PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Pinto, Ameet J ^a   Raskin, Lutgarde ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRIMER DNA; RNA 16S;

ACCURACY; ALPHA DIVERSITY; ANALYTIC METHOD; ANALYTICAL ERROR; ANALYTICAL PARAMETERS; ARTICLE; ARTIFACT; BETA DIVERSITY; CHAO1 ESTIMATOR; CHIMERIC POLYMERASE CHAIN REACTION ARTIFACT; COMMUNITY STRUCTURE; CONTROLLED STUDY; DATA PROCESSING; DNA BASE COMPOSITION; GENE SEQUENCE; GENETIC VARIABILITY; INVERSE SIMPSON INDEX; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NON PARAMETRIC SHANNON INDEX; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERATIONAL TAXONOMIC UNIT ABUNDANCE DISTRIBUTION; POLYMERASE CHAIN REACTION BIAS; POPULATION ABUNDANCE; PYROSEQUENCING; RANK ABUNDANCE DISTRIBUTION; RNA GENE; SEQUENCING DEPTH; SEQUENCING ERROR; SPECIES RICHNESS; TAXA DETECTION FREQUENCY;

ARCHAEA; BACTERIA; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DNA PRIMERS; GENES, ARCHAEAL; GENES, BACTERIAL; GENETIC TECHNIQUES; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84865060813     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043093     Document Type: Article

References (61)

1. Huse S, Huber J, Morrison H, Sogin M, Welch D, ((2007)) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:: R143.1-R143.9.
2. Metzker ML, ((2010)) Sequencing technologies-the next generation. Nat Rev Genet 11:: 31-46.
3. Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, et al. ((2011)) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:: 908-917.
4. Galand PE, Casamayor EO, Kirchman DL, Potvin M, Lovejoy C, ((2009)) Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J 3:: 860-869.
5. Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, et al. ((2010)) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:: 829-838.
6. Werner JJ, Knights D, Garcia ML, Scalfone NB, Smith S, et al. ((2011)) Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc Nat Acad Sci 108:: 4158-4163.
7. Hong PY, Hwang C, Ling F, Andersen GL, LeChevallier MW, et al. ((2010)) Pyrosequencing analysis of bacterial biofilm communities in water meters of a drinking water distribution system. Appl Environ Microbiol 76:: 5631-5635.
8. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, et al. ((2006)) Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Nat Acad Sci U S 103:: 12115-12120.
9. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, et al. ((2011)) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Nat Acad Sci U S 108:: 4516-4522.
10. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. doi:10.1038/ismej.2012.8.
11. Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD, ((2011)) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end Illumina reads. Appl Environ Microbiol 77:: 3846-3852.
12. Hamady M, Walker J, Harris J, Gold N, Knight R, ((2008)) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:: 235-237.
13. Schloss PD, Gevens D, Westcott SL, ((2011)) Reducing the effects of PCR and sequencing artifacts on 16S rRNA-based studies. PLoS One 6(12):: e27310.
14. Youssef N, Sheik C, Krumholz L, Najar F, Roe B, et al. ((2009)) Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 75:: 5227-5236.
15. Kim M, Morrison M, Yu Z, ((2010)) Evaluation of different partial 16S rRNA gene sequence regions for phylogenetic analysis of microbiomes. J Microbiol Methods 84:: 81-87.
16. Schloss PD, ((2010)) The Effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6:: e1000844.
17. Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, et al. ((2010)) Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4:: 642-647.
18. Quince C, Lanzen A, Curtis T, Davenport R, Hall N, et al. ((2009)) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:: 639-641.
19. Reeder J, Knight R, ((2010)) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nature Methods 7:: 668-669.
20. Huse SM, Welch DM, Morrison HG, Sogin ML, ((2010)) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:: 1889-1898.
21. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R, ((2011)) UCHIME improves sensitivity and speed of chimera detection. Bioinform 27:: 2194-2200.
22. Quince C, Lanzen A, Davenport R, Turnbaugh P, ((2011)) Removing Noise From Pyrosequenced Amplicons. BMC Bioinform 12:: 38-56.
23. Haas B, Gevers D, Earl A, Feldgarden M, Ward D, et al. ((2011)) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:: 494-504.
24. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P, ((2010)) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:: 118-123.
25. Hong S, Bunge J, Leslin C, Jeon S, Epstein SS, ((2009)) Polymerase chain reaction primers miss half of rRNA microbial diversity. ISME J 3:: 1365-1373.
26. Polz M, Cavanaugh C, ((1998)) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64:: 3724-3730.
27. Suzuki MT, Giovannoni SJ, ((1996)) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62:: 625-630.
28. Roh SW, Kim KH, Nam YD, Chang HW, Park EJ, et al. ((2010)) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J 4:: 1-16.
29. Berry D, Ben Mahfoudh K, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol: AEM.05220-05211.
30. Wu DY, Ugozzoli L, Pal BK, Qian J, Wallace B, ((1991)) The effect of temperature and oligonucleotide primer length on the specificity and efficiency of amplification by the polymerase chain reaction. DNA Cell Biol 10:: 233-238.
31. Reysenbach AL, Giver LJ, Wickham GS, Pace NR, ((1992)) Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58:: 3417-3418.
32. Benita Y, Oosting RS, Lok MC, Wise MJ, Humphery-Smith I, ((2003)) Regionalized GC content of template DNA as a predictor of PCR success. Nucl Acids Res 31:: e99-e106.
33. Ishii K, Fukui M, ((2001)) Optimization of annealing temperature to reduce bias caused by a primer mismatch in multitemplate PCR. Appl Environ Microbiol 67:: 3753-3755.
34. Ahn J, Yang L, Paster BJ, Ganly I, Morris L, et al. ((2011)) Oral microbiome profiles: 16S rRNA pyrosequencing and microarray assay comparison. PLoS One 6:: e22788.
35. Herlemann DPR, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, et al. ((2011)) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:: 1571-1579.
36. Baker G, Smith J, Cowan D, ((2003)) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:: 541-555.
37. Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Chichester, England: John Wiley & Sons. 205-248.
38. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach A-L, ((1999)) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65:: 4375-4384.
39. Auchtung TA, Takacs-Vesbach CD, Cavanaugh CM, ((2006)) 16S rRNA phylogenetic investigation of the candidate division "Korarchaeota". Appl Environ Microbiol 72:: 5077-5082.
40. Collingro A, Toenshoff ER, Taylor MW, Fritsche TR, Wagner M, et al. ((2005)) 'Candidatus Protochlamydia amoebophila', an endosymbiont of Acanthamoeba spp. International J Syst Evol Microbiol 55:: 1863-1866.
41. Berry D, Xi C, Raskin L, ((2006)) Microbial ecology of drinking water distribution systems. Curr Opin Biotech 17:: 297-302.
42. Shinoda N, Yoshida T, Kusama T, Takagi M, Hayakawa T, et al. ((2009)) High GC contents of primer 5′ - enf increases reaction efficiency in polymerase chain reaction. Nucleos Nucleot Nucl Acids 28:: 324-330.
43. Mamedov TG, Pienaar E, Whitney SE, TerMaat JR, Carvill G, et al. ((2008)) A fundamental study of the PCR amplification of GC-rich DNA templates. Comput Biol Chem 32:: 452-457.
44. Pinard R, de Winter A, Sarkis G, Gerstein M, Tartaro K, et al. ((2006)) Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genom 7:: 216-237.
45. Dohm JC, Lottaz C, Borodina T, Himmelbauer H, ((2008)) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucl Acids Res 36:: e105-e115.
46. Jaenicke S, Ander C, Bekel T, Bisdorf R, Dröge M, et al. ((2011)) Comparative and joint analysis of two metagenomic datasets from a biogas fermenter obtained by 454-pyrosequencing. PLoS One 6:: e14519-e14534.
47. Lozupone C, Hamady M, Knight R, ((2006)) UniFrac- An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:: 371-385.
48. Feinstein L, Sul W, Blackwood C, ((2009)) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:: 5428-5433.
49. Farrelly V, Rainey FA, Stackebrandt E, ((1996)) Effect of genome size and rrn gene copy numbers of PCR amplification products of 16S rRNA genes from mixed bacterial species. Cell Mol Life Sci 52:: 294-295.
50. Sloan WT, Quince C, Curtis TP (2008) The uncountables. In: Zengler K, editor. Accessing uncultivated microorganisms: From the environment to the organisms and genomes and back. Washington, DC: ASM press.
51. Zhou J, Wu L, Deng Y, Zhi X, Jiang Y-H, et al. ((2011)) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5:: 1303-1313.
52. Muyzer G, ((1999)) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2:: 317-322.
53. Liu W, Marsh T, Cheng H, Forney L, ((1997)) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:: 4516-4522.
54. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M, ((1999)) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:: 434-444.
55. Cole J, Wang Q, Cardenas E, Fish J, Chai B, et al. ((2009)) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 37:: D141-145.
56. Pinto A, Xi C, Raskin L (2012) Bacterial community structure in the drinking water microbiome is governed by filtration processes. Environ Sci Technol. doi: 10.1021/es302042t.
57. Thompson JR, Marcelino LA, Polz MF, ((2002)) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucl Acids Res 30:: 2083-2088.
58. Roche (2011) Amplicon sequencing with various emPCR amplification conditions: TCB No: 2011-001.
59. Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, et al. ((2009)) Introducing mothur: Open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbio 75:: 7537-7541.
60. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. ((2007)) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl Acids Res 35:: 7188-7196.
61. Felsenstein J, ((1989)) PHYLIP - Phylogeny inference package (Version 3.2). Cladistics 5:: 164-166.