Whole-genome shotgun optical mapping of Deinococcus radiodurans

Science

Volumn 285, Issue 5433, 1999, Pages 1558-1562

  Lin, Jieyi ^a,f   Qi, Rong ^a   Aston, Christopher ^a,g   Jing, Junping ^a,h   Anantharaman, Thomas S ^b   Mishra, Bud ^b   White, Owen ^c   Daly, Michael J ^d   Minton, Kenneth W ^d   Venter, J Craig ^e   Schwartz, David C ^a,b,i  

^a NEW YORK UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c J CRAIG VENTER INSTITUTE   (United States)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^e CELERA GENOMICS   (United States)

^f GENOME THERAPEUTICS CORPORATION   (United States)

^g PFIZER INC   (United States)

^h GLAXOSMITHKLINE   (United Kingdom)

ⁱ UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA FRAGMENT;

ARTICLE; CHROMOSOME; DEINOCOCCUS RADIODURANS; DNA REPAIR; EPISOME; GAMMA IRRADIATION; GENE MAPPING; GENOTYPE; NONHUMAN; NUCLEOTIDE REPEAT; POLARIMETRY; PRIORITY JOURNAL; RADIOSENSITIVITY;

CHROMOSOMES, BACTERIAL; CONTIG MAPPING; DNA DAMAGE; DNA REPAIR; DNA, BACTERIAL; DNA, CIRCULAR; GAMMA RAYS; GENOME, BACTERIAL; GRAM-POSITIVE COCCI; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; NUCLEIC ACID CONFORMATION; PLASMIDS; RADIATION TOLERANCE; RECOMBINATION, GENETIC; RESTRICTION MAPPING;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS; PROKARYOTA;

EID: 0033520409     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5433.1558     Document Type: Article

References (46)

1. D. C. Schwartz and C. R. Cantor, Cell 37, 67 (1984); C. L. Smith, J. G. Econome, A. Schutt, S. Klco, C. R. Cantor, Science 236, 1448 (1987).
2. D. C. Schwartz and C. R. Cantor, Cell 37, 67 (1984); C. L. Smith, J. G. Econome, A. Schutt, S. Klco, C. R. Cantor, Science 236, 1448 (1987).
3. Y. Kohara, K. Akiyama, K. Isono, Cell 50, 495 (1987).
4. A. J. Link and M. V. Olson, Genetics 127, 681 (1991); L. Riles et al., ibid. 134, 81 (1993).
5. A. J. Link and M. V. Olson, Genetics 127, 681 (1991); L. Riles et al., ibid. 134, 81 (1993).
6. F. R. Blattner et al., Science 277, 1453 (1997).
7. R. D. Fleischmann et al., ibid. 269, 496 (1995).
8. W. Cai et al., Proc. Natl. Acad. Sci. U.S.A. 95, 3390 (1998).
9. C. Aston, C. Hiort, D. C. Schwartz, Methods Enzymol. 303, 55 (1999); D. C. Schwartz et al., Science 262, 110 (1993);
10. C. Aston, C. Hiort, D. C. Schwartz, Methods Enzymol. 303, 55 (1999); D. C. Schwartz et al., Science 262, 110 (1993);
11. W. Bautsch et al., in Genome Mapping, A Practical Approach, P. H. Dear, Ed. (Oxford Univ. Press, New York, 1997), pp. 281-313;
12. D. C. Schwartz and A. Samad, Curr. Opin. Biotechnol. 8, 70 (1997);
13. A. Samad et al., Nature 378, 516 (1995);
14. W. Wang, J. Lin, D. C. Schwartz, Biophys. J. 75, 513 (1998);
15. J. Reed, E. Singer, G. Kresbach, D. C. Schwartz, Anal. Biochem. 259, 80 (1998).
16. T. S. Ananthraman, B. Mishra, D. C. Schwartz, J. Comp. Biol. 4, 91 (1997).
17. X. Meng, K. Benson, K. Chada, E. Huff, D. C. Schwartz, Nature Genet. 9, 432 (1995).
18. W. Cai, H. Aburatani, D. Housman, Y. Wang, D. C. Schwartz, Proc. Natl. Acad. Sci. U.S.A. 92, 5164 (1995).
19. J. Jing et al., Genome Res. 9, 175 (1999).
20. T. S. Anantharaman, B. Mishra, D. C. Schwartz, Tech. Rep. 760 (Courant Institute, New York University, New York, 1998); T. S. Anantharaman, B. Mishra, D. C. Schwartz, in Seventh International Conference on Intelligent Systems for Molecular Biology (ISMB99), in press.
21. T. S. Anantharaman, B. Mishra, D. C. Schwartz, Tech. Rep. 760 (Courant Institute, New York University, New York, 1998); T. S. Anantharaman, B. Mishra, D. C. Schwartz, in Seventh International Conference on Intelligent Systems for Molecular Biology (ISMB99), in press.
22. c is the digestion rate, β is the relative sizing error, n is the expected number of restriction fragments per genomic DNA molecule, and k is the integer parameter directly related to overlap threshold ratio θ.
23. E. Lee, B. Porter, E. Huff, unpublished data.
24. Z. Lai, unpublished data.
25. F. Blattner, unpublished data.
26. O. White et al., data not shown.
27. Deinococcus radiodurans has a number of powerful DNA repair systems, including a fast-acting dimer excision system as well as an unusual double-stranded DNA break repair system (31) [V. Mattimore and J. R. Battista, J. Bacteriol. 178, 633 (1996); K. W. Minton, Mutat. Res. 363, 1 (1996)]. It carries multiple (4 to 10) copies of homologous chromosomes and plasmids, which are postulated to exist in pairs that are aligned relative to one another (28) [M. T. Hansen, J. Bacteriol. 134, 71 (1978); M. J. Daly and K. W. Minton, ibid. 177, 5505 (1995)].
28. J. Lin, data not shown.
29. The systematic error associated with the mapmaking for the second chromosome, for which complete sequence information is available from O. White, was <0.2%. The contig was assembled from 100 molecules by means of the Gentig algorithm. The sizes (in kilobases) of the 91 Nhe I fragments were 5.3, 18.9, 47.2, 23, 28, 18.4, 30.8, 40.8, 132.5, 3.8, 16.4, 29.9, 39, 13, 61.8, 34.4, 50.9, 45.6, 11.5, 12.5, 17.8, 22.9, 19.5, 3.6, 4.2, 3, 28.8, 6.4, 27.7, 9.6, 15, 26.9, 6.2, 15.6, 20.2, 7.5, 118.1, 11.3, 92, 15.7, 30, 23, 94.2, 34.1, 8.8, 18.9, 8.1, 20.1, 1.9, 87.5, 13.5, 79, 9.8, 93.2, 58.8, 3.1, 10.5, 5, 2.9, 8.6, 29.1, 6.4, 16.1, 26.3, 28.7, 17.7, 4.4, 18.4, 8.4, 17.1, 42.5, 30, 64.1, 47, 17.3, 27.7, 46.1, 5.1, 65.6, 46.2, 18.2, 14.4, 37.9, 35.7, 33.3, 23.2, 2.6, 28.8, 13.4, 37.5, and 50.5.
30. A direct calculation for D. radiodurans indicates that about 110 genomic DNA molecules, each of expected length 500 kb, digested with a six-cutter enzyme, with a digestion rate of 50% and a relative sizing error of 10%, would overlap these molecules into one single island with ∼0.04% probability that a declared overlap in the computed contig is false.
31. J. Lin and R. Qi, data not shown. We mapped a series of probes developed from D. radiodurans sequences to the composite map by Southern blot analysis (J. Lin et al., data not shown). Genomic DNA fragments were prepared by Not I digestion in solution (tube), surface-mounted, then optically mapped with Nhe I and overlapped with Gentig. The sizes (in kilobases) of the nine Not I fragments were 381, 354, 468, 239, 400, 180, 228, 253, and 103. Any given sequence or probe was localized to a particular large Not I restriction fragment and to a Nhe I restriction fragment by Southern blotting. Probes were generated by the polymerase chain reaction from genomic DNA templates with primers designed from preliminary shotgun sequence information: recA, (katA, orf1, plsx), DNA polymerase, and ribonuclease P. Results confirmed optical maps and preliminary sequence assemblies.
32. C. Lioutas, C. Schmetz, E. Tannich, Exp. Parasitol. 80, 349 (1995).
33. M. J. Daly, unpublished data.
34. O. White et al., unpublished data.
35. M. J. Daly and K. W. Minton, Gene 187, 225 (1997); J. Bacteriol. 177, 5495 (1995).
36. M. J. Daly and K. W. Minton, Gene 187, 225 (1997); J. Bacteriol. 177, 5495 (1995).
37. M. Kikuchi, S. Kitayama, S. H. Sjarief, H. Watanabe, Radiat. Res. 139, 123 (1994).
38. M. J. Daly and K. W. Minton, Science 270, 1318 (1995).
39. K. W. Minton and M. J. Daly, Bioessays 17, 457 (1995).
40. 37, the dose yielding a 37% survival rate for plateau-phase wild type R1), using gel insert methodology. Agarose inserts were melted at 72°C, diluted 500× in TE buffer [1 mM EDTA and 10 mM tris (pH 8.0)], and mounted for optical mapping. More than 10,000 irradiated DNA molecules were studied for the presence of circles or other aberrant structures.
41. M. J. Daly and K. W. Minton, J. Bacteriol. 178, 4461 (1996).
42. J. Lin, data not shown.
43. B. B. Bederson et al., in Human Factors in Web Development, L. Ratner, E. Grose, C. Forsythe, Eds. (Erlbaum, Mahwah, NJ, 1998), p. 255.
44. J. Lin, data not shown.
45. _, data not shown.
46. We thank T. Burland for Geneplot software, S. Paxia for Pad software (33), and F. Blattner for prepublication E. coli sequence. Partially funded by the U.S. Department of Energy and NIH, by Department of Energy Office of Biological and Environmental Research grants DE-FG02-98ER62583, DE-FG02-97ER62492, DE-FG07-97ER20293, and DE-FG02-98ER62554, and by U.S. Public Health Service grants GM39933 and HG0025-08.