Skip to main content
SpringerLink
Log in

Transcriptomic Analysis of 3-Hydroxypropanoic Acid Stress in Escherichia coli

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The stress response of Escherichia coli to 3-hydroxypropanoic acid (3-HP) was elucidated through global transcriptomic analysis. Around 375 genes showed difference of more than 2-fold in 3-HP-treated samples. Further analysis revealed that the toxicity effect of 3-HP was due to the cation and anion components of this acid and some effects-specific to 3-HP. Genes related to the oxidative stress, DNA protection, and repair were upregulated in treated cells due to the lowered cytoplasmic pH caused by accumulated cations. 3-HP-treated E. coli used the arginine acid tolerance mechanism to increase the cytoplasmic pH. Additionally, the anion effects were manifested as imbalance in the osmotic pressure. Analysis of top ten highly upregulated genes suggests the formation of 3-hydroxypropionaldehyde under 3-HP stress. The transcriptomic analysis shed light on the global genetic reprogramming due to 3-HP stress and suggests strategies for increasing the tolerance of E. coli toward 3-HP.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Tullo, A. (2000). Plastic found at the end maize. Chemical and Engineering News, 78, 13.

    Google Scholar 

  2. Werpy, T., Petersen, G., Aden, A., Bozell, J., Holladay, J., White, J., Manheim, A., Elliot, D., Lasure, L., Jones, S., Gerber, M., Ibsen, K., Lumberg, L., and Kelley, S. (2004). Top value added chemicals from biomass. Oak Ridge, TN, U.S. department of Energy, Washington, DC.

  3. Badarinarayana, V., Estep, P. W., Shendure, J., Edwards, J., Tavazoie, S., Lam, F., & Church, G. M. (2001). Selection analyses of insertional mutants using subgenic resolution arrays. Nature Biotechnology, 19, 1060–1065.

    Article  CAS  Google Scholar 

  4. Christopher, D., Herring, A. R., Honisch, C., Patel, T., Applebee, M. K., Joyce, A. R., Albert, T. J., Blattner, F. R., van den Boom, D., Cantor, C. R., & Palsson, B. Ø. (2006). Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genetics, 38, 1406–1412.

    Article  Google Scholar 

  5. Warnecke, T. E., Lynch, M. D., Karimpour-fard, A., Sandoval, N., & Gill, R. T. (2008). A genomic approach to improve the analysis and design of strain selections. Metabolic Engineering, 10, 154–165.

    Article  CAS  Google Scholar 

  6. Datsenko, K. A., & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Science, 97, 6640–6645.

    Article  CAS  Google Scholar 

  7. Rutherford, B. J., Dahl, R. H., Price, R. E., Szmidt, H. L., Benke, P. I., Mukhopadhyay, A., & Keasling, J. D. (2010). Functional genomic study of exogenous n-butanol stress in Escherichia coli. Applied and Environmental Microbiology, 76, 1935–1945.

    Article  CAS  Google Scholar 

  8. Stephanopoulos, G. N., Aristidou A. A., Nielsen J. (1998). Metabolic engineering-principles and methodologies. Academic Press.

  9. Warnecke, T., & Gill, R. T. (2005). Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microbial Cell Factories, 4, 25.

    Article  Google Scholar 

  10. Choi, S. H., Baulmer, D. J., & Kaspar, C. W. (2000). Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Applied and Environmental Microbiology, 66, 3911–3916.

    Article  CAS  Google Scholar 

  11. Dinglay, S., Trewick, S. C., Lindahl, T., & Sedgwick, B. (2000). Defective processing of methylated single-stranded DNA by Escherichia coli AlkB mutants. Genes and Development, 14, 2097–2105.

    CAS  Google Scholar 

  12. Thompson, S. A., Latch, R. L., & Blaser, J. M. (1998). Molecular characterization of the Helicobacter pylori uvr B gene. Gene, 209, 113–122.

    Article  CAS  Google Scholar 

  13. Chiancone, E. (2008). Dps proteins, an efficient detoxification and DNA protection machinery in the bacterial response to oxidative stress. Rendiconti Lincei, 19, 261–270.

    Article  Google Scholar 

  14. Halliwell, B., & Gutteridge, J. M. C. (2007). Free radicals in biology and medicine (4th ed.). Oxford: Oxford University Press.

    Google Scholar 

  15. Kanjee, U., & Houry, W. A. (2013). Mechanisms of acid resistance in Escherichia coli. Annual Review of Microbiology, 67, 65–81.

    Article  CAS  Google Scholar 

  16. McHugh, J. P., Rodríguez-Quinoñes, F., Abdul-Tehrani, H., Svistunenko, D. A., Poole, R. K., Cooper, C. E., & Andrews, S. C. (2003). Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. Journal of Biological Chemistry, 32, 29478–29486.

    Article  Google Scholar 

  17. Liochev, S. I., & Fridovich, I. (1999). Superoxide and iron: partners in crime. IUBMB Life, 48, 157–161.

    Article  CAS  Google Scholar 

  18. Imlay, J. A. (2003). Pathways of oxidative damage. Annual Review of Microbiology, 57, 395–418.

    Article  CAS  Google Scholar 

  19. Mills, T. Y., Sandoval, N. R., & Gill, R. T. (2009). Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnology for Biofuels, 2, 26.

    Article  Google Scholar 

  20. Roe, A. J., McLaggan, D., Davidson, I., O’Byrne, C., & Booth, I. R. (1998). Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. Journal of Bacteriology, 180(4), 767.

    CAS  Google Scholar 

  21. Kannan, G., Wilks, J. C., Fitzgerald, D. M., Jones, B. D., BonDurant, S. S., & Slonczewski, J. L. (2008). Rapid acid treatment of Escherichia coli: transcriptomic response and recovery. BMC Microbiology, 8, 37.

    Article  Google Scholar 

  22. Darcan, C., Ozkanca, R., & Flint, K. P. (2003). Survival of nonspecific porin deficient mutants of Escherichia coli in black sea water. Letters in Applied Microbiology, 37, 380–385.

    Article  CAS  Google Scholar 

  23. Frost, S. A., Delgado, J., & Inouye, M. (1989). DNA-binding properties of the transcription activator (OmpR) for the upstream sequences of ompF in Escherichia coli are altered by envZ mutations and medium osmolarity. Journal of Bacteriology, 171, 2949–2955.

    Google Scholar 

  24. Gerken, H., Charlson, E. S., Cicirelli, E. M., Kenney, L. J., & Rajeev Misra, R. (2009). MzrA: a novel modulator of the EnvZ/OmpR two-component regulon. Molecular Microbiology, 72, 1408–1422.

    Article  CAS  Google Scholar 

  25. Tucker, D. L., Tucker, N., & Conway, T. (2002). Gene expression profiling of the pH response in Escherichia coli. Journal of Bacteriology, 184, 6551–6558.

    Article  CAS  Google Scholar 

  26. Stincone, A., Daudi, N., Rahman, A. S., Antczak, P., Henderson, I., Cole, J., Johnson, M. D., Lund, P., & Falciani, F. (2011). A systems biology approach sheds new light on Escherichia coli acid resistance. Nucleic Acids Research, 39, 7512–7528.

    Article  CAS  Google Scholar 

  27. Dinnbier, U., Limpinsel, E., Schmid, R., & Bakker, E. P. (1988). Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Archives of Microbiology, 150, 348–357.

    Article  CAS  Google Scholar 

  28. Gonzalez, C. F., Proudfoot, M., Brown, G., Korniyenko, Y., Mori, H., Savchenko, A. V., & Yakunin, A. F. (2006). Molecular basis of formaldehyde detoxification. Characterization of two S-formylglutathione hydrolases from Escherichia coli, FrmB and YeiG. Journal of Biological Chemistry, 281, 14514–14522.

    Article  CAS  Google Scholar 

  29. Ito, K., Takahashi, M., Yoshimoto, T., & Tsuru, D. (1994). Cloning and high-level expression of the glutathione-independent formaldehyde dehydrogenase gene from Pseudomonas putida. Journal of Bacteriology, 176, 2483–2491.

    CAS  Google Scholar 

  30. Murdanoto, A. P., Sakai, Y., Konishi, T., Yasuda, F., Tani, Y., & Kato, N. (1997). Purification and properties of methyl formate synthase, a mitochondrial alcohol dehydrogenase, participating in formaldehyde oxidation in methylotrophic yeasts. Applied and Environmental Microbiology, 63, 1715–1720.

    CAS  Google Scholar 

  31. Harms, N., Ras, J., Reijnders, W. N., van Spanning, R. J., & Stouthamer, A. H. (1996). S-formylglutathione hydrolase of Paracoccus denitrificans is homologous to human esterase D: a universal pathway for formaldehyde detoxification. Journal of Bacteriology, 178, 6296–6299.

    CAS  Google Scholar 

  32. Hanson, A. D., Gage, D. A., & Shachar-Hill, Y. (2000). Plant one-carbon metabolism and its engineering. Trends in Plant Science, 5, 206–213.

    Article  CAS  Google Scholar 

  33. Kildegaard, K. R., Hallström, B. M., Blicher, T. H., Sonnenschein, N., Jensen, N. B., Sherstyk, S., Harrison, S. J., Maury, J., Herrgård, M. J., Juncker, A. S., Forster, J., Nielsen, J., & Borodina, I. (2014). Evolution reveals a glutathione-dependent mechanism of 3-hydroxypropionic acid tolerance. Metabolic Engineering, 26, 57–66.

    Article  CAS  Google Scholar 

  34. Zhao, X., Jiang, R., & Bai, F. (2009). Directed evolution of promoter and cellular transcription machinery and its application in microbial metabolic engineering review. Sheng Wu Gong Cheng Xue Bao, 25, 1312–1315.

    CAS  Google Scholar 

  35. Park, K. S., Lee, D. K., Lee, H., Lee, Y., Jang, Y. S., et al. (2003). Phenotypic alteration of eukaryotic cells using randomized libraries of artificial transcription factors. Nature Biotechnology, 21, 1208–1214.

    Article  CAS  Google Scholar 

  36. Lee, J. Y., Sung, B. H., Yu, B. J., Lee, J. H., Lee, S. H., et al. (2008). Phenotypic engineering by reprogramming gene transcription using novel artificial transcription factors in Escherichia coli. Nucleic Acids Research, 36, e102.

    Article  Google Scholar 

  37. Pomposiello, P. J., & Demple, B. (2001). Redox-operated genetic switches: the SoxR and OxyR transcriptional factors. Trends in Biotechnology, 19, 109–114.

    Article  CAS  Google Scholar 

  38. Hidalgo, E., & Demple, B. (1996). Adaptive responses to oxidative stress: The soxRS and oxyR regulons. In regulation of gene expression in Escherichia coli (Lin, E.C.C. and Lynch, A.S., eds), pp. 435–452.

  39. Patnaik, R. (2008). Engineering complex phenotypes in industrial strains. Biotechnology Progress, 24, 38–47.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the IB group members for their insights and discussion. This work was funded by A*STAR in Singapore (ICES/12-574A01).

Author information

Authors and Affiliations

  1. Industrial Biotechnology Division, Institute of Chemical and Engineering Sciences, Agency for Science, Technology and Research (A*STAR), 1 Pesek Road, Jurong Island, Singapore, 627833, Singapore

    Tu Wang Yung & Hua Zhao

  2. Process Science and Modelling Division, Institute of Chemical and Engineering Sciences, Agency for Science, Technology and Research (A*STAR), 1 Pesek Road, Jurong Island, Singapore, 627833, Singapore

    Sudhakar Jonnalagadda & Balaji Balagurunathan

Authors
  1. Tu Wang Yung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sudhakar Jonnalagadda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Balaji Balagurunathan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hua Zhao.

Additional information

Tu Wang Yung and Sudhakar Jonnalagadda are joint first authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yung, T.W., Jonnalagadda, S., Balagurunathan, B. et al. Transcriptomic Analysis of 3-Hydroxypropanoic Acid Stress in Escherichia coli . Appl Biochem Biotechnol 178, 527–543 (2016). https://doi.org/10.1007/s12010-015-1892-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-015-1892-8

Keywords

Search

Navigation