Assembling large genomes with single-molecule sequencing and locality-sensitive hashing

Nature Biotechnology

Volumn 33, Issue 6, 2015, Pages 623-630

  Berlin, Konstantin ^a,b,c   Koren, Sergey ^d   Chin, Chen Shan ^e   Drake, James P ^e   Landolin, Jane M ^e   Phillippy, Adam M ^d  

^a Bldg 142   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c Invincea Labs   (United States)

^d National Biodefense Analysis and Countermeasures Center   (United States)

^e PACIFIC BIOSCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; MOLECULES; YEAST;

ARABIDOPSIS THALIANA; DE NOVO ASSEMBLIES; DROSOPHILA MELANOGASTER; HYDATIDIFORM MOLE; LOCALITY SENSITIVE HASHING; MICROBIAL GENOMES; SINGLE MOLECULE; TRANSITION SEQUENCES;

GENES;

CONTIG; HETEROCHROMATIN;

ANALYTIC METHOD; ANIMAL CELL; ARABIDOPSIS THALIANA; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BACTERIAL GENOME; CHROMOSOME ARM; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA MODIFICATION; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI K 12; FUNGAL GENOME; GENE SEQUENCE; GENETIC ALGORITHM; GENOME; GENOME SIZE; HETEROCHROMATIN; HUMAN; HUMAN CELL; HUMAN GENOME; HYDATIDIFORM MOLE; INSECT GENOME; MINHASH ALIGNMENT PROCESS; NONHUMAN; OVERLAPPING GENE; PLANT GENOME; PRIORITY JOURNAL; PROBABILITY; SACCHAROMYCES CEREVISIAE; SENSITIVITY AND SPECIFICITY; SEQUENCE ALIGNMENT; SINGLE MOLECULE REAL TIME SEQUENCING; TELOMERE; TRANSPOSON; ANIMAL; ARABIDOPSIS; CHROMOSOME; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; NUCLEOTIDE SEQUENCE; PROCEDURES;

ARABIDOPSIS THALIANA; DROSOPHILA MELANOGASTER; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

ANIMALS; ARABIDOPSIS; BASE SEQUENCE; CHROMOSOMES; DROSOPHILA MELANOGASTER; GENOME, FUNGAL; GENOME, HUMAN; GENOME, INSECT; GENOME, PLANT; HETEROCHROMATIN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 84930851165     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3238     Document Type: Article

References (68)

1. Miller, J.R., Koren, S. & Sutton, G. Assembly algorithms for next-generation sequencing data. Genomics 95, 315-327 (2010).
2. Nagarajan, N. & Pop, M. Sequence assembly demystified. Nat. Rev. Genet. 14, 157-167 (2013).
3. Denton, J.F. et al. Extensive error in the number of genes inferred from draft genome assemblies. PLOS Comput. Biol. 10, e1003998 (2014).
4. Ukkonen, E. Approximate string-matching with q-grams and maximal matches. Theor. Comput. Sci. 92, 191-211 (1992).
5. Schatz, M.C., Delcher, A.L. & Salzberg, S.L. Assembly of large genomes using second-generation sequencing. Genome Res. 20, 1165-1173 (2010).
6. Clarke, J. et al. Continuous base identification for single-molecule nanopore DNA sequencing. Nat. Nanotechnol. 4, 265-270 (2009).
7. Eid, J. et al. Real-time DNA sequencing from single polymerase molecules. Science 323, 133-138 (2009).
8. Lee, H. et al. Error correction and assembly complexity of single molecule sequencing reads. bioRxiv doi:10.1101/006395 (2014).
9. Quick, J., Quinlan, A.R. & Loman, N.J. A reference bacterial genome dataset generated on the MinION portable single-molecule nanopore sequencer. GigaScience 3, 22 (2014).
10. Koren, S. et al. Reducing assembly complexity of microbial genomes with singlemolecule sequencing. Genome Biol. 14, R101 (2013).
11. Koren, S. & Phillippy, A.M. One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly. Curr. Opin. Microbiol. 23, 110-120 (2015).
12. English, A.C. et al. Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS ONE 7, e47768 (2012).
13. Koren, S. et al. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693-700 (2012).
14. Ribeiro, F.J. et al. Finished bacterial genomes from shotgun sequence data. Genome Res. 22, 2270-2277 (2012).
15. Chin, C.S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563-569 (2013).
16. Ross, M.G. et al. Characterizing and measuring bias in sequence data. Genome Biol. 14, R51 (2013).
17. Chaisson, M.J. et al. Resolving the complexity of the human genome using singlemolecule sequencing. Nature 517, 608-611 (2014).
18. Lam, K.K., Khalak, A. & Tse, D. Near-optimal assembly for shotgun sequencing with noisy reads. BMC Bioinformatics 15 (suppl. 9), S4 (2014).
19. PacBio. Data Release: Preliminary de novo Haploid and Diploid Assemblies of Drosophila melanogaster http://blog.pacificbiosciences.com/2014/01/data-release-preliminary-de-novo.html (2014).
20. Broder, A.Z. On the resemblance and containment of documents. Compression and Complexity of Sequences 1997. Proceedings 21-29 (1997).
21. Broder, A.Z. Identifying and filtering near-duplicate documents. Combinatorial pattern matching 1-10 (2000).
22. Chum, O., Philbin, J. & Zisserman, A. Near duplicate image detection: min-Hash and tf-idf weighting. British Machine Vision Conference 810, 812-815 (2008).
23. Buhler, J. Efficient large-scale sequence comparison by locality-sensitive hashing. Bioinformatics 17, 419-428 (2001).
24. Narayanan, M. & Karp, R.M. Gapped local similarity search with provable guarantees. Algorithms Bioinform. 3240, 74-86 (2004).
25. Yang, X. et al. De novo assembly of highly diverse viral populations. BMC Genomics 13, 475 (2012).
26. Rasheed, Z. & Rangwala, H. Mc-minh: Metagenome clustering using minwise based hashing. SIAM International Conference in Data Mining (2013).
27. Roberts, M., Hayes, W., Hunt, B.R., Mount, S.M. & Yorke, J.A. Reducing storage requirements for biological sequence comparison. Bioinformatics 20, 3363-3369 (2004).
28. Chaisson, M.J. & Tesler, G. Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics 13, 238 (2012).
29. Myers, G. Efficient local alignment discovery amongst noisy long reads. Algorithms Bioinform. 8701, 52-67 (2014).
30. Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997 (2013).
31. Zaharia, M. et al. Faster and more accurate sequence alignment with SNAP. arXiv preprint arXiv:1111.5572 (2011).
32. Weese, D., Holtgrewe, M. & Reinert, K. RazerS 3: faster, fully sensitive read mapping. Bioinformatics 28, 2592-2599 (2012).
33. Myers, E.W. AnO(ND) difference algorithm and its variations. Algorithmica 1, 251-266 (1986).
34. Myers, E.W.A. Whole-genome assembly of Drosophila. Science 287, 2196-2204 (2000).
35. Kim, K.E. et al. Long-read, whole-genome shotgun sequence data for five model organisms. Scientific Data 1, 140045 (2014).
36. Ralser, M. et al. The Saccharomyces cerevisiae W303-K6001 cross-platform genome sequence: insights into ancestry and physiology of a laboratory mutt. Open Biol. 2, 120093 (2012).
37. Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815 (2000).
38. Hoskins, R.A. et al. Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316, 1625-1628 (2007).
39. Weber, J.L. & Myers, E.W. Human whole-genome shotgun sequencing. Genome Res. 7, 401-409 (1997).
40. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
41. Venter, J.C. et al. The sequence of the human genome. Science 291, 1304-1351 (2001).
42. Steinberg, K.M. et al. Single haplotype assembly of the human genome from a hydatidiform mole. Genome Res. 24, 2066-2076 (2014).
43. The MHC Sequencing Consortium. Complete sequence and gene map of a human major histocompatibility complex. Nature 401, 921-923 (1999).
44. Huddleston, J. et al. Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res. 24, 688-696 (2014).
45. Phillippy, A.M., Schatz, M.C. & Pop, M. Genome assembly forensics: finding the elusive mis-assembly. Genome Biol. 9, R55 (2008).
46. Adams, M.D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185-2195 (2000).
47. Salzberg, S.L. et al. GAGE: a critical evaluation of genome assemblies and assembly algorithms. Genome Res. 22, 557-567 (2012).
48. Ewing, B., Hillier, L., Wendl, M.C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175-185 (1998).
49. Kaminker, J.S. et al. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 3, research0084 (2002).
50. McCoy, R.C. et al. Illumina TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements. PLoS ONE 9, e106689 (2014).
51. Mewes, H.W. et al. Overview of the yeast genome. Nature 387, 7-65 (1997).
52. Blasco, M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6, 611-622 (2005).
53. George, J.A., DeBaryshe, P.G., Traverse, K.L., Celniker, S.E. & Pardue, M.L. Genomic organization of the Drosophila telomere retrotransposable elements. Genome Res. 16, 1231-1240 (2006).
54. Jurka, J. et al. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462-467 (2005).
55. Koch, P., Platzer, M. & Downie, B.R. RepARK-de novo creation of repeat libraries from whole-genome NGS reads. Nucleic Acids Res. 42, e80 (2014).
56. Schwartz, D.C. et al. Ordered restriction maps of Saccharomyces cerevisiae chromosomes constructed by optical mapping. Science 262, 110-114 (1993).
57. Burton, J.N. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119-1125 (2013).
58. Kaplan, N. & Dekker, J. High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat. Biotechnol. 31, 1143-1147 (2013).
59. Böhringer, S., Gödde, R., Böhringer, D., Schulte, T. & Epplen, J.T. A software package for drawing ideograms automatically. Online J. Bioinform. 1, 51-61 (2002).
60. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477 (2012).
61. PacBio DevNet. Pacific Biosciences DevNet Datasets https://github.com/PacificBiosciences/DevNet/wiki/Datasets (2014).
62. Smith, T.F. & Waterman, M.S. Identification of common molecular subsequences. J. Mol. Biol. 147, 195-197 (1981).
63. Rasmussen, K.R., Stoye, J. & Myers, E.W. Efficient q-gram filters for finding all epsilon-matches over a given length. J. Comput. Biol. 13, 296-308 (2006).
64. Manber, U. & Myers, G. Suffix arrays: a new method for on-line string searches. SIAM J. Comput. 22.5, 935-348 (1993).
65. Cheng, R.C.H. & Amin, N.A.K. Estimating parameters in continuous univariate distributions with a shifted origin. J. R. Stat. Soc., B 45, 394-403 (1983).
66. Lee, C., Grasso, C. & Sharlow, M.F. Multiple sequence alignment using partial order graphs. Bioinformatics 18, 452-464 (2002).
67. Anson, E.L. & Myers, E.W. ReAligner: a program for refining DNA sequence multi-alignments. J. Comput. Biol. 4, 369-383 (1997).
68. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).