Genomics, Biological Features, and Biotechnological Applications of Escherichia coli B: “Is B for better?!”

  • Sung Ho Yoon
  • Haeyoung Jeong
  • Soon-Kyeong Kwon
  • Jihyun F. Kim

Abstract

Strains of Escherichia coli B, especially BL21, have been widely used for overproducing recombinant proteins, ethanol, and other biomolecules. Almost all laboratory strains of E. coli are derivatives of non-pathogenic K-12 or B strains. While most genetic and metabolic studies have been performed with K-12 strains, little has been done on B strains. Recently, genome sequences of two E. coli strains of the B lineage, REL606 and BL21(DE3), have been determined, and results of multi-omics analyses were compared between B and K-12. As compared to K-12, B strains show a number of phenotypes such as faster growth in minimal media, lower acetate production, higher expression levels of recombinant proteins, and less degradation of such proteins during purification. In this review, we summarize the unique biological features of the B strains and overview their academic and industrial applications.

Keywords

Permeability Fermentation Polysaccharide Proline Arginine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Blanco, M., A. Urios, and A. Martinez. 1998. New Escherichia coli WP2 tester strains highly sensitive to reversion by oxidative mutagens. Mutat. Res. 413:95–101.PubMedGoogle Scholar
  2. Blattner, F. R., G. Plunkett, 3rd, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–74.PubMedCrossRefGoogle Scholar
  3. Boulter, J., B. Gielow, M. McFarland, and N. Lee. 1974. Metabolism of D-arabinose by Escherichia coli B/r. J. Bacteriol. 117:920–3.PubMedGoogle Scholar
  4. Cha, H. J., R. Srivastava, V. N. Vakharia, G. Rao, and W. E. Bentley. 1999. Green fluorescent protein as a noninvasive stress probe in resting Escherichia coli cells. Appl. Environ. Microbiol. 65:409–14.PubMedGoogle Scholar
  5. Choi, J. H., K. C. Keum, and S. Y. Lee. 2006. Production of recombinant proteins by high cell density culture of Escherichia coli. Chem. Eng. Sci. 61:876–85.CrossRefGoogle Scholar
  6. Choi, J. H., S. J. Lee, and S. Y. Lee. 2003. Enhanced production of insulin-like growth factor I fusion protein in Escherichia coli by coexpression of the down-regulated genes identified by transcriptome profiling. Appl. Environ. Microbiol. 69:4737–42.PubMedCrossRefGoogle Scholar
  7. Cooper, T. F., D. E. Rozen, and R. E. Lenski. 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl. Acad. Sci. USA 100:1072–7.PubMedCrossRefGoogle Scholar
  8. Cooper, V. S., and R. E. Lenski. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:736–9.PubMedCrossRefGoogle Scholar
  9. Covert, M. W., E. M. Knight, J. L. Reed, M. J. Herrgard, and B. O. Palsson. 2004. Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92–6.PubMedCrossRefGoogle Scholar
  10. Daegelen, P., F. W. Studier, R. E. Lenski, S. Cure, and J. F. Kim. Tracing ancestors and relatives of Escherichia coli B, and the derivation of B strains REL606 and BL21(DE3). submitted.Google Scholar
  11. de Crecy, E., D. Metzgar, C. Allen, M. Penicaud, B. Lyons, C. J. Hansen, and V. de Crecy-Lagard. 2007. Development of a novel continuous culture device for experimental evolution of bacterial populations. Appl. Microbiol. Biotechnol. 77:489–96.PubMedCrossRefGoogle Scholar
  12. Delbruck, M. 1946. Bacterial viruses or bacteriophages. Biol. Rev. 21:30–40.CrossRefGoogle Scholar
  13. Delbruck, M., and S. E. Luria. 1942. Interference between bacterial viruses. I. Interference between two bacterial viruses acting upon the same host, and the mechanism of virus growth. Arch. Biochem. 1:111–41.Google Scholar
  14. Diaz, E., A. Ferrandez, M. A. Prieto, and J. L. Garcia. 2001. Biodegradation of aromatic compounds by Escherichia coli. Microbiol. Mol. Biol. Rev. 65:523–69.PubMedCrossRefGoogle Scholar
  15. Dumon-Seignovert, L., G. Cariot, and L. Vuillard. 2004. The toxicity of recombinant proteins in Escherichia coli: a comparison of overexpression in BL21(DE3), C41(DE3), and C43(DE3). Protein Expr. Purif. 37:203–6.PubMedCrossRefGoogle Scholar
  16. Eiteman, M. A., and E. Altman. 2006. Overcoming acetate in Escherichia coli recombinant protein fermentations. Trends Biotechnol. 24:530–6.PubMedCrossRefGoogle Scholar
  17. Elena, S. F., and R. E. Lenski. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457–69.PubMedCrossRefGoogle Scholar
  18. Elsinghorst, E. A., and R. P. Mortlock. 1994. Molecular cloning of the Escherichia coli B L-fucose-D-arabinose gene cluster. J. Bacteriol. 176:7223–32.PubMedGoogle Scholar
  19. Feist, A. M., C. S. Henry, J. L. Reed, M. Krummenacker, A. R. Joyce, P. D. Karp, L. J. Broadbelt, V. Hatzimanikatis, and B. O. Palsson. 2007. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3:121.PubMedCrossRefGoogle Scholar
  20. Fong, S. S., A. P. Burgard, C. D. Herring, E. M. Knight, F. R. Blattner, C. D. Maranas, and B. O. Palsson. 2005. In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol. Bioeng. 91:643–8.PubMedCrossRefGoogle Scholar
  21. Francetic, O., D. Belin, C. Badaut, and A. P. Pugsley. 2000. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. Embo J. 19: 6697–703.PubMedCrossRefGoogle Scholar
  22. Franchini, A. G., and T. Egli. 2006. Global gene expression in Escherichia coli K-12 during short-term and long-term adaptation to glucose-limited continuous culture conditions. Microbiology 152:2111–27.PubMedCrossRefGoogle Scholar
  23. Gatehouse, D., S. Haworth, T. Cebula, E. Gocke, L. Kier, T. Matsushima, C. Melcion, T. Nohmi, T. Ohta, S. Venitt, et al. 1994. Recommendations for the performance of bacterial mutation assays. Mutat. Res. 312:217–33.PubMedGoogle Scholar
  24. Gross, C. A. 1996. Function and regulation of the heat shock proteins. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, D. Schneider, and H. E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC, pp. 1382–99.Google Scholar
  25. Haeusser, D. P., and P. A. Levin. 2008. The great divide: coordinating cell cycle events during bacterial growth and division. Curr. Opin. Microbiol. 11:94–9.PubMedCrossRefGoogle Scholar
  26. Han, M. J., and S. Y. Lee. 2006. The Escherichia coli proteome: past, present, and future prospects. Microbiol. Mol. Biol. Rev. 70:362–439.PubMedCrossRefGoogle Scholar
  27. Harder, K. J., H. Nikaido, and M. Matsuhashi. 1981. Mutants of Escherichia coli that are resistant to certain beta-lactam compounds lack the ompF porin. Antimicrob. Agents Chemother. 20:549–52.PubMedGoogle Scholar
  28. Hayashi, K., N. Morooka, Y. Yamamoto, K. Fujita, K. Isono, S. Choi, E. Ohtsubo, T. Baba, B. L. Wanner, H. Mori, and T. Horiuchi. 2006. Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol. Syst. Biol. 2:2006 0007.PubMedCrossRefGoogle Scholar
  29. Helmstetter, C. E. 1968. DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J. Mol. Biol. 31:507–18.PubMedCrossRefGoogle Scholar
  30. Herrera, G., A. Martinez, M. Blanco, and J. E. O’Connor. 2002. Assessment of Escherichia coli B with enhanced permeability to fluorochromes for flow cytometric assays of bacterial cell function. Cytometry 49:62–9.PubMedCrossRefGoogle Scholar
  31. Herrera, G., A. Urios, V. Aleixandre, and M. Blanco. 1993. Mutability by polycyclic hydrocarbons is improved in derivatives of Escherichia coli WP2 uvrA with increased permeability. Mutat. Res. 301:1–5.PubMedCrossRefGoogle Scholar
  32. Ishii, N., K. Nakahigashi, T. Baba, M. Robert, T. Soga, A. Kanai, T. Hirasawa, M. Naba, K. Hirai, A. Hoque, P. Y. Ho, Y. Kakazu, K. Sugawara, S. Igarashi, S. Harada, T. Masuda, N. Sugiyama, T. Togashi, M. Hasegawa, Y. Takai, K. Yugi, K. Arakawa, N. Iwata, Y. Toya, Y. Nakayama, T. Nishioka, K. Shimizu, H. Mori, and M. Tomita. 2007. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316:593–7.Google Scholar
  33. Jansson, P. E., A. A. Lindberg, B. Lindberg, and R. Wollin. 1981. Structural studies on the hexose region of the core in lipopolysaccharides from Enterobacteriaceae. Eur. J. Biochem. 115:571–7.PubMedCrossRefGoogle Scholar
  34. Jensen, K. F. 1993. The Escherichia coli K-12 “wild types” W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J. Bacteriol. 175:3401–7.PubMedGoogle Scholar
  35. Jeong, H., V. Barbe, D. Vallenet, S.-H. Choi, C. H. Lee, S.-W. Lee, B. Vacherie, S. H. Yoon, D.-S. Yu, L. Cattolico, C.-G. Hur, H.-S. Park, B. Sègurens, M. Blot, D. Schneider, F. W. Studier, S. C. Kim, T. K. Oh, R. E. Lenski, P. Daegelen, and J. F. Kim. Genome sequencing and comparative analysis of Escherichia coli B REL606 and BL21(DE3). submitted.Google Scholar
  36. Jeong, K. J., and S. Y. Lee. 2002. Excretion of human beta-endorphin into culture medium by using outer membrane protein F as a fusion partner in recombinant Escherichia coli. Appl. Environ. Microbiol. 68:4979–85.PubMedCrossRefGoogle Scholar
  37. LeBlanc, D. J., and R. P. Mortlock. 1971. Metabolism of D-arabinose: a new pathway in Escherichia coli. J. Bacteriol. 106:90–6.PubMedGoogle Scholar
  38. Lederberg, J. 2004. E. coli K-12. Microbiol. Today 31:116.Google Scholar
  39. Lederberg, S. 1966. Genetics of host-controlled restriction and modification of deoxyribonucleic acid in Escherichia coli. J. Bacteriol. 91:1029–36.PubMedGoogle Scholar
  40. Legrain, C., V. Stalon, and N. Glansdorff. 1976. Escherichia coli ornithine carbamolytransferase isoenzymes: evolutionary significance and the isolation of λ argF and λ argI transducing bacteriophages. J. Bacteriol. 128:35–8.PubMedGoogle Scholar
  41. Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138.Google Scholar
  42. Michelsen, O., M. J. Teixeira de Mattos, P. R. Jensen, and F. G. Hansen. 2003. Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149:1001–10.PubMedCrossRefGoogle Scholar
  43. Miroux, B., and J. E. Walker. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260:289–98.PubMedCrossRefGoogle Scholar
  44. Nandakumar, M. P., A. Cheung, and M. R. Marten. 2006. Proteomic analysis of extracellular proteins from Escherichia coli W3110. J. Proteome Res. 5:1155–61.PubMedCrossRefGoogle Scholar
  45. Neidhardt, F. C., and H. E. Umbarger. 1996. Chemical composition of Escherichia coli. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, D. Schneider, and H. E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC, pp. 13–16.Google Scholar
  46. Neijssel, O. M., M. J. Teixeira de Mattos, and D. W. Tempest. 1996. Growth yield and energy distribution. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, D. Schneider, and H. E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC, pp. 1683–92.Google Scholar
  47. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593–656.PubMedCrossRefGoogle Scholar
  48. Nikaido, H. 1996. Outer membrane. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, D. Schneider, and H. E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC, pp. 29–47.Google Scholar
  49. Philippe, N., E. Crozat, R. E. Lenski, and D. Schneider. 2007. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29:846–60.PubMedCrossRefGoogle Scholar
  50. Phue, J. N., B. Kedem, P. Jaluria, and J. Shiloach. 2007. Evaluating microarrays using a semiparametric approach: application to the central carbon metabolism of Escherichia coli BL21 and JM109. Genomics 89:300–5.PubMedCrossRefGoogle Scholar
  51. Phue, J. N., S. B. Noronha, R. Hattacharyya, A. J. Wolfe, and J. Shiloach. 2005. Glucose metabolism at high density growth of E. coli B and E. coli K: differences in metabolic pathways are responsible for efficient glucose utilization in E. coli B as determined by microarrays and Northern blot analyses. Biotechnol. Bioeng. 90:805–20.PubMedCrossRefGoogle Scholar
  52. Pieper, D. H., and W. Reineke. 2000. Engineering bacteria for bioremediation. Curr. Opin. Biotechnol. 11:262–70.PubMedCrossRefGoogle Scholar
  53. Posfai, G., G. Plunkett, 3rd, T. Feher, D. Frisch, G. M. Keil, K. Umenhoffer, V. Kolisnychenko, B. Stahl, S. S. Sharma, M. de Arruda, V. Burland, S. W. Harcum, and F. R. Blattner. 2006. Emergent properties of reduced-genome Escherichia coli. Science 312:1044–6.PubMedCrossRefGoogle Scholar
  54. Pugsley, A. P., and J. P. Rosenbusch. 1983. OmpF porin synthesis in Escherichia coli strains B and K-12 carrying heterologous ompB and/or ompF loci. FEMS Microbiol. Lett. 16:143–47.CrossRefGoogle Scholar
  55. saiSree, L., M. Reddy, and J. Gowrishankar. 2001. IS186 insertion at a hot spot in the lon promoter as a basis for Lon protease deficiency of Escherichia coli B: identification of a consensus target sequence for IS186 transposition. J. Bacteriol. 183:6943–6.PubMedCrossRefGoogle Scholar
  56. Sauer, U. 2001. Evolutionary engineering of industrially important microbial phenotypes. Adv. Biochem. Eng. Biotechnol. 73:129–69.PubMedGoogle Scholar
  57. Schneider, D., E. Duperchy, J. Depeyrot, E. Coursange, R. Lenski, and M. Blot. 2002. Genomic comparisons among Escherichia coli strains B, K-12, and O157:H7 using IS elements as molecular markers. BMC Microbiol. 2:18.PubMedCrossRefGoogle Scholar
  58. Seo, J. H., D. G. Kang, and H. J. Cha. 2003. Comparison of cellular stress levels and green-fluorescent-protein expression in several Escherichia coli strains. Biotechnol. Appl. Biochem. 37:103–7.PubMedCrossRefGoogle Scholar
  59. Sorensen, H. P., and K. K. Mortensen. 2005. Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol. 115:113–28.PubMedCrossRefGoogle Scholar
  60. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113–30.PubMedCrossRefGoogle Scholar
  61. Swartz, J. R. 1996. Escherichia coli recombinant DNA technology. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Shaechter, and H. E. Umbarger (eds.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC, pp. 1693–1712.Google Scholar
  62. Tian, G., D. Lim, J. D. Oppenheim, and W. K. Maas. 1994. Explanation for different types of regulation of arginine biosynthesis in Escherichia coli B and Escherichia coli K12 caused by a difference between their arginine repressors. J. Mol. Biol. 235:221–30.PubMedCrossRefGoogle Scholar
  63. Tsilibaris, V., G. Maenhaut-Michel, and L. Van Melderen. 2006. Biological roles of the Lon ATP-dependent protease. Res. Microbiol. 157:701–13.PubMedCrossRefGoogle Scholar
  64. Umbarger, H. E. 1996. Biosynthesis of the branched-chain amino acids. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, D. Schneider, and H. E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. ASM Press, Washington, DC, pp. 442–57.Google Scholar
  65. Vallenet, D., L. Labarre, Z. Rouy, V. Barbe, S. Bocs, S. Cruveiller, A. Lajus, G. Pascal, C. Scarpelli, and C. Medigue. 2006. MaGe: a microbial genome annotation system supported by synteny results. Nucl. Acids Res. 34:53–65.PubMedCrossRefGoogle Scholar
  66. Vostiar, I., J. Tkac, and C. F. Mandenius. 2004. Off-line monitoring of bacterial stress response during recombinant protein production using an optical biosensor. J. Biotechnol. 111:191–201.PubMedCrossRefGoogle Scholar
  67. Wilcox, P., A. Naidoo, D. J. Wedd, and D. G. Gatehouse. 1990. Comparison of Salmonella typhimurium TA102 with Escherichia coli WP2 tester strains. Mutagenesis 5:285–91.PubMedCrossRefGoogle Scholar
  68. Witkin, E. M. 1946. Inherited differences in sensitivity to radiation in Escherichia coli. Proc. Natl. Acad. Sci. USA 32:59–68.PubMedCrossRefGoogle Scholar
  69. Xia, X. X., M. J. Han, S. Y. Lee, and J. S. Yoo. 2008. Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation. Proteomics 8:2089–103.PubMedCrossRefGoogle Scholar
  70. Yoon, S. H., M. J. Han, H. Jeong, C. H. Lee, X. X. Xia, J. H. Shim, S. Y. Lee, T. K. Oh, and J. F. Kim. Comparative multi-omics systems analysis of closely related Escherichia coli strains. submitted.Google Scholar
  71. Yoon, S. H., M. J. Han, S. Y. Lee, K. J. Jeong, and J. S. Yoo. 2003. Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol. Bioeng. 81:753–67.PubMedCrossRefGoogle Scholar
  72. Yoon, S. H., C. G. Hur, H. Y. Kang, Y. H. Kim, T. K. Oh, and J. F. Kim. 2005. A computational approach for identifying pathogenicity islands in prokaryotic genomes. BMC Bioinformatics 6:184.PubMedCrossRefGoogle Scholar
  73. Yu, B. J., B. H. Sung, M. D. Koob, C. H. Lee, J. H. Lee, W. S. Lee, M. S. Kim, and S. C. Kim. 2002. Minimization of the Escherichia coli genome using a Tn5-targeted Cre/loxP excision system. Nat. Biotechnol. 20:1018–23.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Sung Ho Yoon
    • 1
  • Haeyoung Jeong
    • 1
  • Soon-Kyeong Kwon
    • 1
  • Jihyun F. Kim
    • 2
    • 3
  1. 1.Systems Microbiology Research CenterKorea Research Institute of Bioscience and Biotechnology (KRIBB)Yuseong-guRepublic of Korea
  2. 2.Industrial Biotechnology and Bioenergy Research CenterKorea Research Institute of Bioscience and Biotechnology (KRIBB)YuseongRepublic of Korea
  3. 3.Field of Functional Genomics, School of ScienceUniversity of Science and Technology (UST)YuseongRepublic of Korea

Personalised recommendations