Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1996 Aug;143(4):1843–1860. doi: 10.1093/genetics/143.4.1843

Selfish Operons: Horizontal Transfer May Drive the Evolution of Gene Clusters

J G Lawrence 1, J R Roth 1
PMCID: PMC1207444  PMID: 8844169

Abstract

A model is presented whereby the formation of gene clusters in bacteria is mediated by transfer of DNA within and among taxa. Bacterial operons are typically composed of genes whose products contribute to a single function. If this function is subject to weak selection or to long periods with no selection, the contributing genes may accumulate mutations and be lost by genetic drift. From a cell's perspective, once several genes are lost, the function can be restored only if all missing genes were acquired simultaneously by lateral transfer. The probability of transfer of multiple genes increases when genes are physically proximate. From a gene's perspective, horizontal transfer provides a way to escape evolutionary loss by allowing colonization of organisms lacking the encoded functions. Since organisms bearing clustered genes are more likely to act as successful donors, clustered genes would spread among bacterial genomes. The physical proximity of genes may be considered a selfish property of the operon since it affects the probability of successful horizontal transfer but may provide no physiological benefit to the host. This process predicts a mosaic structure of modern genomes in which ancestral chromosomal material is interspersed with novel, horizontally transferred operons providing peripheral metabolic functions.

Full Text

The Full Text of this article is available as a PDF (5.3 MB).

Selected References

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

  1. AMES B. N., MARTIN R. G. BIOCHEMICAL ASPECTS OF GENETICS: THE OPERON. Annu Rev Biochem. 1964;33:235–258. doi: 10.1146/annurev.bi.33.070164.001315. [DOI] [PubMed] [Google Scholar]
  2. Achtman M., Mercer A., Kusecek B., Pohl A., Heuzenroeder M., Aaronson W., Sutton A., Silver R. P. Six widespread bacterial clones among Escherichia coli K1 isolates. Infect Immun. 1983 Jan;39(1):315–335. doi: 10.1128/iai.39.1.315-335.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BARRATT R. W., NEWMEYER D., PERKINS D. D., GARNJOBST L. Map construction in Neurospora crassa. Adv Genet. 1954;6:1–93. doi: 10.1016/s0065-2660(08)60127-3. [DOI] [PubMed] [Google Scholar]
  4. BECKWITH J. R., PARDEE A. B., AUSTRIAN R., JACOB F. Coordination of the synthesis of the enzymes in the pyrimidine pathway of E. coli. J Mol Biol. 1962 Dec;5:618–634. doi: 10.1016/s0022-2836(62)80090-4. [DOI] [PubMed] [Google Scholar]
  5. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bannister J. V., Parker M. W. The presence of a copper/zinc superoxide dismutase in the bacterium Photobacterium leiognathi: a likely case of gene transfer from eukaryotes to prokaryotes. Proc Natl Acad Sci U S A. 1985 Jan;82(1):149–152. doi: 10.1073/pnas.82.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beadle G. W., Tatum E. L. Genetic Control of Biochemical Reactions in Neurospora. Proc Natl Acad Sci U S A. 1941 Nov 15;27(11):499–506. doi: 10.1073/pnas.27.11.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Belfaiza J., Parsot C., Martel A., de la Tour C. B., Margarita D., Cohen G. N., Saint-Girons I. Evolution in biosynthetic pathways: two enzymes catalyzing consecutive steps in methionine biosynthesis originate from a common ancestor and possess a similar regulatory region. Proc Natl Acad Sci U S A. 1986 Feb;83(4):867–871. doi: 10.1073/pnas.83.4.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bobik T. A., Ailion M., Roth J. R. A single regulatory gene integrates control of vitamin B12 synthesis and propanediol degradation. J Bacteriol. 1992 Apr;174(7):2253–2266. doi: 10.1128/jb.174.7.2253-2266.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Botstein D. A theory of modular evolution for bacteriophages. Ann N Y Acad Sci. 1980;354:484–490. doi: 10.1111/j.1749-6632.1980.tb27987.x. [DOI] [PubMed] [Google Scholar]
  11. Boyd E. F., Nelson K., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic basis of allelic polymorphism in malate dehydrogenase (mdh) in natural populations of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1280–1284. doi: 10.1073/pnas.91.4.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brisson-Noël A., Arthur M., Courvalin P. Evidence for natural gene transfer from gram-positive cocci to Escherichia coli. J Bacteriol. 1988 Apr;170(4):1739–1745. doi: 10.1128/jb.170.4.1739-1745.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brückner R., Matzura H. In vivo synthesis of a polycistronic messenger RNA for the ribosomal proteins L11, L1, L10 and L7/12 in Escherichia coli. Mol Gen Genet. 1981;183(2):277–282. doi: 10.1007/BF00270629. [DOI] [PubMed] [Google Scholar]
  14. Buehner M., Ford G. C., Moras D., Olsen K. W., Rossman M. G. D-glyceraldehyde-3-phosphate dehydrogenase: three-dimensional structure and evolutionary significance. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3052–3054. doi: 10.1073/pnas.70.11.3052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Burland V., Plunkett G., 3rd, Daniels D. L., Blattner F. R. DNA sequence and analysis of 136 kilobases of the Escherichia coli genome: organizational symmetry around the origin of replication. Genomics. 1993 Jun;16(3):551–561. doi: 10.1006/geno.1993.1230. [DOI] [PubMed] [Google Scholar]
  16. Buvinger W. E., Lampel K. A., Bojanowski R. J., Riley M. Location and analysis of nucleotide sequences at one end of a putative lac transposon in the Escherichia coli chromosome. J Bacteriol. 1984 Aug;159(2):618–623. doi: 10.1128/jb.159.2.618-623.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Casjens S. Bacteriophage lambda FII gene protein: role in head assembly. J Mol Biol. 1974 Nov 25;90(1):1–20. doi: 10.1016/0022-2836(74)90252-6. [DOI] [PubMed] [Google Scholar]
  18. Crawford I. P. Evolution of a biosynthetic pathway: the tryptophan paradigm. Annu Rev Microbiol. 1989;43:567–600. doi: 10.1146/annurev.mi.43.100189.003031. [DOI] [PubMed] [Google Scholar]
  19. DEMEREC M., DEMEREC Z. E. Analysis of linkage relationships in Salmonella by transduction techniques. Brookhaven Symp Biol. 1956 Feb;(8):75–87. [PubMed] [Google Scholar]
  20. Demerec M., Blomstrand I., Demerec Z. E. EVIDENCE OF COMPLEX LOCI IN SALMONELLA. Proc Natl Acad Sci U S A. 1955 Jun 15;41(6):359–364. doi: 10.1073/pnas.41.6.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Desjardins P., Picard B., Kaltenböck B., Elion J., Denamur E. Sex in Escherichia coli does not disrupt the clonal structure of the population: evidence from random amplified polymorphic DNA and restriction-fragment-length polymorphism. J Mol Evol. 1995 Oct;41(4):440–448. doi: 10.1007/BF00160315. [DOI] [PubMed] [Google Scholar]
  22. Doolittle R. F., Feng D. F., Anderson K. L., Alberro M. R. A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J Mol Evol. 1990 Nov;31(5):383–388. doi: 10.1007/BF02106053. [DOI] [PubMed] [Google Scholar]
  23. Ebbole D. J., Zalkin H. Cloning and characterization of a 12-gene cluster from Bacillus subtilis encoding nine enzymes for de novo purine nucleotide synthesis. J Biol Chem. 1987 Jun 15;262(17):8274–8287. [PubMed] [Google Scholar]
  24. Fani R., Liò P., Chiarelli I., Bazzicalupo M. The evolution of the histidine biosynthetic genes in prokaryotes: a common ancestor for the hisA and hisF genes. J Mol Evol. 1994 May;38(5):489–495. doi: 10.1007/BF00178849. [DOI] [PubMed] [Google Scholar]
  25. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  26. GOLDSCHMIDT R. B. Chromosomes and genes. Cold Spring Harb Symp Quant Biol. 1951;16:1–11. doi: 10.1101/sqb.1951.016.01.003. [DOI] [PubMed] [Google Scholar]
  27. GORINI L., GUNDERSEN W., BURGER M. Genetics of regulation of enzyme synthesis in the arginine biosynthetic pathway of Escherichia coli. Cold Spring Harb Symp Quant Biol. 1961;26:173–182. doi: 10.1101/sqb.1961.026.01.022. [DOI] [PubMed] [Google Scholar]
  28. Green C. J., Vold B. S. Staphylococcus aureus has clustered tRNA genes. J Bacteriol. 1993 Aug;175(16):5091–5096. doi: 10.1128/jb.175.16.5091-5096.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Groisman E. A., Ochman H. Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J. 1993 Oct;12(10):3779–3787. doi: 10.1002/j.1460-2075.1993.tb06056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Guttman D. S., Dykhuizen D. E. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics. 1994 Dec;138(4):993–1003. doi: 10.1093/genetics/138.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. HARTMAN P. E., LOPER J. C., SERMAN D. Fine structure mapping by complete transduction between histidine-requiring Salmonella mutants. J Gen Microbiol. 1960 Apr;22:323–353. doi: 10.1099/00221287-22-2-323. [DOI] [PubMed] [Google Scholar]
  32. HOROWITZ N. H., LEUPOLD U. Some recent studies bearing on the one geneone enzyme hypothesis. Cold Spring Harb Symp Quant Biol. 1951;16:65–74. doi: 10.1101/sqb.1951.016.01.006. [DOI] [PubMed] [Google Scholar]
  33. Hardy S. J. The stoichiometry of the ribosomal proteins of Escherichia coli. Mol Gen Genet. 1975 Oct 3;140(3):253–274. doi: 10.1007/BF00334270. [DOI] [PubMed] [Google Scholar]
  34. Hartl D. L., Lozovskaya E. R., Lawrence J. G. Nonautonomous transposable elements in prokaryotes and eukaryotes. Genetica. 1992;86(1-3):47–53. doi: 10.1007/BF00133710. [DOI] [PubMed] [Google Scholar]
  35. Hildebrandt V., Ramezani-Rad M., Swida U., Wrede P., Grzesiek S., Primke M., Büldt G. Genetic transfer of the pigment bacteriorhodopsin into the eukaryote Schizosaccharomyces pombe. FEBS Lett. 1989 Jan 30;243(2):137–140. doi: 10.1016/0014-5793(89)80115-2. [DOI] [PubMed] [Google Scholar]
  36. Holloway B. W., Morgan A. F. Genome organization in Pseudomonas. Annu Rev Microbiol. 1986;40:79–105. doi: 10.1146/annurev.mi.40.100186.000455. [DOI] [PubMed] [Google Scholar]
  37. Holm L., Sander C. The FSSP database of structurally aligned protein fold families. Nucleic Acids Res. 1994 Sep;22(17):3600–3609. [PMC free article] [PubMed] [Google Scholar]
  38. Horowitz N. H. On the Evolution of Biochemical Syntheses. Proc Natl Acad Sci U S A. 1945 Jun;31(6):153–157. doi: 10.1073/pnas.31.6.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Howarth S. Suppressor Mutations in Some Cystine-Requiring Mutants of Salmonella Typhimurium. Genetics. 1958 May;43(3):404–418. doi: 10.1093/genetics/43.3.404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Hurst G. D., Hurst L. D., Majerus M. E. Evolutionary genetics. Selfish genes move sideways. Nature. 1992 Apr 23;356(6371):659–660. doi: 10.1038/356659a0. [DOI] [PubMed] [Google Scholar]
  41. Jeter R. M., Olivera B. M., Roth J. R. Salmonella typhimurium synthesizes cobalamin (vitamin B12) de novo under anaerobic growth conditions. J Bacteriol. 1984 Jul;159(1):206–213. doi: 10.1128/jb.159.1.206-213.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kepes A. Sequential transcription and translation in the lactose operon of Escherichia coli. Biochim Biophys Acta. 1967 Mar 29;138(1):107–123. doi: 10.1016/0005-2787(67)90591-6. [DOI] [PubMed] [Google Scholar]
  43. Kidwell M. G. Lateral transfer in natural populations of eukaryotes. Annu Rev Genet. 1993;27:235–256. doi: 10.1146/annurev.ge.27.120193.001315. [DOI] [PubMed] [Google Scholar]
  44. Klena J. D., Pradel E., Schnaitman C. A. The rfaS gene, which is involved in production of a rough form of lipopolysaccharide core in Escherichia coli K-12, is not present in the rfa cluster of Salmonella typhimurium LT2. J Bacteriol. 1993 Mar;175(5):1524–1527. doi: 10.1128/jb.175.5.1524-1527.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. LEE N., ENGLESBERG E. Dual effects of structural genes in Escherichia coli. Proc Natl Acad Sci U S A. 1962 Mar 15;48:335–348. doi: 10.1073/pnas.48.3.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. LEWIS E. B. Pseudoallelism and gene evolution. Cold Spring Harb Symp Quant Biol. 1951;16:159–174. doi: 10.1101/sqb.1951.016.01.014. [DOI] [PubMed] [Google Scholar]
  47. Lawrence J. G., Roth J. R. Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and reacquisition of a multigene complex. Genetics. 1996 Jan;142(1):11–24. doi: 10.1093/genetics/142.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lawrence J. G., Roth J. R. The cobalamin (coenzyme B12) biosynthetic genes of Escherichia coli. J Bacteriol. 1995 Nov;177(22):6371–6380. doi: 10.1128/jb.177.22.6371-6380.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lederberg E M. Allelic Relationships and Reverse Mutation in Escherichia Coli. Genetics. 1952 Sep;37(5):469–483. doi: 10.1093/genetics/37.5.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Levin B. R. Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics. 1981 Sep;99(1):1–23. doi: 10.1093/genetics/99.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Liu D., Reeves P. R. Presence of different O antigen forms in three isolates of one clone of Escherichia coli. Genetics. 1994 Sep;138(1):6–10. [PMC free article] [PubMed] [Google Scholar]
  52. Martin J., Webster R. E. The in vitro translation of a terminating signal by a single Escherichia coli ribosome. The fate of the subunits. J Biol Chem. 1975 Oct 25;250(20):8132–8139. [PubMed] [Google Scholar]
  53. Matsui K., Sano K., Ohtsubo E. Complete nucleotide and deduced amino acid sequences of the Brevibacterium lactofermentum tryptophan operon. Nucleic Acids Res. 1986 Dec 22;14(24):10113–10114. doi: 10.1093/nar/14.24.10113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Milkman R., Bridges M. M. Molecular evolution of the Escherichia coli chromosome. III. Clonal frames. Genetics. 1990 Nov;126(3):505–517. doi: 10.1093/genetics/126.3.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mitchell M. B. ABERRANT RECOMBINATION OF PYRIDOXINE MUTANTS OF Neurospora. Proc Natl Acad Sci U S A. 1955 Apr 15;41(4):215–220. doi: 10.1073/pnas.41.4.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Mitchell M. B., Mitchell H. K. The Selective Advantage of an Adenineless Double Mutant Over One of the Single Mutants Involved. Proc Natl Acad Sci U S A. 1950 Feb;36(2):115–119. doi: 10.1073/pnas.36.2.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Miyake T, Demerec M. Proline Mutants of Salmonella Typhimurium. Genetics. 1960 Jun;45(6):755–762. doi: 10.1093/genetics/45.6.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Médigue C., Rouxel T., Vigier P., Hénaut A., Danchin A. Evidence for horizontal gene transfer in Escherichia coli speciation. J Mol Biol. 1991 Dec 20;222(4):851–856. doi: 10.1016/0022-2836(91)90575-q. [DOI] [PubMed] [Google Scholar]
  59. NEWMEYER D. Arginine synthesis in Neurospora crassa; Genetic studies. J Gen Microbiol. 1957 Apr;16(2):449–462. doi: 10.1099/00221287-16-2-449. [DOI] [PubMed] [Google Scholar]
  60. Nolan C., Margoliash E. Comparative aspects of primary structures of proteins. Annu Rev Biochem. 1968;37:727–790. doi: 10.1146/annurev.bi.37.070168.003455. [DOI] [PubMed] [Google Scholar]
  61. Oppenheim D. S., Yanofsky C. Translational coupling during expression of the tryptophan operon of Escherichia coli. Genetics. 1980 Aug;95(4):785–795. doi: 10.1093/genetics/95.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Orengo C. A., Flores T. P., Taylor W. R., Thornton J. M. Identification and classification of protein fold families. Protein Eng. 1993 Jul;6(5):485–500. doi: 10.1093/protein/6.5.485. [DOI] [PubMed] [Google Scholar]
  63. Petrilli P. Classification of protein sequences by their dipeptide composition. Comput Appl Biosci. 1993 Apr;9(2):205–209. doi: 10.1093/bioinformatics/9.2.205. [DOI] [PubMed] [Google Scholar]
  64. ROPER J. A. Search for linkage between genes determining a vitamin requirement. Nature. 1950 Dec 2;166(4231):956–957. doi: 10.1038/166956b0. [DOI] [PubMed] [Google Scholar]
  65. Rambach A. New plate medium for facilitated differentiation of Salmonella spp. from Proteus spp. and other enteric bacteria. Appl Environ Microbiol. 1990 Jan;56(1):301–303. doi: 10.1128/aem.56.1.301-303.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Reeves P. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet. 1993 Jan;9(1):17–22. doi: 10.1016/0168-9525(93)90067-R. [DOI] [PubMed] [Google Scholar]
  67. Roth J. R., Lawrence J. G., Rubenfield M., Kieffer-Higgins S., Church G. M. Characterization of the cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium. J Bacteriol. 1993 Jun;175(11):3303–3316. doi: 10.1128/jb.175.11.3303-3316.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. SANDERSON K. E., DEMEREC M. THE LINKAGE MAP OF SALMONELLA TYPHIMURIUM. Genetics. 1965 Jun;51:897–913. doi: 10.1093/genetics/51.6.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. SMITH E. L., MARGOLIASH E. EVOLUTION OF CYTOCHROME C. Fed Proc. 1964 Nov-Dec;23:1243–1247. [PubMed] [Google Scholar]
  70. STEPHENS S. G. Possible significances of duplication in evolution. Adv Genet. 1951;4:247–265. doi: 10.1016/s0065-2660(08)60237-0. [DOI] [PubMed] [Google Scholar]
  71. STOKES J. L., BAYNE H. G. Growth-factor-dependent strains of Salmonellae. J Bacteriol. 1958 Oct;76(4):417–421. doi: 10.1128/jb.76.4.417-421.1958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Sanderson K. E., Hessel A., Rudd K. E. Genetic map of Salmonella typhimurium, edition VIII. Microbiol Rev. 1995 Jun;59(2):241–303. doi: 10.1128/mr.59.2.241-303.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Saxild H. H., Nygaard P. Gene-enzyme relationships of the purine biosynthetic pathway in Bacillus subtilis. Mol Gen Genet. 1988 Jan;211(1):160–167. doi: 10.1007/BF00338408. [DOI] [PubMed] [Google Scholar]
  74. Schmidt J., Bubunenko M., Subramanian A. R. A novel operon organization involving the genes for chorismate synthase (aromatic biosynthesis pathway) and ribosomal GTPase center proteins (L11, L1, L10, L12: rplKAJL) in cyanobacterium Synechocystis PCC 6803. J Biol Chem. 1993 Dec 25;268(36):27447–27457. [PubMed] [Google Scholar]
  75. Selander R. K., Levin B. R. Genetic diversity and structure in Escherichia coli populations. Science. 1980 Oct 31;210(4469):545–547. doi: 10.1126/science.6999623. [DOI] [PubMed] [Google Scholar]
  76. Shanley M. S., Harrison A., Parales R. E., Kowalchuk G., Mitchell D. J., Ornston L. N. Unusual G + C content and codon usage in catIJF, a segment of the ben-cat supra-operonic cluster in the Acinetobacter calcoaceticus chromosome. Gene. 1994 Jan 28;138(1-2):59–65. doi: 10.1016/0378-1119(94)90783-8. [DOI] [PubMed] [Google Scholar]
  77. Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Smith J. M., Smith N. H., O'Rourke M., Spratt B. G. How clonal are bacteria? Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384–4388. doi: 10.1073/pnas.90.10.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Spencer J. B., Stolowich N. J., Roessner C. A., Scott A. I. The Escherichia coli cysG gene encodes the multifunctional protein, siroheme synthase. FEBS Lett. 1993 Nov 29;335(1):57–60. doi: 10.1016/0014-5793(93)80438-z. [DOI] [PubMed] [Google Scholar]
  80. Stahl F. W., Murray N. E. The evolution of gene clusters and genetic circularity in microorganisms. Genetics. 1966 Mar;53(3):569–576. doi: 10.1093/genetics/53.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Stevenson G., Neal B., Liu D., Hobbs M., Packer N. H., Batley M., Redmond J. W., Lindquist L., Reeves P. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. J Bacteriol. 1994 Jul;176(13):4144–4156. doi: 10.1128/jb.176.13.4144-4156.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Subramanian A. R. Copies of proteins L7 and L12 and heterogeneity of the large subunit of Escherichia coli ribosome. J Mol Biol. 1975 Jun 15;95(1):1–8. doi: 10.1016/0022-2836(75)90330-7. [DOI] [PubMed] [Google Scholar]
  83. Syvanen M. Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet. 1994;28:237–261. doi: 10.1146/annurev.ge.28.120194.001321. [DOI] [PubMed] [Google Scholar]
  84. Whitfield H. J., Jr, Gutnick D. L., Margolies M. N., Martin R. G., Rechler M. M., Voll M. J. Relative translation frequencies of the cistrons of the histidine operon. J Mol Biol. 1970 Apr 14;49(1):245–249. doi: 10.1016/0022-2836(70)90391-8. [DOI] [PubMed] [Google Scholar]
  85. Whittam T. S., Ochman H., Selander R. K. Geographic components of linkage disequilibrium in natural populations of Escherichia coli. Mol Biol Evol. 1983 Dec;1(1):67–83. doi: 10.1093/oxfordjournals.molbev.a040302. [DOI] [PubMed] [Google Scholar]
  86. Woehlke G., Wifling K., Dimroth P. Sequence of the sodium ion pump oxaloacetate decarboxylase from Salmonella typhimurium. J Biol Chem. 1992 Nov 15;267(32):22798–22803. [PubMed] [Google Scholar]
  87. YANOFSKY C., LENNOX E. S. Transduction and recombination study of linkage relationships among the genes controlling tryptophan synthesis in Escherichia coli. Virology. 1959 Aug;8:425–447. doi: 10.1016/0042-6822(59)90046-7. [DOI] [PubMed] [Google Scholar]
  88. van de Guchte M., Kok J., Venema G. Distance-dependent translational coupling and interference in Lactococcus lactis. Mol Gen Genet. 1991 May;227(1):65–71. doi: 10.1007/BF00260708. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES