Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Mar;172(3):1374–1379. doi: 10.1128/jb.172.3.1374-1379.1990

Capsulation in distantly related strains of Haemophilus influenzae type b: genetic drift and gene transfer at the capsulation locus.

J S Kroll 1, E R Moxon 1
PMCID: PMC208608  PMID: 2137816

Abstract

Among natural populations of capsulate Haemophilus influenzae, clones of strains with type b capsular polysaccharide are found in each of two widely separated phylogenetic divisions. The chromosomal capsulation locus found in strains from either division has a three-segment organization, with serotype-specific DNA nested between elements common to all serotypes, but pairwise comparison of the segments between the divisions suggests that they have distinct phylogenetic histories. Genes clustered in one of the non-serotype-specific segments appear to have diverged from an ancestral element, reflected in 12% nucleotide sequence divergence in one homologous pair. In contrast, genes conferring the capacity to produce type-specific polysaccharide exhibit no such divergence, and we speculate that these have been subject more recently to horizontal transfer within the bacterial population. Clinically important capsulate gram-negative bacteria share a common organization of their capsulation loci, arguing convergence on a successful arrangement of genes. In H. influenzae this appears to have allowed the occasional exchange of serotype-specific capsulation genes between strains, a event of potential clinical importance in this major bacterial pathogen.

Full text

PDF
1379

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beltran P., Musser J. M., Helmuth R., Farmer J. J., 3rd, Frerichs W. M., Wachsmuth I. K., Ferris K., McWhorter A. C., Wells J. G., Cravioto A. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7753–7757. doi: 10.1073/pnas.85.20.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boulnois G. J., Roberts I. S., Hodge R., Hardy K. R., Jann K. B., Timmis K. N. Analysis of the K1 capsule biosynthesis genes of Escherichia coli: definition of three functional regions for capsule production. Mol Gen Genet. 1987 Jun;208(1-2):242–246. doi: 10.1007/BF00330449. [DOI] [PubMed] [Google Scholar]
  3. Crisel R. M., Baker R. S., Dorman D. E. Capsular polymer of Haemophilus influenzae, type b. I. Structural characterization of the capsular polymer of strain Eagan. J Biol Chem. 1975 Jul 10;250(13):4926–4930. [PubMed] [Google Scholar]
  4. Echarti C., Hirschel B., Boulnois G. J., Varley J. M., Waldvogel F., Timmis K. N. Cloning and analysis of the K1 capsule biosynthesis genes of Escherichia coli: lack of homology with Neisseria meningitidis group B DNA sequences. Infect Immun. 1983 Jul;41(1):54–60. doi: 10.1128/iai.41.1.54-60.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ely S., Tippett J., Moxon E. R. Identification and characterization of a serotype b-specific segment of the Haemophilus influenzae genome. Infect Immun. 1989 Sep;57(9):2926–2928. doi: 10.1128/iai.57.9.2926-2928.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  7. Frosch M., Weisgerber C., Meyer T. F. Molecular characterization and expression in Escherichia coli of the gene complex encoding the polysaccharide capsule of Neisseria meningitidis group B. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1669–1673. doi: 10.1073/pnas.86.5.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Herriott R. M., Meyer E. M., Vogt M. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J Bacteriol. 1970 Feb;101(2):517–524. doi: 10.1128/jb.101.2.517-524.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hoiseth S. K., Connelly C. J., Moxon E. R. Genetics of spontaneous, high-frequency loss of b capsule expression in Haemophilus influenzae. Infect Immun. 1985 Aug;49(2):389–395. doi: 10.1128/iai.49.2.389-395.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hoiseth S. K., Moxon E. R., Silver R. P. Genes involved in Haemophilus influenzae type b capsule expression are part of an 18-kilobase tandem duplication. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1106–1110. doi: 10.1073/pnas.83.4.1106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Karlin S., Ghandour G. Multiple-alphabet amino acid sequence comparisons of the immunoglobulin kappa-chain constant domain. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8597–8601. doi: 10.1073/pnas.82.24.8597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kroll J. S., Hopkins I., Moxon E. R. Capsule loss in H. influenzae type b occurs by recombination-mediated disruption of a gene essential for polysaccharide export. Cell. 1988 May 6;53(3):347–356. doi: 10.1016/0092-8674(88)90155-9. [DOI] [PubMed] [Google Scholar]
  13. Kroll J. S., Moxon E. R. Capsulation and gene copy number at the cap locus of Haemophilus influenzae type b. J Bacteriol. 1988 Feb;170(2):859–864. doi: 10.1128/jb.170.2.859-864.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kroll J. S., Zamze S., Loynds B., Moxon E. R. Common organization of chromosomal loci for production of different capsular polysaccharides in Haemophilus influenzae. J Bacteriol. 1989 Jun;171(6):3343–3347. doi: 10.1128/jb.171.6.3343-3347.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  16. Moxon E. R., Deich R. A., Connelly C. Cloning of chromosomal DNA from Haemophilus influenzae. Its use for studying the expression of type b capsule and virulence. J Clin Invest. 1984 Feb;73(2):298–306. doi: 10.1172/JCI111214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moxon E. R. The molecular basis of Haemophilus influenzae virulence. J R Coll Physicians Lond. 1985 Jul;19(3):174–178. [PMC free article] [PubMed] [Google Scholar]
  18. Musser J. M., Kroll J. S., Moxon E. R., Selander R. K. Clonal population structure of encapsulated Haemophilus influenzae. Infect Immun. 1988 Aug;56(8):1837–1845. doi: 10.1128/iai.56.8.1837-1845.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Musser J. M., Kroll J. S., Moxon E. R., Selander R. K. Evolutionary genetics of the encapsulated strains of Haemophilus influenzae. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7758–7762. doi: 10.1073/pnas.85.20.7758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schlech W. F., 3rd, Ward J. I., Band J. D., Hightower A., Fraser D. W., Broome C. V. Bacterial meningitis in the United States, 1978 through 1981. The National Bacterial Meningitis Surveillance Study. JAMA. 1985 Mar 22;253(12):1749–1754. [PubMed] [Google Scholar]
  22. Vimr E. R., Aaronson W., Silver R. P. Genetic analysis of chromosomal mutations in the polysialic acid gene cluster of Escherichia coli K1. J Bacteriol. 1989 Feb;171(2):1106–1117. doi: 10.1128/jb.171.2.1106-1117.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zwahlen A., Kroll J. S., Rubin L. G., Moxon E. R. The molecular basis of pathogenicity in Haemophilus influenzae: comparative virulence of genetically-related capsular transformants and correlation with changes at the capsulation locus cap. Microb Pathog. 1989 Sep;7(3):225–235. doi: 10.1016/0882-4010(89)90058-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES