Skip to main content

Experimental Evolution of an Essential Bacillus Gene in an E. coli Host

  • Protocol
Horizontal Gene Transfer

Part of the book series: Methods in Molecular Biology ((MIMB,volume 532))

Abstract

The acquisition of foreign genes by HGT potentially greatly speeds up adaptation by allowing faster evolution of beneficial traits. The evolutionary integration of novel genes into host gene expression and physiology is critical for adaptation by HGT, but remains largely unknown. We are exploring the evolutionary consequences of gene acquisition in populations of Escherichia coli in real time. A plasmid bearing the genes necessary for sucrose catabolism was constructed and introduced into a single E. coli genotype. Wild-type E. coli is generally incapable of utilizing sucrose, but E. coli transformants were able to grow on sucrose as a sole carbon and energy source, albeit poorly. Twelve replicate populations were initiated and propagated in sucrose minimal media for 300 generations. Over this time, we observed large fitness improvements in the selected environment. These results demonstrate the potential for HGT to substantially increase microbial niche breadth.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ochman, H., Lawrence, J.G., Groisman, E.A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.

    Article  CAS  PubMed  Google Scholar 

  2. Koonin, E.V., Makarova, K.S., Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol., 55, 709–742.

    Article  CAS  PubMed  Google Scholar 

  3. Lawrence, J.G., Ochman, H. (1998). Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. U. S. A, 95, 9413–9417.

    Article  CAS  PubMed  Google Scholar 

  4. Cortez, D.Q., Lazcano, A., Becerra, A. (2005). Comparative analysis of methodologies for the detection of horizontally transferred genes: a reassessment of first-order Markov models. In Silico. Biol., 5, 581–592.

    CAS  PubMed  Google Scholar 

  5. Romero, D., Palacios, R. (1997). Gene amplification and genomic plasticity in prokaryotes. Annu. Rev. Genet., 31, 91–111.

    Article  CAS  PubMed  Google Scholar 

  6. Spratt, B.G., Hanage, W.P., Feil, E.J. (2001). The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr. Opin. Microbiol., 4, 602–606.

    Article  CAS  PubMed  Google Scholar 

  7. Koonin, E.V., Galperin, M.Y. (1997). Prokaryotic genomes: the emerging paradigm of genome-based microbiology. Curr. Opin. Genet. Dev., 7, 757–763.

    Article  CAS  PubMed  Google Scholar 

  8. Lawrence, J.G., Ochman, H. (1997). Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol., 44, 383–397.

    Article  CAS  PubMed  Google Scholar 

  9. Lawrence, J.G. (1999). Gene transfer, speciation, and the evolution of bacterial genomes. Curr. Opin. Microbiol., 2, 519–523.

    Article  CAS  PubMed  Google Scholar 

  10. Aravind, L., Tatusov, R.L., Wolf, Y.I., Walker, D.R., Koonin, E.V. (1998). Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet., 14, 442–444.

    Article  CAS  PubMed  Google Scholar 

  11. Huynen, M.A., Bork, P. (1998). Measuring genome evolution. Proc. Natl. Acad. Sci. U. S. A, 95, 5849–5856.

    Article  CAS  PubMed  Google Scholar 

  12. Doolittle, W.F. (1999). Phylogenetic classification and the universal tree. Science, 284, 2124–2129.

    Article  CAS  PubMed  Google Scholar 

  13. Doolittle, W.F. (2000). The nature of the universal ancestor and the evolution of the proteome. Curr. Opin. Struct. Biol., 10, 355–358.

    Article  CAS  PubMed  Google Scholar 

  14. Woese, C.R. (2000). Interpreting the universal phylogenetic tree. Proc. Natl. Acad. Sci. U. S. A. 97, 8392–8396.

    Article  CAS  PubMed  Google Scholar 

  15. Gogarten, J.P., Doolittle, W.F., Lawrence, J.G. (2002). Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol., 19, 2226–2238.

    CAS  PubMed  Google Scholar 

  16. de la, Cruz, F., Davies, J. (2000). Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol., 8, 128–133.

    Article  CAS  PubMed  Google Scholar 

  17. Scholten, J.C., Culley, D.E., Brockman, F.J., Wu, G., Zhang, W. (2007). Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: Involvement of an ancient horizontal gene transfer. Biochem. Biophys. Res. Commun., 352, 48–54.

    Article  CAS  PubMed  Google Scholar 

  18. Rosas-Magallanes, V., Deschavanne, P., Quintana-Murci, L., Brosch, R., Gicquel, B., Neyrolles, O. (2006). Horizontal transfer of a virulence operon to the ancestor of Mycobacterium tuberculosis. Mol. Biol. Evol., 23, 1129–1135.

    Article  CAS  PubMed  Google Scholar 

  19. Walsh, T.R. (2006). Combinatorial genetic evolution of multiresistance. Curr. Opin. Microbiol., 9, 476–482.

    Article  CAS  PubMed  Google Scholar 

  20. Wertz, J.E., Riley, M.A. (2004). Chimeric nature of two plasmids of Hafnia alvei encoding the bacteriocins alveicins A and B. J. Bacteriol., 186, 1598–1605.

    Article  CAS  PubMed  Google Scholar 

  21. van der Meer, J.R., Sentchilo, V. (2003). Genomic islands and the evolution of catabolic pathways in bacteria. Curr. Opin. Biotechnol., 14, 248–254.

    Article  PubMed  Google Scholar 

  22. O’Driscoll, J., Glynn, F., Fitzgerald, G.F., van Sinderen, D. (2006). Sequence analysis of the lactococcal plasmid pNP40: a mobile replicon for coping with environmental hazards. J. Bacteriol., 188, 6629–6639.

    Article  PubMed  Google Scholar 

  23. Kunin, V., Goldovsky, L., Darzentas, N., Ouzounis, C.A. (2005). The net of life: reconstructing the microbial phylogenetic network. Genome Res., 15, 954–959.

    Article  CAS  PubMed  Google Scholar 

  24. Travisano, M., Mongold, J.A., Bennett, A.F., Lenski, R.E. (1995). Experimental tests of the roles of adaptation, chance, and history in evolution. Science, 267, 87–90.

    Article  CAS  PubMed  Google Scholar 

  25. Lenski, R.E., Simpson, S.C., Nguyen, T.T. (1994). Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness. J. Bacteriol., 176, 3140–3147.

    CAS  PubMed  Google Scholar 

  26. Purrington, C.B., Bergelson, J. (1999). Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana. The American Naturalist, 154, S82–S91.

    Article  Google Scholar 

  27. Feder, M.E., Bennett, A.F., Huey, R.B. (2000). Evolutionary physiology. Annu. Rev. Ecol. Syst., 31, 315–341.

    Article  Google Scholar 

  28. Dieckmann, U., Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature, 400, 354–357.

    Article  CAS  PubMed  Google Scholar 

  29. Goldstein, M.A., Doi, R.H. (1995). Prokaryotic promoters in biotechnology. Biotechnol. Annu. Rev., 1, 105–128.

    Article  CAS  PubMed  Google Scholar 

  30. Vellanoweth, R.L., Rabinowitz, J.C. (1992). The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo. Mol. Microbiol., 6, 1105–1114.

    Article  CAS  PubMed  Google Scholar 

  31. Kane, J.F. (1995). Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol., 6, 494–500.

    Article  CAS  PubMed  Google Scholar 

  32. Chen, S.L., Lee, W., Hottes, A.K., Shapiro, L., McAdams, H.H. (2004). Codon usage between genomes is constrained by genome-wide mutational processes. Proc. Natl. Acad. Sci. U. S. A, 101, 3480–3485.

    Article  CAS  PubMed  Google Scholar 

  33. van Passel, M.W., van der, E.A., Bart, A. (2006). Plasmid diversity in neisseriae. Infect. Immun., 74, 4892–4899.

    Article  PubMed  Google Scholar 

  34. Bouma, J.E., Lenski, R.E. (1988). Evolution of a bacteria/plasmid association. Nature, 335, 351–352.

    Article  CAS  PubMed  Google Scholar 

  35. Haubold, B., Travisano, M., Rainey, P.B., Hudson, R.R. (1998). Detecting linkage disequilibrium in bacterial populations. Genetics, 150, 1341–1348.

    CAS  PubMed  Google Scholar 

  36. Lawrence, J.G., Ochman, H., Hartl, D.L. (1992). The evolution of insertion sequences within enteric bacteria. Genetics, 131, 9–20.

    CAS  PubMed  Google Scholar 

  37. Naas, T., Blot, M., Fitch, W.M., Arber, W. (1994). Insertion sequence-related genetic variation in resting Escherichia coli K-12. Genetics, 136, 721–730.

    CAS  PubMed  Google Scholar 

  38. Sorek, R., Zhu, Y., Creevey, C.J., Francino, M.P., Bork, P., Rubin, E.M. (2007) Genome-wide experimental determination of barriers to horizontal gene transfer. Science, 318, 1449–1452.

    Article  CAS  PubMed  Google Scholar 

  39. Alcaraz, L.D., Olmedo, G., Bonilla, G., Cerritos, R., Hernandez, G., Cruz, A., Ramirez, E., Putonti, C., Jimenez, B., Martinez, E., Lopez, V., Arvizu, J.L., Ayala, F., Razo, F., Caballero, J., Siefert, J., Eguiarte, L., Vielle, J.P., Martinez, O., Souza, V., Herrera-Estrella, A., Herrera-Estrella, L. (2008) The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. Proc. Natl. Acad. Sci. U. S. A, 105, 5803–5808.

    Article  CAS  PubMed  Google Scholar 

  40. Lenski, R.E., Bouma, J.E. (1987). Effects of segregation and selection on instability of plasmid pACYC184 in Escherichia coli B. J. Bacteriol., 169, 5314–5316.

    CAS  PubMed  Google Scholar 

  41. Nguyen, T.N., Phan, Q.G., Duong, L.P., Bertrand, K.P., Lenski, R.E. (1989). Effects of carriage and expression of the Tn10 tetracycline-resistance operon on the fitness of Escherichia coli K12. Mol. Biol. Evol., 6, 213–225.

    CAS  PubMed  Google Scholar 

  42. Ho, T.Q., Zhong, Z., Aung, S., Pogliano, J. (2002). Compatible bacterial plasmids are targeted to independent cellular locations in Escherichia coli. EMBO J., 21, 1864–1872.

    Article  CAS  PubMed  Google Scholar 

  43. De Gelder, L., Ponciano, J.M., Abdo, Z., Joyce, P., Forney, L.J., Top, E.M. (2004). Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution. Genetics, 168, 1131–1144.

    Article  PubMed  Google Scholar 

  44. Lenski, R.E., Souza, V., Duong, L.P., Phan, Q.G., Nguyen, T.N., Bertrand, K.P. (1994). Epistatic effects of promoter and repressor functions of the Tn10 tetracycline-resistance operon of the fitness of Escherichia coli. Mol. Ecol., 3, 127–135.

    Article  CAS  PubMed  Google Scholar 

  45. Dahlberg, C., Chao, L. (2003). Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics, 165, 1641–1649.

    CAS  PubMed  Google Scholar 

  46. Reid, S.J., Abratt, V.R. (2005) Sucrose utilisation in bacteria: genetic organisation and regulation. Appl. Microbiol. Biotechnol., 67, 312–321.

    Article  CAS  PubMed  Google Scholar 

  47. Trevino-Quintanilla, L.G., Escalante, A., Caro, A.D., Martinez, A., Gonzalez, R., Puente, J.L., Bolivar, F., Gosset, G. (2007) The phosphotransferase system-dependent sucrose utilization regulon in enteropathogenic Escherichia coli strains is located in a variable chromosomal region containing iap sequences. J. Mol. Microbiol. Biotechnol., 13, 117–125.

    Article  CAS  PubMed  Google Scholar 

  48. Cowan, P.J., Nagesha, H., Leonard, L., Howard, J.L., Pittard, A.J. (1991) Characterization of the major promoter for the plasmid-encoded sucrose genes scrY, scrA, and scrB. J. Bacteriol., 173, 7464–7470.

    CAS  PubMed  Google Scholar 

  49. Doroshenko, V.G., Livshits, V.A. (2004) Structure and mode of transposition of Tn2555 carrying sucrose utilization genes. FEMS Microbiol. Lett., 233, 353–359.

    Article  CAS  PubMed  Google Scholar 

  50. Jahreis, K., Bentler, L., Bockmann, J., Hans, S., Meyer, A., Siepelmeyer, J., Lengeler, J.W. (2002) Adaptation of sucrose metabolism in the Escherichia coli wild-type strain EC3132. J. Bacteriol., 184, 5307–5316.

    Article  CAS  PubMed  Google Scholar 

  51. Titgemeyer, F., Jahreis, K., Ebner, R., Lengeler, J.W. (1996) Molecular analysis of the scrA and scrB genes from Klebsiella pneumoniae and plasmid pUR400, which encode the sucrose transport protein Enzyme II Scr of the phosphotransferase system and a sucrose-6-phosphate invertase. Mol. Gen. Genet., 250, 197–206.

    CAS  PubMed  Google Scholar 

  52. Fouet, A., Arnaud, M., Klier, A., Rapoport, G. (1987) Bacillus subtilis sucrose-specific enzyme II of the phosphotransferase system: expression in Escherichia coli and homology to enzymes II from enteric bacteria. Proc. Natl. Acad. Sci. U. S. A, 84, 8773–8777.

    Article  CAS  PubMed  Google Scholar 

  53. Kornberg, H.L. (2001) Routes for fructose utilization by Escherichia coli. J. Mol. Microbiol. Biotechnol., 3, 355–359.

    CAS  PubMed  Google Scholar 

  54. Sabbagh, Y., Theriault, E., Sanschagrin, F., Voyer, N., Palzkill, T., Levesque, R.C. (1998). Characterization of a PSE-4 mutant with different properties in relation to penicillanic acid sulfones: importance of residues 216 to 218 in class A beta-lactamases. Antimicrob. Agents Chemother., 42, 2319–2325.

    CAS  PubMed  Google Scholar 

  55. Lenski, R.E., Travisano, M. (1994). Dynamics of adaptation and diversification: a 10, 000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. U. S. A, 91, 6808–6814.

    Article  CAS  PubMed  Google Scholar 

  56. Turner, P.E., Cooper, V.S., Lenski, R.E. (1998). Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution, 52, 315–329.

    Article  Google Scholar 

  57. Travisano, M., Lenski, R.E. (1996). Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics, 143, 15–26.

    CAS  PubMed  Google Scholar 

  58. Akashi, H., Gojobori, T. (2002). Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A, 99, 3695–3700.

    Article  CAS  PubMed  Google Scholar 

  59. Mann, R.S., Carroll, S.B. (2002). Molecular mechanisms of selector gene function and evolution. Curr. Opin. Genet. Dev., 12, 592–600.

    Article  CAS  PubMed  Google Scholar 

  60. Cooper, T.F., Rozen, D.E., Lenski, R.E. (2003). Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A, 100, 1072–1077.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Larios-Sanz, M., Travisano, M. (2009). Experimental Evolution of an Essential Bacillus Gene in an E. coli Host. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-853-9_16

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

  • Online ISBN: 978-1-60327-853-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics