Abstract
Capsular polysaccharides are important virulence factors both in Gram-positive and Gramnegative bacteria. A similar cluster organization of the genes involved in the synthesis of bacterial exopolysaccharides has been postulated in both cases, suggesting that these clusters evolved by module assembly. Horizontal gene transfer has been postulated to explain the polymorphism found in these cellular polymers. The caplK and cap3A genes coding for the pneumococcal type 1 and type 3 UDP-glucose dehydrogenases, respectively, have been compared with other UDP-sugar dehydrogenases. We have observed that the evolutionary distance between CaplK and Cap3A is approximately equal to that found between CaplK (or Cap3A) and other UDP-GlcDH of families evolutionary distant like KfiD, the dehydrogenase from Escherichia coli K5. On the basis of comparisons of G + C content, patterns of synonymous and nonsynonymous substitutions, dinucleotide frequencies, and codon usage bias, we conclude that the kfiD gene has been introduced into E. coli from an exogenous source, probably from a streptococcal species.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Appel RD, Bairoch A, Hochstrasser DF (1994) A new generation of information retrieval tools for biologists: the example of the Ex-PASy WWW server. Trends Biochem Sci 19:258–260
Arrecubieta C, López R, Garciía E (1994) Molecular characterization of cap3A, a gene from the operon required for the synthesis of the capsule of Streptococcus pneumoniae type 3: sequencing of mutations responsible for the unencapsulated phenotype and localization of the capsular cluster on the pneumococcal chromosome. J Bacteriol 176:6375–6383
Arrecubieta C, Garcia E, Lopez R (1996) Demonstration of UDP- glucose dehydrogenase activity in cell extracts of Escherichia coli expressing the pneumococcal cap3A gene required for the synthesis of type 3 capsular polysaccharide. J Bacteriol 178:2971–2974
Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, Fitzgerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb T-F, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NSM, Weidman JF, Fuhrmann JL, Nguyen D, Utterback TR, Kelley JM, Peterson JD, Sadow PW, Hanna MC, Cotton MD, Roberts KM, Hurst MA, Kaine BP, Borodovsky M, Klenk H-P, Fraser CM, Smith HO, Woese CR, Venter JC (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073
Dougherty BA, van de Rijn I (1993) Molecular characterization of hasB from an operon required for hyaluronic acid synthesis in group A streptococci. Demonstration of UDP-glucose dehydrogenase activity. J Biol Chem 268:7118–7124
Dowson CG, Hutchison A, Brannigan JA, George RC, Hansman D, Linares J, Tomasz A, Maynard Smith J, Spratt BG (1989) Horizontal transfer of penicillin-binding protein genes in penicillin- resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci USA 86:8842–8846
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–7797
Felsenstein J (1993) PHYLIP (phytogeny inference package) version 3.5c. University of Washington, Seattle
Garci’a E, Lopez R (1997) Molecular biology of the capsular genes of Streptococcus pneumoniae. FEMS Microbiol Lett 149:1–10
Griffith F (1928) The significance of pneumococcal types. J Hyg 27: 113–159
Hyde JE, Sims PFG (1987) Anomalous dinucleotide frequencies in both coding and non-coding regions from the genome of the human malaria parasite Plasmodium falciparum. Gene 61:177–187
Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602
Medigue C, Rouxel T, Vigier P, Henault A, Danchin A (1990) Evidence for horizontal gene transfer in Escherichia coli speciation. J Mol Biol 222:851–856
Munoz R, Mollerach M, Lopez R, Garcia E (1997) Molecular organisation of the genes required for the synthesis of type 1 capsular polysaccharide of Streptococcus pneumoniae: formation of binary encapsulated pneumococci and identification of cryptic dTDP- rhamnose biosynthesis genes. Mol Microbiol 25:79–92
Nakamura Y, Gojobori T, Ikemura T (1997) Codon usage tabulated from the international DNA sequence databases. Nucleic Acids Res 25:244–245
Perter F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566
Petit C, Rigg GP, Pazzani C, Smith A, Sieberth V, Stevens M, Boulnois G, Jann K, Roberts IS (1995) Region 2 of the Escherichia coli K5 capsule gene cluster encoding proteins for the biosynthesis of the K5 polysaccharide. Mol Microbiol 17:611–620
Phillip GJ, Arnold J, Ivarie R (1987) The effect of codon usage on the oligonucleotide composition of the E. coli genome and identification of over- and underrepresented sequences by Markov chain analysis. Nucleic Acids Res 15:2627–2638
Reeves PR (1993) Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet 9:17–22
Reeves P (1997) Specialised clones and lateral transfer in pathogens. In: van der Zeijst BAM, Hoekstra WPM, van Embden JDA, van Alphen AJW (eds) Ecology of pathogenic bacteria. North-Holland, Amsterdam p 237
Roberts IS (1996) The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu Rev Microbiol 50:285–315
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sau S, Sun J, Lee CY (1997) Molecular characterization and transcriptional analysis of type 8 capsule genes in Staphylococcus aureus. J Bacteriol 179:1614–1621
Sharp P (1991) Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Biol 33:23–33
Stingele F, Neeser J-R, Mollet B (1996) Identification and characterization of the eps (exopolysaccharide) gene cluster for the Streptococcus thermophilus Sfi6. J Bacteriol 178:1680–1690
Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657
Syvanen M (1994) Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet 28:237–261
Thompson JD, Higgins DG, Ginson TJ (1994) CLUSTAL V: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Muñoz, R., García, E. & López, R. Evidence for horizontal transfer from streptococcus to escherichia coli of the kfid gene encoding the K5-specific UDP-glucose dehydrogenase. J Mol Evol 46, 432–436 (1998). https://doi.org/10.1007/PL00006322
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/PL00006322