Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1988 Aug;119(4):771–778. doi: 10.1093/genetics/119.4.771

Effects of Chromosomal Inversion on Cell Fitness in Escherichia Coli K-12

C W Hill 1, J A Gray 1
PMCID: PMC1203463  PMID: 2900793

Abstract

In an effort to learn what factors might mitigate the establishment of Escherichia coli variants bearing major chromosomal rearrangements, we have examined the effects on cell growth of two inversions between rRNA operons. One of these inversions, IN(rrnD-rrnE), had been propagated in a commonly used subline of E. coli K-12 for approximately 30 yr before its discovery, a fact that illustrates the absence of obvious detrimental effects associated with the inversion. We found that culturing under conditions requiring repeated transition from stationary phase to rapid growth led to the replacement of IN(rrnD-rrnE) cells by cells that had undergone either of two types of additional chromosomal inversion: one type fully restored the wild-type order, while the other partially restored it. The partial reinversion was also between rrn operons, but it left a small transposition. The tendency for overgrowth by these revertants persisted through several rounds of periodic selection. In contrast, the other inversion, IN(rrnG-rrnE), was associated with severe, detrimental effects. The effects of IN(rrnG-rrnE) were also alleviated by full or partial reinversion. The probable relationship between the severity of the effects caused by the inversions and the degree of displacement of the replication origin is discussed. Spontaneous inversion events between rrn operons separated by 18% of the chromosome were estimated to occur at a frequency of roughly 10(-5). If extended to natural situations, the growth disadvantage together with the relatively high frequency of reinversion suggest that clones of cells with an inversion between these rrn operons would be readily overgrown by revertants.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

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

  1. ATWOOD K. C., SCHNEIDER L. K., RYAN F. J. Periodic selection in Escherichia coli. Proc Natl Acad Sci U S A. 1951 Mar;37(3):146–155. doi: 10.1073/pnas.37.3.146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson R. P., Roth J. R. Gene duplication in bacteria: alteration of gene dosage by sister-chromosome exchanges. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1083–1087. doi: 10.1101/sqb.1979.043.01.120. [DOI] [PubMed] [Google Scholar]
  3. Boros I., Kiss A., Venetianer P. Physical map of the seven ribosomal RNA genes of Escherichia coli. Nucleic Acids Res. 1979;6(5):1817–1830. doi: 10.1093/nar/6.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Caro L. G., Berg C. M. Chromosome replication in some strains of Escherichia coli K12. Cold Spring Harb Symp Quant Biol. 1968;33:559–573. doi: 10.1101/sqb.1968.033.01.063. [DOI] [PubMed] [Google Scholar]
  5. Casse F., Pascal M. C., Chippaux M. Comparison between the chromosomal maps of Escherichia coli and Salmonella typhimurium. Length of the inverted segment in the trp region. Mol Gen Genet. 1973 Aug 17;124(3):253–257. doi: 10.1007/BF00293096. [DOI] [PubMed] [Google Scholar]
  6. Hill C. W., Combriato G. Genetic duplications induced at very high frequency by ultraviolet irradiation in Escherichia coli. Mol Gen Genet. 1973 Dec 31;127(3):197–214. doi: 10.1007/BF00333760. [DOI] [PubMed] [Google Scholar]
  7. Hill C. W., Grafstrom R. H., Harnish B. W., Hillman B. S. Tandem duplications resulting from recombination between ribosomal RNA genes in Escherichia coli. J Mol Biol. 1977 Nov 5;116(3):407–428. doi: 10.1016/0022-2836(77)90077-8. [DOI] [PubMed] [Google Scholar]
  8. Hill C. W., Harnish B. W. Inversions between ribosomal RNA genes of Escherichia coli. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7069–7072. doi: 10.1073/pnas.78.11.7069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hill C. W., Harnish B. W. Transposition of a chromosomal segment bounded by redundant rRNA genes into other rRNA genes in Escherichia coli. J Bacteriol. 1982 Feb;149(2):449–457. doi: 10.1128/jb.149.2.449-457.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  11. Lehner A. F., Harvey S., Hill C. W. Mapping and spacer identification of rRNA operons of Salmonella typhimurium. J Bacteriol. 1984 Nov;160(2):682–686. doi: 10.1128/jb.160.2.682-686.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lin R. J., Capage M., Hill C. W. A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome. J Mol Biol. 1984 Jul 25;177(1):1–18. doi: 10.1016/0022-2836(84)90054-8. [DOI] [PubMed] [Google Scholar]
  13. Louarn J. M., Bouché J. P., Legendre F., Louarn J., Patte J. Characterization and properties of very large inversions of the E. coli chromosome along the origin-to-terminus axis. Mol Gen Genet. 1985;201(3):467–476. doi: 10.1007/BF00331341. [DOI] [PubMed] [Google Scholar]
  14. Louarn J., Patte J., Louarn J. M. Suppression of Escherichia coli dnaA46 mutations by integration of plasmid R100.1. derivatives: constraints imposed by the replication terminus. J Bacteriol. 1982 Aug;151(2):657–667. doi: 10.1128/jb.151.2.657-667.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Riley M., Anilionis A. Evolution of the bacterial genome. Annu Rev Microbiol. 1978;32:519–560. doi: 10.1146/annurev.mi.32.100178.002511. [DOI] [PubMed] [Google Scholar]
  16. Sanderson K. E. Genetic relatedness in the family Enterobacteriaceae. Annu Rev Microbiol. 1976;30:327–349. doi: 10.1146/annurev.mi.30.100176.001551. [DOI] [PubMed] [Google Scholar]
  17. Savić D. J., Romac S. P., Ehrlich S. D. Inversion in the lactose region of Escherichia coli K-12: inversion termini map within IS3 elements alpha 3 beta 3 and beta 5 alpha 5. J Bacteriol. 1983 Aug;155(2):943–946. doi: 10.1128/jb.155.2.943-946.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schmid M. B., Roth J. R. Gene location affects expression level in Salmonella typhimurium. J Bacteriol. 1987 Jun;169(6):2872–2875. doi: 10.1128/jb.169.6.2872-2875.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schmid M. B., Roth J. R. Genetic methods for analysis and manipulation of inversion mutations in bacteria. Genetics. 1983 Nov;105(3):517–537. doi: 10.1093/genetics/105.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Timmons M. S., Lieb M., Deonier R. C. Recombination between IS5 elements: requirement for homology and recombination functions. Genetics. 1986 Aug;113(4):797–810. doi: 10.1093/genetics/113.4.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wolf B., Pato M. L., Ward C. B., Glaser D. A. On the origin and direction of replication of the E. coli chromosome. Cold Spring Harb Symp Quant Biol. 1968;33:575–584. doi: 10.1101/sqb.1968.033.01.064. [DOI] [PubMed] [Google Scholar]
  22. Xia X. M., Enomoto M. A naturally occurring large chromosomal inversion in Escherichia coli K12. Mol Gen Genet. 1986 Nov;205(2):376–379. doi: 10.1007/BF00430454. [DOI] [PubMed] [Google Scholar]
  23. de Massy B., Béjar S., Louarn J., Louarn J. M., Bouché J. P. Inhibition of replication forks exiting the terminus region of the Escherichia coli chromosome occurs at two loci separated by 5 min. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1759–1763. doi: 10.1073/pnas.84.7.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES