Systematic evaluation of bias in microbial community profiles induced by whole genome amplification

Environmental Microbiology

Volumn 16, Issue 3, 2014, Pages 643-657

  Direito, Susana O L ^a,d   Zaura, Egija ^a   Little, Miranda ^a   Ehrenfreund, Pascale ^b,c   Röling, Wilfred F M ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIAL GENOME; BIODIVERSITY; CHEMISTRY; COMPARATIVE STUDY; DNA BASE COMPOSITION; DNA FRAGMENTATION; DNA SEQUENCE; GENETICS; MOLECULAR WEIGHT; NUCLEIC ACID AMPLIFICATION; POLYMERASE CHAIN REACTION; STANDARD; STATISTICAL BIAS;

BASE COMPOSITION; BIAS (EPIDEMIOLOGY); BIODIVERSITY; DNA FRAGMENTATION; DNA, BACTERIAL; GENOME, BACTERIAL; MOLECULAR WEIGHT; NUCLEIC ACID AMPLIFICATION TECHNIQUES; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 84896690320     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12365     Document Type: Article

References (59)

1. Abulencia, C.B., Wyborski, D.L., Garcia, J.A., Podar, M., Chen, W., Chang, S.H., etal. (2006) Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl Environ Microbiol 72: 3291-3301.
2. Binga, E.K., Lasken, R.S., and Neufeld, J.D. (2008) Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME J 2: 233-241.
3. de Boer, T.E., Taş, N., Braster, M., Temminghoff, E.J.M., Röling, W.F.M., and Roelofs, D. (2011) The influence of long-term copper contaminated agricultural soil at different pH levels on microbial communities and springtail transcriptional regulation. Environ Sci Technol 46: 60-68.
4. Brandt, B.W., Bonder, M.J., Huse, S.M., and Zaura, E. (2012) TaxMan: a server to trim rRNA reference databases and inspect taxonomic coverage. Nucleic Acids Res 40: W82-W87.
5. Bredel, M., Bredel, C., Juric, D., Kim, Y., Vogel, H., Harsh, G.R., etal. (2005) Amplification of whole tumor genomes and gene-by-gene mapping of genomic aberrations from limited sources of fresh-frozen and paraffin-embedded DNA. J Mol Diagn 7: 171-182.
6. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., etal. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
7. Cheung, V.G., and Nelson, S.F. (1996) Whole genome amplification using a degenerate oligonucleotide primer allows hundreds of genotypes to be performed on less than one nanogram of genomic DNA. Proc Natl Acad Sci U S A 93: 14676-14679.
8. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., etal. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
9. d'Abbadie, M., Hofreiter, M., Vaisman, A., Loakes, D., Gasparutto, D., Cadet, J., etal. (2007) Molecular breeding of polymerases for amplification of ancient DNA. Nat Biotechnol 25: 939-943.
10. Dean, F.B., Hosono, S., Fang, L., Wu, X., Faruqi, A.F., Bray-Ward, P., etal. (2002) Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci U S A 99: 5261-5266.
11. Direito, S.O.L., Ehrenfreund, P., Marees, A., Staats, M., Foing, B., and Röling, W.F.M. (2011) A wide variety of putative extremophiles and large beta-diversity at the Mars Desert Research Station (Utah). Int J Astrobiology 10: 191-207.
12. Drees, K.P., Neilson, J.W., Betancourt, J.L., Quade, J., Henderson, D.A., Pryor, B.M., and Maier, R.M. (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol 72: 7902-7908.
13. Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
14. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
15. Ehrenfreund, P., Röling, W.F.M., Thiel, C.S., Quinn, R., Sephton, M.A., Stoker, C., etal. (2011) Astrobiology and habitability studies in preparation for future Mars missions: trends from investigating minerals, organics and biota. Int J Astrobiology 10: 239-253.
16. Felske, A., Rheims, H., Wolterink, A., Stackebrandt, E., and Akkermans, A.D.L. (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143: 2983-2989.
17. Forterre, P. (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci U S A 103: 3669-3674.
18. Garcia-Garcera, M., Gigli, E., Sanchez-Quinto, F., Ramirez, O., Calafell, F., Civit, S., and Lalueza-Fox, C. (2011) Fragmentation of contaminant and endogenous DNA in ancient samples determined by shotgun sequencing; prospects for human palaeogenomics. PLoS ONE 6: e24161.
19. Hammer, Ø., Harper, D.A.T., and Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electron 4: 9.
20. Hawkins, T.L., Detter, J.C., and Richardson, P.M. (2002) Whole genome amplification - applications and advances. Curr Opin Biotechnol 13: 65-67.
21. He, Z.L., Gentry, T.J., Schadt, C.W., Wu, L.Y., Liebich, J., Chong, S.C., etal. (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1: 67-77.
22. Hildebrand, F., Meyer, A., and Eyre-Walker, A. (2010) Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6: e1001107.
23. Huber, H., Hohn, M.J., Rachel, R., Fuchs, T., Wimmer, V.C., and Stetter, K.O. (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417: 63-67.
24. Isenbarger, T.A., Carr, C.E., Johnson, S.S., Finney, M., Church, G.M., Gilbert, W., etal. (2008) The most conserved genome segments for life detection on earth and other planets. Orig Life Evol Biosph 38: 517-533.
25. Itoh, T., Yamanoi, K., Kudo, T., Ohkuma, M., and Takashina, T. (2011) Aciditerrimonas ferrireducens gen. nov., sp. nov., an iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field. Int J Syst Evol Microbiol 61: 1281-1285.
26. Kämpfer, P., Young, C.-C., Arun, A.B., Shen, F.-T., Jäckel, U., Rosselló-Mora, R., etal. (2006) Pseudolabrys taiwanensis gen. nov., sp. nov., an alphaproteobacterium isolated from soil. Int J Syst Evol Microbiol 56: 2469-2472.
27. Kim, K.-H., and Bae, J.-W. (2011) Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77: 7663-7668.
28. Kraneveld, E.A., Buijs, M.J., Bonder, M.J., Visser, M., Keijser, B.J.F., Crielaard, W., and Zaura, E. (2012) The relation between oral Candida load and bacterial microbiome profiles in Dutch older adults. PLoS ONE 7: e42770.
29. Lage, J.M., Leamon, J.H., Pejovic, T., Hamann, S., Lacey, M., Dillon, D., etal. (2003) Whole genome analysis of genetic alterations in small DNA samples using hyperbranched strand displacement amplification and array - CGH. Genome Res 13: 294-307.
30. Lasken, R.S., and Egholm, M. (2003) Whole genome amplification: abundant supplies of DNA from precious samples or clinical specimens. Trends Biotechnol 21: 531-535.
31. Li, Y., Kim, H.-J., Zheng, C., Chow, W.H.A., Lim, J., Keenan, B., etal. (2008) Primase-based whole genome amplification. Nucleic Acids Res 36: e79.
32. Lim, J.H., Baek, S.-H., and Lee, S.-T. (2009) Ferruginibacter alkalilentus gen. nov., sp. nov. and Ferruginibacter lapsinanis sp. nov., novel members of the family 'Chitinophagaceae' in the phylum Bacteroidetes, isolated from freshwater sediment. Int J Syst Evol Microbiol 59: 2394-2399.
33. Marmur, J., and Doty, P. (1959) Heterogeneity in deoxyribonucleic acids. I. Dependence on composition of the configurational stability of deoxyribonucleic acids. Nature 183: 1427-1429.
34. Miller, D.N., Bryant, J.E., Madsen, E.L., and Ghiorse, W.C. (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65: 4715-4724.
35. Montero-Barrientos, M., Rivas, R., Velázquez, E., Monte, E., and Roig, M.G. (2005) Terrabacter terrae sp. nov., a novel actinomycete isolated from soil in Spain. Int J Syst Evol Microbiol 55: 2491-2495.
36. Mullis, K., Faloona, F., Scharf, S., Saiki, R., Horn, G., and Erlich, H. (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol 51 (Part 1): 263-273.
37. Muyzer, G., Dewaal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
38. Pace, N.R., Stahl, D.A., Lane, D.J., and Olsen, G.J. (1986) The analysis of natural microbial-populations by ribosomal-RNA sequences. Adv Microb Ecol 9: 1-55.
39. Pinard, R., de Winter, A., Sarkis, G.J., Gerstein, M.B., Tartaro, K.R., Plant, R.N., etal. (2006) Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genomics 7: 216.
40. Pinheiro, V.B., Taylor, A.I., Cozens, C., Abramov, M., Renders, M., Zhang, S., etal. (2012) Synthetic genetic polymers capable of heredity and evolution. Science 336: 341-344.
41. Pointing, S.B., Chan, Y.K., Lacap, D.C., Lau, M.C.Y., Jurgens, J.A., and Farrell, R.L. (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci U S A 106: 19964-19969.
42. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
43. Pugh, T.J., Delaney, A.D., Farnoud, N., Flibotte, S., Griffith, M., Li, H.I., etal. (2008) Impact of whole genome amplification on analysis of copy number variants. Nucleic Acids Res 36: e80.
44. Raghunathan, A., Ferguson, H.R., Bornarth, C.J., Song, W., Driscoll, M., and Lasken, R.S. (2005) Genomic DNA amplification from a single bacterium. Appl Environ Microbiol 71: 3342-3347.
45. Reeder, J., and Knight, R. (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668-669.
46. Reysenbach, A.L., Giver, L.J., Wickham, G.S., and Pace, N.R. (1992) Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58: 3417-3418.
47. Schaerli, Y., Stein, V., Spiering, M.M., Benkovic, S.J., Abell, C., and Hollfelder, F. (2010) Isothermal DNA amplification using the T4 replisome: circular nicking endonuclease-dependent amplification and primase-based whole-genome amplification. Nucleic Acids Res 38: e201.
48. Schneegurt, M.A., Dore, S.Y., and Kulpa, C.F., Jr (2003) Direct extraction of DNA from soils for studies in microbial ecology. Curr Issues Mol Biol 5: 1-8.
49. Shoaib, M., Baconnais, S., Mechold, U., Le Cam, E., Lipinski, M., and Ogryzko, V. (2008) Multiple displacement amplification for complex mixtures of DNA fragments. BMC Genomics 9: 415.
50. Spits, C., Le Caignec, C., De Rycke, M., Van Haute, L., Van Steirteghem, A., Liebaers, I., and Sermon, K. (2006) Whole-genome multiple displacement amplification from single cells. Nat Protoc 1: 1965-1970.
51. Tate, C.M., Nunez, A.N., Goldstein, C.A., Gomes, I., Robertson, J.M., Kavlick, M.F., and Budowle, B. (2012) Evaluation of circular DNA substrates for whole genome amplification prior to forensic analysis. Forensic Sci Int Genet 6: 185-190.
52. Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., etal. (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37-43.
53. van Verseveld, H.W., and Röling, W.F.M. (2004) Cluster analysis and statistical comparison of molecular community profile data. In Molecular Microbial Ecology Manual, Vol. 2, 2nd edn. Kowalchuk, G.A., de Bruijn, F.J., Head, I.M., Akkermans, A.D.L., and van Elsas, J.D. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 1373-1396.
54. Vincent, M., Xu, Y., and Kong, H. (2004) Helicase-dependent isothermal DNA amplification. EMBO Rep 5: 795-800.
55. Vora, G.J., Meador, C.E., Stenger, D.A., and Andreadis, J.D. (2004) Nucleic acid amplification strategies for DNA microarray-based pathogen detection. Appl Environ Microbiol 70: 3047-3054.
56. Wu, L., Liu, X., Schadt, C.W., and Zhou, J. (2006) Microarray-based analysis of subnanogram quantities of microbial community DNAs by using whole-community genome amplification. Appl Environ Microbiol 72: 4931-4941.
57. Yilmaz, S., Allgaier, M., and Hugenholtz, P. (2010) Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat Methods 7: 943-944.
58. Yoon, M.-H., and Im, W.-T. (2007) Flavisolibacter ginsengiterrae gen. nov., sp. nov. and Flavisolibacter ginsengisoli sp. nov., isolated from ginseng cultivating soil. Int J Syst Evol Microbiol 57: 1834-1839.
59. Zhang, K., Martiny, A.C., Reppas, N.B., Barry, K.W., Malek, J., Chisholm, S.W., and Church, G.M. (2006) Sequencing genomes from single cells by polymerase cloning. Nat Biotechnol 24: 680-686.