Pyrosequencing as a tool for better understanding of human microbiomes

Journal of Oral Microbiology

Volumn 4, Issue 2012, 2012, Pages

  Siqueira, José F ^a   Fouad, Ashraf F ^b   Rôças, Isabela N ^a  

^a Department of Endodontics and Molecular Microbiology Laboratory   (Brazil)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Human microbiome; Next generation DNA sequencing; Oral microbiome; Pyrosequencing

Indexed keywords

CIPROFLOXACIN; CLARITHROMYCIN; METRONIDAZOLE; RNA 16S;

ACTINOBACTERIA; ANALYZER; ANTIBIOTIC THERAPY; AUTISM; BACTEROIDETES; BIOFILM; BIOINFORMATICS; BRAIN ABSCESS; CHRONIC WOUND; COMMUNITY STRUCTURE; DATA ANALYSIS; DENTAL CARIES; DENTAL TECHNOLOGY; DIABETES MELLITUS; DIABETIC FOOT; DIAGNOSTIC ACCURACY; DIARRHEA; DISEASE ACTIVITY; DNA DETERMINATION; DNA LIBRARY; DNA PURIFICATION; DNA SEQUENCE; DNA SYNTHESIS; DNA TEMPLATE; ENTEROBACTER; FIRMICUTES; FUSOBACTERIA; GENE TARGETING; GENETIC ANALYSIS; GENETIC PARAMETERS; GENETIC PROCEDURES; HALITOSIS; HEALTH; HIGH THROUGHPUT SEQUENCING; HUMAN; INTESTINE FLORA; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIAL IDENTIFICATION; MICROBIOME; MOUTH CAVITY; MOUTH DISEASE; MOUTH FLORA; MOUTH HYGIENE; MOUTH INFECTION; NEWBORN SEPSIS; NEXT GENERATION SEQUENCING; NONHUMAN; OBESITY; PATHOGENICITY; PERIIMPLANTITIS; PERIODONTAL DISEASE; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PREVENTIVE DENTISTRY; PROTEOBACTERIA; PROTEUS; PSEUDOMONAS; PYROSEQUENCING; REVIEW; SANGER SEQUENCING APPROACH; SERRATIA; SKIN; SPIROCHETE; STAPHYLOCOCCUS; STENOTROPHOMONAS; TOOTH INFECTION; TREATMENT RESPONSE; VAGINA; VAGINITIS;

EID: 84863000773     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.3402/jom.v4i0.10743     Document Type: Review

References (101)

1. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, et al. Bacterial diversity in human subgingival plaque. J Bacteriol 2001; 183: 3770-83.
2. Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ, Dewhirst FE, et al. Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 2003; 41: 558-63.
3. Munson MA, Banerjee A, Watson TF, Wade WG. Molecular analysis of the microflora associated with dental caries. J Clin Microbiol 2004; 42: 3023-9.
4. Munson MA, Pitt-Ford T, Chong B, Weightman A, WadeWG. Molecular and cultural analysis of the microflora associated with endodontic infections. J Dent Res 2002; 81: 761-6.
5. Kumar PS, Griffen AL, Moeschberger ML, Leys EJ. Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J Clin Microbiol 2005; 43: 3944-55.
6. Sakamoto M, Rôças IN, Siqueira JF, Jr, Benno Y. Molecular analysis of bacteria in asymptomatic and symptomatic endodontic infections. Oral Microbiol Immunol 2006; 21: 112-22.
7. Corby PM, Lyons-Weiler J, Bretz WA, Hart TC, Aas JA, Boumenna T, et al. Microbial risk indicators of early childhood caries. J Clin Microbiol 2005; 43: 5753-9.
8. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ. New bacterial species associated with chronic periodontitis. J Dent Res 2003; 82: 338-44.
9. Siqueira JF, Jr, Rôças IN. The microbiota of acute apical abscesses. J Dent Res 2009; 88: 61-5.
10. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored rare biosphere. Proc Natl Acad Sci U S A 2006; 103: 12115-20.
11. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 2010; 12: 118-23.
12. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005; 43: 5721-32.
13. Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, et al. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J 2010; 4: 962-74.
14. Kanasi E, Dewhirst FE, Chalmers NI, Kent R, Jr, Moore A, Hughes CV, et al. Clonal analysis of the microbiota of severe early childhood caries. Caries Res 2010; 44: 485-97.
15. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, et al. Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 2008; 46: 1407-17.
16. Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, et al. Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 2002; 40: 1001-9.
17. Sakamoto M, Siqueira JF, Jr, Rôças IN, Benno Y. Molecular analysis of the root canal microbiota associated with endodontic treatment failures. Oral Microbiol Immunol 2008; 23: 275-81.
18. Handal T, Caugant DA, Olsen I, Sunde PT. Bacterial diversity in persistent periapical lesions on root-filled teeth. J Oral Microbiol 2009; 1: 1946.
19. Ribeiro AC, Matarazzo F, Faveri M, Zezell DM, Mayer MP. Exploring bacterial diversity of endodontic microbiota by cloning and sequencing 16S rRNA. J Endod 2011; 37: 922-6.
20. Saito D, de Toledo Leonardo R, Rodrigues JLM, Tsai SM, Hofling JF, Gonçalves RB. Identification of bacteria in endodontic infections by sequence analysis of 16S rDNA clone libraries. J Med Microbiol 2006; 55: 101-7.
21. Faveri M, Mayer MP, Feres M, de Figueiredo LC, Dewhirst FE, Paster BJ. Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol 2008; 23: 112-8.
22. Paster BJ, Russell MK, Alpagot T, Lee AM, Boches SK, Galvin JL, et al. Bacterial diversity in necrotizing ulcerative periodontitis in HIV-positive subjects. Ann Periodontol 2002; 7: 8-16.
23. De Lillo A, Ashley FP, Palmer RM, Munson MA, Kyriacou L, Weightman AJ, et al. Novel subgingival bacterial phylotypes detected using multiple universal polymerase chain reaction primer sets. Oral Microbiol Immunol 2006; 21: 61-8.
24. Koyanagi T, Sakamoto M, Takeuchi Y, Ohkuma M, Izumi Y. Analysis of microbiota associated with peri-implantitis using 16S rRNA gene clone library. J Oral Microbiol 2010; 2: 5104.
25. Haraszthy VI, Zambon JJ, Sreenivasan PK, Zambon MM, Gerber D, Rego R, et al. Identification of oral bacterial species associated with halitosis. J Am Dent Assoc 2007; 138: 1113-20.
26. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, et al. The human oral microbiome. J Bacteriol 2010; 192: 5002-17.
27. Paster BJ, Olsen I, Aas JA, Dewhirst FE. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 2006; 42: 80-7.
28. Olsen I, Preza D, Aas JA, Paster BJ. Cultivated and notyet-cultivated bacteria in oral biofilms. Microb Ecol Health Dis 2009; 21: 65-71.
29. Voelkerding KV, Dames SA, Durtschi JD. Next-generation sequencing: from basic research to diagnostics. Clin Chem 2009; 55: 641-58.
30. Higuchi R, Gyllensten U, Persing DH. Next-generation DNA sequencing and microbiology. In: Persing DH, Tenover FC, Tang Y-W, Nolte FS, Hayden RT, van Belkum A, eds. Molecular microbiology. diagnostic, principles and practice. Washington, DC: ASM Press; 2011, p. 301-12.
31. Mardis ER. Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 2008; 9: 387-402.
32. Rothberg JM, Leamon JH. The development and impact of 454 sequencing. Nat Biotechnol 2008; 26: 1117-24.
33. Varshney RK, Nayak SN, May GD, Jackson SA. Nextgeneration sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 2009; 27: 522-30.
34. Shendure J, Ji H. Next-generation DNA sequencing. Nat Biotechnol 2008; 26: 1135-45.
35. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, et al. Realtime DNA sequencing from single polymerase molecules. Science 2009; 323: 133-8.
36. Metzker ML. Sequencing technologies-the next generation. Nat Rev Genet 2010; 11: 31-46.
37. Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, et al. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 2010; 4: 642-7.
38. Tringe SG, Hugenholtz P. A renaissance for the pioneering 16S rRNA gene. Curr Opin Microbiol 2008; 11: 442-6.
39. Parameswaran P, Jalili R, Tao L, Shokralla S, Gharizadeh B, Ronaghi M, et al. A pyrosequencing-tailored nucleotide barcode design unveils opportunities for large-scale sample multiplexing. Nucleic Acids Res 2007; 35: e130.
40. Kuczynski J, Costello EK, Nemergut DR, Zaneveld J, Lauber CL, Knights D, et al. Direct sequencing of the human microbiome readily reveals community differences. Genome Biol 2010; 11: 210.
41. Lemos LN, Fulthorpe RR, Triplett EW, Roesch LF. Rethinking microbial diversity analysis in the high throughput sequencing era. J Microbiol Methods 2011; 86: 42-51.
42. Siqueira JF, Jr, Rôças IN. Molecular analysis of endodontic infections. In: Fouad AF, ed. Endodontic microbiology. Ames, Iowa: Wiley-Blackwell; 2009, p. 68-107.
43. Reeder J, Knight R. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 2010; 7: 668-9.
44. Clarridge JE. 3rd. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 2004; 17: 840-62.
45. Huse SM, Dethlefsen L, Huber JA, Mark Welch D, Relman DA, Sogin ML. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 2008; 4: e1000255.
46. Nasidze I, Quinque D, Li J, Li M, Tang K, Stoneking M. Comparative analysis of human saliva microbiome diversity by barcoded pyrosequencing and cloning approaches. Anal Biochem 2009; 391: 64-8.
47. Wu GD, Lewis JD, Hoffmann C, Chen YY, Knight R, Bittinger K, et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol 2010; 10: 206.
48. Schloss PD, Handelsman J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 2005; 71: 1501-6.
49. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy core microbiome of oral microbial communities. BMC Microbiol 2009; 9: 259.
50. Lazarevic V, Whiteson K, Huse S, Hernandez D, Farinelli L, Osteras M, et al. Metagenomic study of the oral microbiota by Illumina high-throughput sequencing. J Microbiol Methods 2009; 79: 266-71.
51. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, et al. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 2005; 33: D294-6.
52. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72: 5069-72.
53. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, et al. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008; 9: 386.
54. Griffen AL, Beall CJ, Firestone ND, Gross EL, Difranco JM, Hardman JH, et al. CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS One 2011; 6: e19051.
55. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009; 326: 1694-7.
56. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71: 8228-35.
57. Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, Knight R. Forensic identification using skin bacterial communities. Proc Natl Acad Sci U S A 2010; 107: 6477-81.
58. Relman DA. Microbial genomics and infectious diseases. N Engl J Med 2011; 365: 347-57.
59. Xu J. Metagenomics and Ecosystems Biology: conceptual frameworks, tools and methods. In: Macro D, ed. Metagenomics. Norfolk, UK: Caister Academic Press; 2010, p. 1-15.
60. Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM, et al. Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 2006; 7: 57.
61. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 2008; 3: e2836.
62. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107: 11971-5.
63. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A 2011; 108(Suppl 1): 4554-61.
64. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 2007; 449: 804-10.
65. Gonzalez A, Clemente JC, Shade A, Metcalf JL, Song S, Prithiviraj B, et al. Our microbial selves: what ecology can teach us. EMBO Rep 2011; 12: 775-84.
66. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 1998; 95: 6578-83.
67. Egert M, de Graaf AA, Smidt H, de Vos WM, Venema K. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol 2006; 14: 86-91.
68. Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, Niazi F, et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci U S A 2010; 107: 7503-8.
69. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010; 107: 14691-6.
70. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444: 1022-3.
71. Armougom F, Raoult D. Use of pyrosequencing and DNA barcodes to monitor variations in Firmicutes and Bacteroidetes communities in the gut microbiota of obese humans. BMC Genomics 2008; 9: 576.
72. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 2009; 106: 2365-70.
73. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-4.
74. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 2010; 5: e9085.
75. Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010; 16: 444-53.
76. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6: e280.
77. Jakobsson HE, Jernberg C, Andersson AF, Sjolund-Karlsson M, Jansson JK, Engstrand L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 2010; 5: e9836.
78. Fierer N, Hamady M, Lauber CL, Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 2008; 105: 17994-9.
79. Sundquist A, Bigdeli S, Jalili R, Druzin ML, Waller S, Pullen KM, et al. Bacterial flora-typing with targeted, chip-based pyrosequencing. BMC Microbiol 2007; 7: 108.
80. Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y, et al. Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 2010; 11: 488.
81. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011; 108(Suppl 1): 4680-7.
82. Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One 2010; 5: e15216.
83. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 2008; 3: e3326.
84. Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA, et al. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 2008; 8: 43.
85. Wolcott RD, Gontcharova V, Sun Y, Dowd SE. Evaluation of the bacterial diversity among and within individual venous leg ulcers using bacterial tag-encoded FLX and titanium amplicon pyrosequencing and metagenomic approaches. BMC Microbiol 2009; 9: 226.
86. Smith DM, Snow DE, Rees E, Zischkau AM, Hanson JD, Wolcott RD, et al. Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med Genomics 2010; 3: 41.
87. Jordan JA, Butchko AR, Durso MB. Use of pyrosequencing of 16S rRNA fragments to differentiate between bacteria responsible for neonatal sepsis. J Mol Diagn 2005; 7: 105-10.
88. Al Masalma M, Armougom F, Scheld WM, Dufour H, Roche PH, Drancourt M, et al. The expansion of the microbiological spectrum of brain abscesses with use of multiple 16S ribosomal DNA sequencing. Clin Infect Dis 2009; 48: 1169-78.
89. Nakamura S, Maeda N, Miron IM, Yoh M, Izutsu K, Kataoka C, et al. Metagenomic diagnosis of bacterial infections. Emerg Infect Dis 2008; 14: 1784-6.
90. Luna RA, Fasciano LR, Jones SC, Boyanton BL, Jr, Ton TT, Versalovic J. DNA pyrosequencing-based bacterial pathogen identification in a pediatric hospital setting. J Clin Microbiol 2007; 45: 2985-92.
91. Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, et al. Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 2008; 87: 1016-20.
92. Crielaard W, Zaura E, Schuller AA, Huse SM, Montijn RC, Keijser BJ. Exploring the oral microbiota of children at various developmental stages of their dentition in the relation to their oral health. BMC Med Genomics 2011; 4: 22.
93. Lazarevic V, Whiteson K, Hernandez D, Francois P, Schrenzel J. Study of inter- and intra-individual variations in the salivary microbiota. BMC Genomics 2010; 11: 523.
94. Li L, Hsiao WW, Nandakumar R, Barbuto SM, Mongodin EF, Paster BJ, et al. Analyzing endodontic infections by deep coverage pyrosequencing. J Dent Res 2010; 89: 980-4.
95. Siqueira JF, Jr, Alves FR, Rôças IN. Pyrosequencing analysis of the apical root canal microbiota. J Endod 2011; 37: 1499-503.
96. Santos AL, Siqueira JF, Jr, Rôças IN, Jesus EC, Rosado AS, Tiedje JM. Comparing the bacterial diversity of acute and chronic dental root canal infections. PLoS One 2011; 6: e28088.
97. Fouad AF. The microbial challenge to pulp regeneration. Adv Dent Res 2011; 23: 285-9.
98. Ahn J, Yang L, Paster BJ, Ganly I, Morris L, Pei Z, et al. Oral Microbiome Profiles: 16S rRNA pyrosequencing and microarray assay comparison. PLoS ONE 2011; 6: e22788.
99. Koren O, Spor A, Felin J, Fak F, Stombaugh J, Tremaroli V, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 2011; 108(Suppl 1): 4592-8.
100. Xie G, Chain PS, Lo CC, Liu KL, Gans J, Merritt J, et al. Community and gene composition of a human dental plaque microbiota obtained by metagenomic sequencing. Mol Oral Microbiol 2010; 25: 391-405.
101. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 2010; 6: e1000713.