Abstract
We used 94 RAPD primers of different nucleotide composition to probe the genomic differences between a highly virulent P. multocida strain and an attenuated vaccine strain derived from the virulent strain after culturing the latter under increasing temperature for approximately 14,400 generations. The GC content of the vaccine strain is significantly (P < 0.05) lower than that of the virulent strain, contrary to the popular hypothesis of covariation between the GC content and temperature. The frequencies of AA, TA, and TT dinucleotides were higher, and those of AT, GC, and CG dinucleotides were lower, in the vaccine strain than in the virulent strain. A statistic called genomic RAPD entropy is formulated to measure the randomness of the genome, and the genome of the vaccine strain is more random than that of the virulent strain. These differences between the virulent and vaccine strains are interpreted in terms of mutation and selection under increased culturing temperature. A method for estimating substitution rates is developed in the appendix.
Full Text
The Full Text of this article is available as a PDF (211.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Argos P., Rossman M. G., Grau U. M., Zuber H., Frank G., Tratschin J. D. Thermal stability and protein structure. Biochemistry. 1979 Dec 11;18(25):5698–5703. doi: 10.1021/bi00592a028. [DOI] [PubMed] [Google Scholar]
- Bennett A. F., Dao K. M., Lenski R. E. Rapid evolution in response to high-temperature selection. Nature. 1990 Jul 5;346(6279):79–81. doi: 10.1038/346079a0. [DOI] [PubMed] [Google Scholar]
- Bernardi G., Olofsson B., Filipski J., Zerial M., Salinas J., Cuny G., Meunier-Rotival M., Rodier F. The mosaic genome of warm-blooded vertebrates. Science. 1985 May 24;228(4702):953–958. doi: 10.1126/science.4001930. [DOI] [PubMed] [Google Scholar]
- Bull J. J., Badgett M. R., Wichman H. A., Huelsenbeck J. P., Hillis D. M., Gulati A., Ho C., Molineux I. J. Exceptional convergent evolution in a virus. Genetics. 1997 Dec;147(4):1497–1507. doi: 10.1093/genetics/147.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fryxell K. J., Zuckerkandl E. Cytosine deamination plays a primary role in the evolution of mammalian isochores. Mol Biol Evol. 2000 Sep;17(9):1371–1383. doi: 10.1093/oxfordjournals.molbev.a026420. [DOI] [PubMed] [Google Scholar]
- Gojobori T., Li W. H., Graur D. Patterns of nucleotide substitution in pseudogenes and functional genes. J Mol Evol. 1982;18(5):360–369. doi: 10.1007/BF01733904. [DOI] [PubMed] [Google Scholar]
- Hirsh D. C., Hansen L. M., Dorfman L. C., Snipes K. P., Carpenter T. E., Hird D. W., McCapes R. H. Resistance to antimicrobial agents and prevalence of R plasmids in Pasteurella multocida from turkeys. Antimicrob Agents Chemother. 1989 May;33(5):670–673. doi: 10.1128/aac.33.5.670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunt M. L., Adler B., Townsend K. M. The molecular biology of pasteurella multocida. Vet Microbiol. 2000 Mar 1;72(1-2):3–25. doi: 10.1016/s0378-1135(99)00183-2. [DOI] [PubMed] [Google Scholar]
- Hunter C. A. Sequence-dependent DNA structure. The role of base stacking interactions. J Mol Biol. 1993 Apr 5;230(3):1025–1054. doi: 10.1006/jmbi.1993.1217. [DOI] [PubMed] [Google Scholar]
- Kasten R. W., Hansen L. M., Hinojoza J., Bieber D., Ruehl W. W., Hirsh D. C. Pasteurella multocida produces a protein with homology to the P6 outer membrane protein of Haemophilus influenzae. Infect Immun. 1995 Mar;63(3):989–993. doi: 10.1128/iai.63.3.989-993.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawashima T., Amano N., Koike H., Makino S., Higuchi S., Kawashima-Ohya Y., Watanabe K., Yamazaki M., Kanehori K., Kawamoto T. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14257–14262. doi: 10.1073/pnas.97.26.14257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kushiro M., Shimizu M., Tomita K. Molecular cloning and sequence determination of the tuf gene coding for the elongation factor Tu of Thermus thermophilus HB8. Eur J Biochem. 1987 Dec 30;170(1-2):93–98. doi: 10.1111/j.1432-1033.1987.tb13671.x. [DOI] [PubMed] [Google Scholar]
- Lenski R. E., Mongold J. A., Sniegowski P. D., Travisano M., Vasi F., Gerrish P. J., Schmidt T. M. Evolution of competitive fitness in experimental populations of E. coli: what makes one genotype a better competitor than another? Antonie Van Leeuwenhoek. 1998 Jan;73(1):35–47. doi: 10.1023/a:1000675521611. [DOI] [PubMed] [Google Scholar]
- Leroi A. M., Bennett A. F., Lenski R. E. Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1917–1921. doi: 10.1073/pnas.91.5.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li W. H., Wu C. I., Luo C. C. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol. 1984;21(1):58–71. doi: 10.1007/BF02100628. [DOI] [PubMed] [Google Scholar]
- Marcelino L. A., André P. C., Khrapko K., Coller H. A., Griffith J., Thilly W. G. Chemically induced mutations in mitochondrial DNA of human cells: mutational spectrum of N-methyl-N'-nitro-N-nitrosoguanidine. Cancer Res. 1998 Jul 1;58(13):2857–2862. [PubMed] [Google Scholar]
- May B. J., Zhang Q., Li L. L., Paustian M. L., Whittam T. S., Kapur V. Complete genomic sequence of Pasteurella multocida, Pm70. Proc Natl Acad Sci U S A. 2001 Mar 6;98(6):3460–3465. doi: 10.1073/pnas.051634598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miguel B., Wang C., Maslin W. R., Keirs R. W., Glisson J. R. Subacute to chronic fowl cholera in a flock of Pharaoh breeder quail. Avian Dis. 1998 Jan-Mar;42(1):204–208. [PubMed] [Google Scholar]
- Packer M. J., Dauncey M. P., Hunter C. A. Sequence-dependent DNA structure: dinucleotide conformational maps. J Mol Biol. 2000 Jan 7;295(1):71–83. doi: 10.1006/jmbi.1999.3236. [DOI] [PubMed] [Google Scholar]
- Packer M. J., Dauncey M. P., Hunter C. A. Sequence-dependent DNA structure: tetranucleotide conformational maps. J Mol Biol. 2000 Jan 7;295(1):85–103. doi: 10.1006/jmbi.1999.3237. [DOI] [PubMed] [Google Scholar]
- Papadopoulos D., Schneider D., Meier-Eiss J., Arber W., Lenski R. E., Blot M. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3807–3812. doi: 10.1073/pnas.96.7.3807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Price S. B., Freeman M. D., MacEwen M. W. Molecular analysis of a cryptic plasmid isolated from avian strains of Pasteurella multocida. Vet Microbiol. 1993 Oct;37(1-2):31–43. doi: 10.1016/0378-1135(93)90180-f. [DOI] [PubMed] [Google Scholar]
- Riehle M. M., Bennett A. F., Long A. D. Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci U S A. 2001 Jan 9;98(2):525–530. doi: 10.1073/pnas.021448998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rocha E. P., Viari A., Danchin A. Oligonucleotide bias in Bacillus subtilis: general trends and taxonomic comparisons. Nucleic Acids Res. 1998 Jun 15;26(12):2971–2980. doi: 10.1093/nar/26.12.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang R. F., Campbell W., Cao W. W., Summage C., Steele R. S., Cerniglia C. E. Detection of Pasteurella pneumotropica in laboratory mice and rats by polymerase chain reaction. Lab Anim Sci. 1996 Feb;46(1):81–85. [PubMed] [Google Scholar]
- Wichman H. A., Badgett M. R., Scott L. A., Boulianne C. M., Bull J. J. Different trajectories of parallel evolution during viral adaptation. Science. 1999 Jul 16;285(5426):422–424. doi: 10.1126/science.285.5426.422. [DOI] [PubMed] [Google Scholar]
- Xia X., Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J Hered. 2001 Jul-Aug;92(4):371–373. doi: 10.1093/jhered/92.4.371. [DOI] [PubMed] [Google Scholar]
- Yang H., Fitz-Gibbon S., Marcotte E. M., Tai J. H., Hyman E. C., Miller J. H. Characterization of a thermostable DNA glycosylase specific for U/G and T/G mismatches from the hyperthermophilic archaeon Pyrobaculum aerophilum. J Bacteriol. 2000 Mar;182(5):1272–1279. doi: 10.1128/jb.182.5.1272-1279.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]