarashi T, Yamamoto A, Goto N. 1995 Sequence analysis of theStreptococcus mutans Ingbritt dexA gene encoding extracellular dextranase. Microbiol. Immunol. 39, 853-860. (doi: 10. 1111/j. 1348-0421. 1995. tb03282. x)
50. Maruyama Fet al. 2009 Comparative genomic analyses ofStreptococcus mutans provide insights into chromosomal shuffling and species-specific content. Genomics10, 358. (doi: 10. 1186/1471-2164-10-358)
51. Aikawa Cet al. 2012 Complete genome sequence of the serotype k Streptococcus mutans strain LJ23. J. Bacteriol. 194, 2754-2755. (doi: 10. 1128/JB. 00350-12)
52. Ajdic D et al. 2002 Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc. Natl Acad. Sci. USA99, 14 434-14 439. (doi: 10. 1073/pnas. 172501299)
53. Biswas S, Biswas I. 2012 Complete genome sequence of the Streptococcus mutansGS-5, a serotype c strain. J. Bacteriol. 194, 4787-4788. (doi: 10. 1128/JB. 01106-12)
54. Song L, Sudhakar P, Wang W, Conrads G, Brock A, Sun J, Wagner-Döbler IW, Zeng AP. 2012 A genome-wide study of two-component signal transduction systems in eight newly sequenced mutans streptococci strains. BMC Genomics13, 128. (doi: 10. 1186/1471-2164-13-128)
55. Kim YMet al. 2011 Truncation of N-and C-terminal regions of Streptococcus mutansdextranase enhances catalytic activity. Appl. Microbiol. Biotechnol. 91, 329-339. (doi: 10. 1007/s00253-011-3201-y)
56. Rocha EPC, Smith JM, Hurst LD, Holden MTG, Cooper JE, Smith NH, Feil EJ. 2006 Comparisons of dN/dS are time dependent for closely related bacterial genomes. J. Theor. Biol. 239, 226-235. (doi: 10. 1016/j. jtbi. 2005. 08. 037)
57. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. 2002 Microevolutionary genomics of bacteria. Theor. Popul. Biol. 61, 435-447. (doi: 10. 1006/tpbi. 2002. 1588)
58. Read TDet al. 2002 Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis. Science 296, 2028-2033. (doi: 10. 1126/science. 1071837)
59. Baker L, Brown T, Maiden MC, Drobniewski F. 2004 Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg. Infect. Dis. 10, 1568-1577. (doi: 10. 3201/eid1009. 040046)
60. Gutacker MMet al. 2002 Genome-wide analysis of synonymous single nucleotide polymorphisms in Mycobacterium tuberculosiscomplex organisms: resolution of genetic relationships among closely related microbial strains. Genetics162, 1533-1543.
61. Feil EJet al. 2003 How clonal is Staphylococcus aureus?J. Bacteriol. 185, 3307-3316. (doi: 10. 1128/ JB. 185. 11. 3307-3316. 2003)
62. Anisimova M, Bielawski J, Dunn K, Yang Z. 2007 Phylogenomic analysis of natural selection pressure in Streptococcusgenomes. BMC Evol. Biol. 7, 154. (doi: 10. 1186/1471-2148-7-154)
63. Cornejo OEet al. 2012 Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol. Biol. Evol. 30, 881-893. (doi: 10. 1093/molbev/mss278)
64. Do Tet al. 2010 Generation of diversity in Streptococcus mutansgenes demonstrated by MLST. PLoS ONE5, e9073. (doi: 10. 1371/journal. pone. 0009073)
65. Bernal V, Novellino P, González P, Perez SI. 2007 Role of wild plant foods among Late Holocene hunter-gatherers from Central and North Patagonia (SouthAmerica): an approach from dental evidence. Am. J. Phys Anthropol. 133, 1047-1059. (doi: 10. 1002/ajpa. 20638)
66. Pezo-Lanfranco L. 2010 Reconstrução de padres paleopatológicos dentais em agricultores incipientes e desenvolvidos do litoral dos Andes Centrais. MSc. dissertation. Instituto de Biociências. Universidade de São Paulo, São Paulo.
67. Piperno D. 2011 Northern Peruvian early and middle preceramic agriculture in Central and South American contexts. InFrom foraging to farming in the Andes. New perspectives on food production and social organization(ed. T Dillehay), pp. 274-284. New York, NY: Cambridge University Press.
68. Caselitz P. 1998 Caries ancient plague of humankind. In Dental anthropology. fundamentals, limits, and prospects(eds KWAlt, FW Rösing, M Teschler-Nicola), pp. 203-226. Wien, NY: Springer.
69. Larsen CS, Shavit R, Griffin MC. 1991 Dental caries evidence for dietary change: an archaeological context. In Advances in dental anthropology(eds MA Kelley, CS Larsen), pp. 179-203. New York, NY: Wiley-Liss.
70. White CD. 1994 Dietary dental pathology and cultural change in the Maya. InStrength in diversity (eds DA Herring, L Chan), pp. 279-302. Toronto, Canada: Canadian Scholar's Press.
71. Rodríguez JV. 2003Dientes y diversidad humana, Avances de la antropología dental. Bogotá: Editorial Guadalupe Ltda.
72. Saunders S, De Vito C, Katzenberg A. 1997 Dental caries in nineteenth century Upper Canada. Am. J. Phys. Anthropol. 104, 71-87. (doi: 10. 1002/ (SICI)1096-8644(199709)104: 1,71:: AID-AJPA5. 3. 0. CO; 2-G)
73. Parker M. 2011The sugar barons: family, corruption, empire and war. London, UK: Hutchinson.
74. Lieberman LS. 2003 Dietary, evolutionary and modernizing influences on the prevalence of type 2 diabetes. Annu. Rev. Nutr. 23, 345-377. (doi: 10. 1146/annurev. nutr. 23. 011702. 073212)
75. Shafer WG, Hine MK, Levy BW. 1983A textbook of oral pathology. Philadelphia, PA: Saunders.
76. Brunelle JA, Carlos JP. 1990 Recent trends in dental caries in US children and the effect of water fluoridation. J. Dent. Res. 69, 723-727.
77. Nikiforouk G. 1985Understanding dental caries. New York, NY: Basel Karger.
78. Shaw JH. 1985 Diet and dental health. Am. J. Clin. Nutr. 41, 1117-1131.
79. Haugejorden O. 1996 Using the DMF gender difference to assess the 'major' role of fluoride toothpastes in the caries decline in industrialized countries: a meta-analysis. Community Dent. Oral Epidemiol. 24, 369-375. (doi: 10. 1111/j. 1600-0528. 1996. tb00881. x)
80. Caufield PW. 2009 Tracking human migration patterns through the oral bacterial flora. Clin. Microbiol. Infect. 1(Suppl), 37-39. (doi: 10. 1111/j. 1469-0691. 2008. 02680. x)
81. Moodley Yet al. 2009 The peopling of the Pacific from a bacterial perspective. Science323, 527-530. (doi: 10. 1126/science. 1166083)