1887

Abstract

Previously, a complete genome analysis of strain MC58 revealed the largest repertoire of putative phase-variable genes described in any species to date. Initial comparisons with two incomplete spp. genome sequences available at that time revealed differences in the repeats associated with these genes in the form of polymorphisms, the absence of the potentially unstable elements in some alleles, and in the repertoire of the genes that were present. Analyses of the complete genomes of strain Z2491 and strain FA1090 have been performed and are combined with a comprehensive comparative analysis between the three available complete genome sequences. This has increased the sensitivity of these searches and provided additional contextual information that facilitates the interpretation of the functional consequences of repeat instability. This analysis identified: (i) 68 phase-variable gene candidates in strain Z2491, rather than the 27 previously reported; (ii) 83 candidates in strain FA1090; and (iii) 82 candidates in strain MC58, including an additional 19 identified through cross-comparisons with the other two strains. In addition to the 18 members of the gene family, a repertoire of 119 putative phase-variable genes is described, indicating a huge potential for diversification mediated by this mechanism of gene switching in these species that is central to their interactions with the host and environmental transitions. Eighty-two of these are either known (14) or strong (68) candidates for phase variation, which together with the genes make a total of 100 identified genes. The repertoires of the genes identified in this analysis diverge from the different species groupings, indicating horizontal exchange that significantly affects the species and strain complements of these genes.

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2001-08-01
2020-09-23
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References

  1. Akiyama M., Crooke E., Kornberg A.. 1993; An exopolyphosphatase of Escherichia coli . The enzyme and its ppx gene in a polyphosphate operon. J Biol Chem268:633–639
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Zhang J., Zhang Z., Miller W., Lipman D. J., Schäffer A. A.. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  3. Antognoni F., Del Duca S., Kuraishi A., Kawabe E., Fukuchi-Shimogori T., Kashiwagi K., Igarashi K.. 1999; Transcriptional inhibition of the operon for the spermidine uptake system by the substrate binding protein PotD. J Biol Chem274:1942–1948[CrossRef]
    [Google Scholar]
  4. Appelmelk B. J., Martin S. L., Monteiro M. A.. 10 other authors 1999; Phase variation in Helicobacter pylori lipopolysaccharide due to changes in the lengths of poly(C) tracts in alpha3-fucosyltransferase genes. Infect Immun67:5361–5366
    [Google Scholar]
  5. Appelmelk B. J., Martino M. C., Veenhof E.. 7 other authors 2000; Phase variation in H type I and Lewis a epitopes of Helicobacter pylori lipopolysaccharide. Infect Immun68:5928–5932[CrossRef]
    [Google Scholar]
  6. Banerjee A., Wang R., Uljon S. N., Rice P. A., Gotschlich E. C., Stein D. C.. 1998; Identification of the gene ( lgtG ) encoding the lipooligosaccharide beta chain synthesizing glucosyl transferase from Neisseria gonorrhoeae . Proc Natl Acad Sci USA95:10872–10877[CrossRef]
    [Google Scholar]
  7. Blinkowa A. L., Walker J. R.. 1990; Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res18:1725–1729[CrossRef]
    [Google Scholar]
  8. Bowler L. D., Zhang Q. Y., Riou J. Y., Spratt B. G.. 1994; Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis : natural events and laboratory simulation. J Bacteriol176:333–337
    [Google Scholar]
  9. Carson S. D., Stone B., Beucher M., Fu J., Sparling P. F.. 2000; Phase variation of the gonococcal siderophore receptor FetA. Mol Microbiol36:585–593
    [Google Scholar]
  10. Chen C. J., Elkins C., Sparling P. F.. 1998; Phase variability of hemoglobin utilization in N. gonorrhoeae . Infect Immun66:987–993
    [Google Scholar]
  11. Durbin R., Thierry-Mieg J. T.. 1991; A . e legans DataBase. Documentation, code and data. available from http://www.acedb.org
  12. Eckert K. A., Yan G.. 2000; Mutational analyses of dinucleotide and tetranucleotide microsatellites in Escherichia coli : influence of sequence on expansion mutagenesis. Nucleic Acids Res28:2831–2838[CrossRef]
    [Google Scholar]
  13. Eisenberg M. A.. 1987; Biosynthesis of biotin and lipoic acid. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp544–550 Edited by Neidhardt F. C., Ingraham J. L., Magasanik B., Low K. B., Schaechter M., Umbarger H. E.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  14. van der Ende A., Hopman C. T., Zaat S., Essink B. B., Berkhout B., Dankert J.. 1995; Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the −10 and −35 regions of the promoter. J Bacteriol177:2475–2480
    [Google Scholar]
  15. van der Ende A., Hopman C. T., Dankert J.. 2000; Multiple mechanisms of phase variation of PorA in Neisseria meningitidis. . Infect Immun68:6685–6690[CrossRef]
    [Google Scholar]
  16. Erwin A. L., Gotschlich E. C.. 1996; Cloning of a Neisseria meningitidis gene for l-lactate dehydrogenase (l-LDH): evidence for a second meningococcal l-LDH with different regulation. J Bacteriol178:4807–4813
    [Google Scholar]
  17. Feil E., Carpenter G., Spratt B. G.. 1995; Electrophoretic variation in adenylate kinase of Neisseria meningitidis is due to inter- and intraspecies recombination. Proc Natl Acad Sci USA92:10535–10539[CrossRef]
    [Google Scholar]
  18. Flower A. M., McHenry C. S.. 1990; The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci USA87:3713–3717[CrossRef]
    [Google Scholar]
  19. Haas R., Meyer T. F.. 1987; Molecular principles of antigenic variation in Neisseria gonorrhoeae . Antonie Leeuwenhoek53:431–434[CrossRef]
    [Google Scholar]
  20. van Ham S. M., van Alphen L., Mooi F. R., van Putten J. P.. 1993; Phase variation of H. influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell73:1187–1196[CrossRef]
    [Google Scholar]
  21. Hammerschmidt S., Muller A., Sillmann H.. 7 other authors 1996; Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene ( siaD ): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol Microbiol20:1211–1220[CrossRef]
    [Google Scholar]
  22. Hancock J. M., Shaw P. J., Bonneton F., Dover G. A.. 1999; High sequence turnover in the regulatory regions of the developmental gene hunchback in insects. Mol Biol Evol16:253–265[CrossRef]
    [Google Scholar]
  23. Hood D. W., Deadman M. E., Jennings M. P., Bisercic M., Fleischmann R. D., Venter J. C., Moxon E. R.. 1996; DNA repeats identify novel virulence genes in Haemophilus influenzae. . Proc Natl Acad Sci USA93:11121–11125[CrossRef]
    [Google Scholar]
  24. Imamura N., Nakayama H.. 1982; thiK and thiL loci of Escherichia coli. . J Bacteriol151:708–717
    [Google Scholar]
  25. Jennings M. P., Virji M., Evans D., Foster V., Srikhanta Y. N., Steeghs L., Moxon E. R., van der Ley P.. 1998; Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. . Mol Microbiol29:975–984[CrossRef]
    [Google Scholar]
  26. Jennings M. P., Srikhanta Y. N., Moxon E. R., Kramer M., Poolman J. T., Kuipers B., van der Lay P.. 1999; The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. . Microbiology145:3013–3021
    [Google Scholar]
  27. Jonsson A. B., Nyberg G., Normark S.. 1991; Phase variation of gonococcal pili by frameshift mutation in pilC , a novel gene for pilus assembly. EMBO J10:477–488
    [Google Scholar]
  28. Josenhans C., Eaton K. A., Thevenot T., Suerbaum S.. 2000; Switching of flagellar motility in Helicobacter pylori by reversible length variation of a short homopolymeric sequence repeat in fliP , a gene encoding a basal body protein. Infect Immun68:4598–4603[CrossRef]
    [Google Scholar]
  29. Kizil G., Todd I., Atta M., Borriello S. P., Ait-Tahar K., Ala’Aldeen D. A.. 1999; Identification and characterization of TspA, a major CD4(+) T-cell- and B-cell-stimulating Neisseria -specific antigen. Infect Immun67:3533–3541
    [Google Scholar]
  30. Malorny B., Morelli G., Kusecek B., Kolberg J., Achtman M.. 1998; Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J Bacteriol180:1323–1330
    [Google Scholar]
  31. Meyer T. F., van Putten J. P.. 1989; Genetic mechanisms and biological implications of phase variation in pathogenic neisseriae. Clin Microbiol Rev Suppl 2S139–S145
    [Google Scholar]
  32. O’Hara B. P., Norman R. A., Wan P. T., Roe S. M., Barrett T. E., Drew R. E., Pearl L. H.. 1999; Crystal structure and induction mechanism of AmiC–AmiR: a ligand-regulated transcription antitermination complex. EMBO J18:5175–5186[CrossRef]
    [Google Scholar]
  33. Parkhill J., Achtman M., James K. D.. 25 other authors 2000; Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature404:502–506[CrossRef]
    [Google Scholar]
  34. Peak I. R. A., Jennings M., Hood D. W., Moxon E. R.. 1999; Tetranucleotide repeats identify novel virulence determinant homologues in Neisseria meningitidis. . Microb Pathog26:13–23[CrossRef]
    [Google Scholar]
  35. Peck B., Ortkamp M., Diehl K. D., Hundt E., Knapp B.. 1999; Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. . Nucleic Acids Res27:3325–3333[CrossRef]
    [Google Scholar]
  36. Richardson A. R., Stojiljkovic I.. 1999; HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis , undergoes phase variation. J Bacteriol181:2067–2074
    [Google Scholar]
  37. Ruiz-Lozano J. M., Bonfante P.. 2000; A Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita possesses the vacB gene, which is involved in host cell colonization by bacteria. Microb Ecol39:137–144[CrossRef]
    [Google Scholar]
  38. Sarkari J., Pandit N., Moxon E. R., Achtman M.. 1994; Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol13:207–217[CrossRef]
    [Google Scholar]
  39. Saunders N. J.. 1999; Bacterial phase variation associated with repetitive DNA. PhD thesisThe Open University
    [Google Scholar]
  40. Saunders N. J., Peden J. F., Hood D. W., Moxon E. R.. 1998; Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol27:1091–1098[CrossRef]
    [Google Scholar]
  41. Saunders N. J., Hood D. W., Moxon E. R.. 1999; Bacterial evolution: bacteria play pass the gene. Curr Biol9:R180–R183[CrossRef]
    [Google Scholar]
  42. Saunders N. J., Jeffries A. C., Peden J. F., Hood D. W., Tettelin H., Rappuoli R., Moxon E. R.. 2000; Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol37:207–215[CrossRef]
    [Google Scholar]
  43. Snyder L. A. S., Saunders N. J., Shafer W. M.. 2001; A putatively phase variable gene ( dca ) required for natural competence in Neisseria gonorrhoeae but not Neisseria meningitidis is located within the division cell wall ( dcw ) gene cluster. J Bacteriol183:1233–1241[CrossRef]
    [Google Scholar]
  44. Sparling P. F., Cannon J. G., So M.. 1986; Phase and antigenic variation of pili and outer membrane protein II of Neisseria gonorrhoeae.. J Infect Dis153:196–201[CrossRef]
    [Google Scholar]
  45. Stern A., Brown M., Nickel P., Meyer T. F.. 1986; Opacity genes in Neisseria gonorrhoeae : control of phase and antigenic variation. Cell47:61–71[CrossRef]
    [Google Scholar]
  46. Stibitz S., Aaronson W., Monack D., Falkow S.. 1989; Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature338:266–269[CrossRef]
    [Google Scholar]
  47. Tettelin H., Saunders N. J., Heidelberg J.. 39 other authors 2000; Complete genome sequence of Neisseria meningitidis serotype B strain MC58. Science287:1809–1815[CrossRef]
    [Google Scholar]
  48. Tinsley C. R., Gotschlich E. C.. 1995; Cloning and characterization of the meningococcal polyphosphate kinase gene: production of polyphosphate synthesis mutants. Infect Immun63:1624–1630
    [Google Scholar]
  49. Tobe T., Sasakawa C., Okada N., Honma Y., Yoshikawa M.. 1992; vacB , a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri. . J Bacteriol 174:6359–6367
    [Google Scholar]
  50. Tomb J. F., White O., Kerlavage A. R.. 39 other authors 1997; The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature388:539–547
    [Google Scholar]
  51. Tsuchihashi Z., Kornberg A.. 1990; Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci USA87:2516–2520[CrossRef]
    [Google Scholar]
  52. Wang G., Rasko D. A., Sherburne R., Taylor D. E.. 1999; Molecular genetic basis for the variable expression of Lewis Y antigen in Helicobacter pylori : analysis of the α(1,2) fucosyltransferase gene. Mol Microbiol31:1265–1274[CrossRef]
    [Google Scholar]
  53. Wilson S., Drew R.. 1991; Cloning and DNA sequence of amiC , a new gene regulating expression of the Pseudomonas aeruginosa aliphatic amidase, and purification of the amiC product. J Bacteriol173:4914–4921
    [Google Scholar]
  54. Yamaoka Y., Kwon D. H., Graham D. Y.. 2000; A M(r) 34,000 proinflammatory outer membrane protein ( oipA ) of Helicobacter pylori. . Proc Natl Acad Sci USA97:7533–7538[CrossRef]
    [Google Scholar]
  55. Yang Q. L., Gotschlich E. C.. 1996; Variation of gonococcal lipooligosaccharide structure is due to alterations in poly-G tracts in lgt genes encoding glycosyl transferases. J Exp Med183:323–327[CrossRef]
    [Google Scholar]
  56. Yurieva O., Skangalis M., Kuriyan J., O’Donnell M.. 1997; Thermus thermophilis dnaX homolog encoding gamma- and tau-like proteins of the chromosomal replicase. J Biol Chem272:27131–2719[CrossRef]
    [Google Scholar]
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