Abstract
One way in which bacteria adapt to changes in their environment is by altering the expression states of their cellular surface structures such as fimbriae, flagella, and capsules. In some cases, expression of a structure varies between OFF and ON states, whereas in other cases expression fluctuates between high and low levels. This mechanism, known as phase variation, results in a skewed distribution of phenotypic characteristics within a bacterial population. Bacteria may also undergo antigenic variation in which they display qualitative differences in cell surface molecules that can be detected by specific antisera. As discussed below, phase variation and antigenic variation are not always separate processes. For example, antigenic variation between H1 and H2 flagellar expression in Salmonella is regulated by phase variation of H2 (Glasgow et al., 1989). In contrast, fimbrial antigenic variation in Neisseria gonorrhoeae can result in fimbrial phase variation (Davies et al., 1994). In this chapter, we focus on four basic mechanisms by which phase variation occurs: homologous recombination, site-specific recombination, slipped strand mispairing at nucleotide repeats, and DNA methylation pattern formation.
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References
Abraham, J. M., C. S. Freitag, J. R. Clements, and B. I. Eisenstein. 1985. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc. Natl. Acad. Sci. USA 82:5724–5727.
Barbour, A. 1993. Linear DNA of Borrelia species and antigenic variation. Trends in Microbiol.pp. 239–239.
Bartlett, D. H., M. E. Wright, and M. Silverman. 1988. Variable expression of extracellular polysaccharide in the marine bacterium Pseudomonas atlantica is controlled by genome rearrangement. Proc. Natl. Acad. Sci. USA 85:3923–3927.
Belland, R. J. 1991. H-DNA formation by the coding repeat elements of neisserial opa genes. Mol. Microbiol.5:2351–2360.
Belland, R. J., S. G. Morrison, P. van der Ley, and J. Swanson. 1989. Expression and phase variation of gonococcal P.II genes in Escherichia coli involves ribosomal frameshifting and slipped-strand mispairing. Mol. Microbiol.3:777–786.
Bergstrom, S., K. Robbins, J. M. Koomey, and J. Swanson. 1986. Piliation control mechanisms in Neisseria gonorrhoeae. Proc. Acad. Natl. Sci. USA 83:3890–3894.
Blyn, L. B., B. A. Braaten, and D. A. Low. 1990. Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. EMBO J.9:4045–4054.
Braaten, B. A., X. Nou, L. S. Kaltenbach, and D. A. Low. 1994. Methylation patterns in pap regulatory DNA control the pyelonephritis-associated pili phase variation in E. coli. Cell 76:577–588.
Craig, N. L. 1988. The mechanism of conservative site-specific recombination. Ann. Rev. Genet.22:77–105.
Dybvig, K., and H. Yu. 1994. Regulation of a restriction and modification system via DNA inversion in Mycoplasma pulmonis. Mol. Microbiol.12:547–560.
Feng, J. A., R. C. Johnson, and R. E. Dickerson. 1994. Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science 263:348–355.
Glasgow, A. C., and A. G. Lenich. 1994. Amino acid sequence homology between Piv, an essential protein in site-specific DNA inversion in Moraxella lacunata, and transposases of an unusual family of insertion elements. J. Bacteriol.176:4160–4164.
Haas, R. and T. F. Meyer. 1986. The repertoire of silent pilus genes in Neisseria gonorr-hoeae: evidence for gene conversion. Cell 44:107–115.
Hagblom, P., E. Segal, E. Billyard, and M. So. 1985. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315:156–158.
Heichman, K. A. and R. C. Johnson. 1990. The hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science 249:511–517.
Jonsson, A. B., J. Pfeifer, and S. Normark. 1992. Neisseria gonorrhoeae PilC expression provides a selective mechanism for structural diversity of pili. Proc. Natl. Acad. Sci. USA 89:3204–3208.
Kaltenbach, L. S., B. A. Braaten, and D. A. Low. 1995. Specific binding of Papl to Lrp-pap DNA complexes. J. Bacteriol. 177:6449–6455.
Komano, T., S. R. Kim, T. Yoshida, and T. Nisioka. 1994. DNA rearrangement of the shufflon determines recipient specificity in liquid mating of Incll plasmid R64. J. Mol. Biol.243:6–9.
Levinson, G. and G. A. Gutman. 1987. Slipped-strand mispairing: A major mechanism for DNA sequence evolution. Mol. Biol. Evol.4:203–221.
Manning, P. A., A. Kaufmann, U. Roll, J. Pohlner, T. F. Meyer, and R. Haas. 1991. L-pilin variants of Neisseria gonorrhoeae MS11. Mol. Microbiol.5:917–926.
Marrs, C. F., F. W. Rozsa, M. Hackel, S. P. Stevens, and A. C. Glasgow. 1990. Identification, cloning, and sequencing of piv, a new gene involved in inverting the pilin genes of Moraxella lacunata. J. Bacteriol. 172:4370–4377.
Marrs, C. F. 1994. Type IV pili in the families Moraxellaceae and Neisseriaciae.In Molecular Genetics of Bacterial Pathogenesis, V. L. Miller et al., eds. pp. 127–143. ASM Press, Washington, D.C.
McClain, M. S., I. C. Blomfield, and B. I. Eisenstein. 1991. Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli. J. Bacteriol.173:5308–5314.
Nou, X., B. Braaten, L. Kaltenbach, and D. Low. 1995. Differential binding of Lrp to two sets of pap DNA binding sites, mediated by PapI, regulates Pap phase variation in Escherichia coli.EMBO J.14:5785–5797.
Nou, X., B. Skinner, B. Braaten, L. Blyn, D. Hirsh, and D. Low. 1993. Regulation of pyelonephritis-associated pili phase variation in Escherichia coli: binding of the PapI and Lrp regulatory proteins is controlled by DNA methylation. Mol. Microbiol.7:545–553.
Ou, J. T., L. S. Baron, F. A. Rubin, and D. J. Kopecko. 1988. Specific insertion and deletion of insertion sequence l-like DNA element causes the reversible expression of the virulence capsular antigen of Citrobacter freundii in Escherichia coli. Proc. Natl. Acad. Sci. USA 85:4402–4405.
Restrepo, B. I., and A. G. Barbour. 1994. Antigen diversity in the bacterium B. hermsii through somatic mutations in rearranged vmp genes. Cell 78:867–876.
Robertson, B. D. and T. F. Meyer. 1992. Genetic variation in pathogenic bacteria. Trends in Genetics 8:422–427.
Roche, R. J. and E. R. Moxon. 1995. Phenotypic variation of carbohydrate surface antigens and pathogenesis of Haemophilus influenzae infections. Trends Microbiol.8:304–309.
Rudel, T., J. P. M. van Putten, C. P. Gibbs, R. Haas, and T. F. Meyer. 1992. Interaction of two variable proteins (pilE and pilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol.6:3439–3450.
Sarkari, J., N. Pandit, E. R. Moxon, and M. Achtman. 1994. Variable expression of the Opc outer membrane protein of Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol.13:207–217.
Seifert, H. S., R. S. Ajioka, C. Marchai, P. F. Sparling, and M. So. 1988. DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature 336:392–396.
Sparling, P. F., J. G. Cannon, and M. So. 1986. Phase and antigenic variation of pili and outer membrane protein II of Neisseria gonorrhoeae. J. Infect. Dis.153:196–201.
Stark, W. M., M. R. Boocock, and D. J. Sherratt. 1992. Catalysis by site-specific recombinases. Trends in Genetics 8:432–438.
Stern, A., M. Brown, P. Nickel, and T. F. Meyer. 1986. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61–71.
Stibitz, S., W. Aaronson, D. Monack, and S. Falkow. 1989. Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338:266–269.
Swanson, J., S. Morrison, O. Barrerea, and S. Hill. 1990. Piliation changes in transformation-defective Neisseria gonorrhoeae: J. Exp. Med.171:2131.
van der Ende, A., C. T. Hopman, S. Zaat, B. B. O. Essink, B. Berkhout, and J. Dankert. 1995. Variable expression of Class 1 outer membrane protein in Neissera meningitidis is caused by variation in the spacing between the-10 and-35 regions of the promoter. J. Bacteriol.177:2475–2480.
van der Woude, M. W. and D. A. Low. 1994. Leucine-responsive regulatory protein and deoxyadenosine methylase control the phase variation and expression of the E. coli sfa and daa pili operons. Mol. Microbiol.11:605–618.
van der Woude, M. W., L. S. Kaltenbach, and D. A. Low. 1995. Leucine-responsive regulatory protein plays dual roles as both an activator and a repressor of the E. coli pap operon. Molec. Microbiol.17:303–312.
van Ham, S. M., L. van Alphen, F. R. Mooi, and J. P. M. van Putten. 1993. Phase variation of H. influenzae fimbriae: Transcriptional control of two divergent genes through a variable combined promoter region. Cell 73:1187–1196.
Weiser, J. N., J. M. Love, and R. E. Moxon. 1989. The molecular mechanism of phase variation of H. influenzae lipopolysaccharide. Cell 59:657–665.
Yogev, D., R. Rosengarten, R. Watson-McKown, and K. S. Wise. 1991. Molecular basis of Mycoplasma surface antigenic variation: a novel set of divergent genes undergo spontaneous mutation of periodic coding regions and 5″ regulatory sequences. EMBO J.13:4069–4079.
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van der Woude, M., Braaten, B., Low, D. (1998). Phase Variation. In: de Bruijn, F.J., Lupski, J.R., Weinstock, G.M. (eds) Bacterial Genomes. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6369-3_14
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DOI: https://doi.org/10.1007/978-1-4615-6369-3_14
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