Article thumbnail

Fate of the H-NS–Repressed bgl Operon in Evolution of Escherichia coli

By T. Sabari Sankar, Girish Neelakanta, Vartul Sangal, Georg Plum, Mark Achtman and Karin Schnetz


In the enterobacterial species Escherichia coli and Salmonella enterica, expression of horizontally acquired genes with a higher than average AT content is repressed by the nucleoid-associated protein H-NS. A classical example of an H-NS–repressed locus is the bgl (aryl-β,D-glucoside) operon of E. coli. This locus is “cryptic,” as no laboratory growth conditions are known to relieve repression of bgl by H-NS in E. coli K12. However, repression can be relieved by spontaneous mutations. Here, we investigated the phylogeny of the bgl operon. Typing of bgl in a representative collection of E. coli demonstrated that it evolved clonally and that it is present in strains of the phylogenetic groups A, B1, and B2, while it is presumably replaced by a cluster of ORFans in the phylogenetic group D. Interestingly, the bgl operon is mutated in 20% of the strains of phylogenetic groups A and B1, suggesting erosion of bgl in these groups. However, bgl is functional in almost all B2 isolates and, in approximately 50% of them, it is weakly expressed at laboratory growth conditions. Homologs of bgl genes exist in Klebsiella, Enterobacter, and Erwinia species and also in low GC-content Gram-positive bacteria, while absent in E. albertii and Salmonella sp. This suggests horizontal transfer of bgl genes to an ancestral Enterobacterium. Conservation and weak expression of bgl in isolates of phylogenetic group B2 may indicate a functional role of bgl in extraintestinal pathogenic E. coli

Topics: Research Article
Publisher: Public Library of Science
OAI identifier:
Provided by: PubMed Central

Suggested articles


  1. (1986). A
  2. (2005). A cis-spreading nucleoprotein filament is responsible for the gene silencing activity found in the promoter relay mechanism.
  3. (2007). A congruence index for testing topological similarity between trees.
  4. (1996). A mutation in a new gene, bglJ, activates the bgl operon in Escherichia coli K-12.
  5. (2004). Aballay A
  6. (1990). Analysis of the Erwinia chrysanthemi arb genes, which mediate metabolism of aromatic b-glucosides.
  7. (1987). b-Glucoside (bgl) operon of Escherichia coli K-12: nucleotide sequence, genetic organization, and possible evolutionary relationship to regulatory components of two Bacillus subtilis genes.
  8. (2008). Carbon catabolite repression in bacteria: many ways to make the most out of nutrients.
  9. (2008). Characterization of a yjjQ mutant of avian pathogenic E. coli (APEC).
  10. (1997). Characterization of the negative elements involved in silencing the bgl operon of Escherichia coli: possible roles for DNA gyrase, H-NS, and CRP-cAMP in regulation.
  11. (2006). Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli.
  12. (2001). Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12.
  13. (1981). Correlation between uropathogenic properties of Escherichia coli from urinary tract infections and the antibody-coated bacteria test and comparison with faecal strains.
  14. (2004). Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study.
  15. (2008). Enhanced expression ofthe bgloperon of Escherichia coli in the stationary phase.
  16. (2006). Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA Polymerase.
  17. (1977). Esculin hydrolysis by Enterobacteriaceae.
  18. (2005). Evolutionary origins of genomic repertoires in bacteria.
  19. (2002). Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli.
  20. (2001). Genome sequence of enterohaemorrhagic Escherichia coli O157:H7.
  21. (2005). Genome variations in commensal and pathogenic E.
  22. (2004). Genomic islands in pathogenic and environmental microorganisms.
  23. (2007). Go ¨rke B
  24. (2007). H-NS, the genome sentinel.
  25. (2004). H-NS: a universal regulator for a dynamic genome.
  26. (1991). Hafnia alvei, a probable cause of diarrhea in humans.
  27. (2006). How to become a uropathogen: Comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains.
  28. (1998). In vivo expression of the b-glucoside (bgl) operon of Escherichia coli occurs in mouse liver.
  29. (2005). Independent regulation of H-NS mediated silencing of the bgl operon at two levels: upstream by BglJ and LeuO and downstream by DnaKJ.
  30. (1967). Inducible System for the Utilization of b-Glucosides in Escherichia coli. I. Active Transport and Utilization of b-Glucosides.
  31. (1967). Inducible System for the Utilization of bGlucosides in Escherichia coli II. Description of mutant types and genetic analysis.
  32. (2008). Microbial diversity and the genetic nature of microbial species.
  33. (1998). Molecular archaeology of the Escherichia coli genome.
  34. (2006). Multi locus Sequence Typing of Bacteria.
  35. (2005). Mutations that activate the silent bgl operon of Escherichia coli confer a growth advantage in stationary phase.
  36. (1987). Positive and negative regulation of the bgl operon in Escherichia coli.
  37. (1998). PRD - a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria.
  38. (1999). Recruitment of ZipA to the division site by interaction with FtsZ.
  39. (1974). Regulation of the b-glucoside system in Escherichia coli K12.
  40. (2003). Regulation of the Escherichia coli Antiterminator Protein BglG by Phosphorylation at Multiple Sites and Evidence for Transfer of Phosphoryl Groups between Monomers.
  41. (2008). Regulation of the yjjQ-bglJ operon, encoding LuxR-type transcription factors, and the divergent yjjP gene by H-NS and LeuO.
  42. (2007). Repression by binding of H-NS within the transcription unit.
  43. (1983). Role of cryptic genes in microbial evolution.
  44. (2006). Salmonella enterica serovar Typhimurium ompS1 and ompS2 mutants are attenuated for virulence in mice.
  45. (2006). Sex and virulence in Escherichia coli: an evolutionary perspective.
  46. (1995). Silencing of Escherichia coli bgl promoter by flanking sequence elements.
  47. (2007). Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA.
  48. (1984). Standard reference strains of Escherichia coli from natural populations.
  49. (2007). tDNA locus polymorphism and ecto-chromosomal DNA insertion hot-spots are related to the phylogenetic group of Escherichia coli strains.
  50. (2003). The b-glucoside genes of Klebsiella aerogenes: conservation and divergence in relation to the cryptic bgl genes of Escherichia coli.
  51. (1997). The complete genome sequence of Escherichia coli K-12.
  52. (2003). The Evolutionary History of Shigella and Enteroinvasive Escherichia coli.
  53. (1999). The gene bglH present in the bgl operon of Escherichia coli, responsible for uptake and fermentation of b-glucosides encodes for a carbohydrate-specific outer membrane porin.
  54. (2004). The histone-like nucleoid structuring protein H-NS represses the Escherichia coli bgl operon downstream of the promoter.
  55. (2007). The integrated microbial genomes (IMG) system in 2007: data content and analysis tool extensions.
  56. (2008). The LysR-Type Transcriptional Regulator LeuO Controls Expression of Several Genes in Salmonella enterica Serovar Typhi.
  57. (2008). The Universal Protein Resource (UniProt).
  58. Ueguchi C,Ohta T,SetoC,SuzukiT,MizunoT (1998)The leuOgene-producthas a latent ability to relieve the bgl silencing in Escherichia coli.
  59. (2008). Unraveling the evolutionary history of the phosphoryl-transfer chain of the phosphoenolpyruvate:phosphotransferase system through phylogenetic analyses and genome context.
  60. (1980). Uropathogenic properties of Escherichia coli in recurrent urinary-tract infection.
  61. (1988). Widespread distribution of deletions of the bgl operon in natural isolates of Escherichia coli.

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.