Skip to main content
Log in

Effect of the Structural and Regulatory Heat Shock Proteins on Hydrocarbon Degradation by Rhodococcus pyridinivorans 5Ap

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The role of heat shock proteins in ability of Rhodococcus pyridinivorans 5Ap to degrade hydrocarbons at different temperatures was studied. The presence of the Сpn60.1–Сpn10 chaperons and of the Hrc regulatory protein was found to be required for hexadecane degradation at 42°C. When genetic determinants responsible for synthesis of these proteins were inactivated, the efficiency of hexadecane degradation decreased 1.7 and 2.7 times, respectively. Mutations in the cpn and hrcA genes did not affect the viability of R. pyridinivorans 5Ар: the original strain and the mutants exhibited the same growth rates at all temperatures in the minimal medium with succinate and in full-strength medium. In the absence of the Сpn60.1–Сpn10 heat shock proteins, the growth rate at 42°C decreased in the case of minimal agar media with kerosene, diesel fuel, acetone, naphthalene, 2-methylnaphthalene, or phenanthrene.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Barreiro, C., González-Lavado, E., Pátek, M., and Martín, J.F., Transcriptional analysis of the groES-groEL1, groEL2, and dnaK genes in Corynebacterium glutamicum: characterization of heat shock-induced promoters, J. Bacteriol., 2004, vol. 186, pp. 4813–4817.

    Article  CAS  Google Scholar 

  2. Bullock, W.O., Fernandez, J.M., and Short, J.M., XL1-Blue–a high-efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection, Biotechniques, 1987, vol. 5, pp. 376–379.

    CAS  Google Scholar 

  3. Charniauskaya, M.I., Bukliarevich, A.A., Akhremchuk, A.E., Valentovich, L.N., and Titok, M.A., Primary analysis of the genome of oil-degrading bacteria Rhodococcus pyridinivorans 5Ap, Tr. Belorus. Gos. Univ., 2016, vol. 11, no. 1, pp. 219–223.

    Google Scholar 

  4. Charniauskaya, M.I., Bukliarevich, A.A., Delegan, Ya.A., Akhremchuk, A.E., Filonov, A.E., and Titok, M.A., Biodiversity of hydrocarbon-oxidizing soil bacteria from various climatic zones, Microbiology (Moscow), 2018, vol. 87, pp. 699–711.

    Article  CAS  Google Scholar 

  5. Chaturongakul, S., Raengpradub, S., Palmer, M.E., Bergholz, T.M., Orsi, R.H., Hu, Y., Ollinger, J., Wiedmann, M., and Boor, K.J., Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors sigmaB, sigmaC, sigmaH, and sigmaL in Listeria monocytogenes, Appl. Environ. Microbiol., 2011, no. 77, pp. 187–200.

  6. Crombie, A.T., Khawand, M.E., Rhodius, V.A., Fengler, K.A., Miller, M.C., Whited, G.M., McGenity, T.J., and Murrell, J.C., Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle, Environ. Microbiol., 2015, vol. 17, pp. 3314–3329.

    Article  CAS  Google Scholar 

  7. Furuya, T., Hayashi, M., Semba, H., and Kino, K., The mycobacterial binuclear iron monooxygenases require a specific chaperonin-like protein for functional expression in a heterologous host, FEBS J., 2013, vol. 280, pp. 817–826.

    CAS  PubMed  Google Scholar 

  8. Goyal, K., Qamra, R., and Mande, S.C., Multiple gene duplication and rapid evolution in the groEL gene: functional implications, J. Mol. Evol., 2006, vol. 63, pp. 781–787.

    Article  CAS  Google Scholar 

  9. Grandvalet, C., Rapoport, G., and Mazodier, P., hrcA, encoding the repressor of the groEL genes in Streptomyces albus G, is associated with a second dnaJ gene, J. Bacteriol., 1998, vol. 180, pp. 5129–5134.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Hu, Y., Henderson, B., Lund, P.A., Tormay, P., Ahmed, M.T., Gurcha, S.S., Besra, G.S., and Coates, A.R., A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable but fails to induce an inflammatory response in animal models of infection, Infect. Immun., 2008, vol. 76, pp. 1535–1546.

    Article  CAS  Google Scholar 

  11. Katalog shtammov regional’noi profilirovannoi kollektsii alkanotrofnykh mikroorganizmov (Strain Catalog of the Regional Profiled Collection of Alkanotrophic Microorganisms), Ivshina, I.B., Ed., 1994.

    Google Scholar 

  12. Khosravinia, S., Mahdavi, M.A., Gheshlaghi, R., and Dehghani, H., Characterization of truncated dsz operon responsible for dibenzothiophene biodesulfurization in Rhodococcus sp. FUM94, Appl. Biochem. Biotechnol., 2018, vol. 184, pp. 885–896.

    Article  CAS  Google Scholar 

  13. Kim, A.I., Ghosh, P., Aaron, M.A., Bibb, L.A., Jain, S.,and Hatfull, G.F., Mycobacteriophage Bxb1 integrates into the Mycobacterium smegmatis groEL1 gene, Mol. Microbiol., 2003, vol. 50, pp. 463–473.

    Article  CAS  Google Scholar 

  14. Kolaj, O., Spada, S., Robin, S., and Wall, J.G., Use of folding modulators to improve heterologous protein production in Escherichia coli [Electronic resource], Microbial Cell Factories, 2009, vol. 8, no. 9. Date of access: 14.10.2018.https://doi.org/10.1186/1475-2859-8-9

  15. Lin, Z., Madan, D., and Rye, H.S., GroEL stimulates protein folding through forced unfolding, Nat. Struct. Mol. Biol., 2008, vol. 15, pp. 303–311.

    Article  CAS  Google Scholar 

  16. Lund, P.A., Multiple chaperonins in bacteria–why so many?, FEMS Microbiol. Rev., 2009, vol. 334, pp. 785–800.

    Article  Google Scholar 

  17. Maniatis, T., Fritsh, E.E., and Sambrook, J., Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory, 1982.

    Google Scholar 

  18. Manual of Methods for General Bacteriology, Gerhardt, P., Murray, R.G.E., Costilow, R.N., Nester, E.W., Wood, W.A., Krieg, N.R., and Phillips, G.B., Eds., Washington: Amer. Soc. Microbiol., 1981.

    Google Scholar 

  19. McCarl, V., Somerville, M.V., Ly, M.A., Henry, R., Liew, E.F., Wilson, N.L., Holmes, A.J., and Coleman, N.V., Heterologous expression of Mycobacterium alkene monooxygenases in gram-positive and gram-negative bacterial hosts [Electronic resource], Appl. Environ Microbiol., 2018, vol. 84, no. 15. Date of access: 14.10.2018.https://doi.org/10.1128/AEM.00397-18

  20. Metcalf, W.W., Jiang, W., and Wanner, B.L., Use of the rep technique for allele replacement to construct new Escherichia coli hosts for maintenance of R6Kgamma origin plasmids at different copy numbers, Gene, 1994, vol. 138, pp. 1–7.

    Article  CAS  Google Scholar 

  21. Miller, J.H., Experiments in Molecular Genetics, Cold Spring Harbor: Cold Spring Harbor Lab., 1972.

    Google Scholar 

  22. Nicolaou, S.A., Gaida, S.M., and Papoutsakis, E.T., A comparative view of metabolic and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation, Metabolic Engineering., 2010, vol. 12, pp. 307–331.

    Article  CAS  Google Scholar 

  23. Ojha, A., Anand, M., Bhatt, A., Kremer, L., Jacobs, W.R., Jr., and Hatfull, G.F., GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria, Cell, 2005, vol. 123, pp. 861–873.

    Article  CAS  Google Scholar 

  24. Orro, A., Cappelletti, M., D’Ursi, P., Milanesi, L., Di Canito, A., Zampolli, J., Collina, E., Decorosi, F., Viti, C., Fedi, S., Presentato, A., Zannoni, D., and Di Gennaro, P., Genome and phenotype microarray analyses of Rhodococcus sp. BCP1 and Rhodococcus opacus R7: genetic determinants and metabolic abilities with environmental relevance [Electronic resource], PloS One, 2015, vol. 10, no. 10. Date of access: 14.10.2018.https://doi.org/10.1371/journal.pone.0139467

  25. RF Patent no. 2617941, 2017.

  26. Romanenko, V.I. and Kuznetsov, S.I., Ekologiya mikroorganizmov presnykh vod: Laboratornoe rukovodstvo (Ecology of Freshwater Microorganisms: A Laboratory Manual), Moscow: Nauka, 1974.

  27. Roncarati, D. and Scarlato, V., Regulation of heat shock genes in bacteria: from signal sensing to gene expression output, FEMS Microbiol. Rev., 2017, vol. 41, pp. 549–574.

    Article  CAS  Google Scholar 

  28. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G., and Pühler, A., Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum, Gene, 1994, vol. 145, pp. 69–73.

    Article  Google Scholar 

  29. Servant, P., Thompson, C.J., and Mazodier, P., Post-transcriptional regulation of the groEL1 gene of Streptomyces albus, Mol. Microbiol., 1994, vol. 12, pp. 423–432.

    Article  CAS  Google Scholar 

  30. Stewart, G.R., Wernisch, L., Stabler, R., Mangan, J.A., Hinds, J., Laing, K.G., Young, D.B, and Butcher, P.D., Dissection of the heatshock response in Mycobacterium tuberculosis using mutants and microarrays, Microbiology (UK), 2002, vol. 148, pp. 3129–3138.

    Article  CAS  Google Scholar 

  31. Takihara, H., Ogihara, J., Yoshida, T., Okuda, S., Nakajima, M., Iwabuchi, N., and Sunairi, M. Enhanced translocation and growth of Rhodococcus erythropolis PR4 in the alkane phase of aqueous-alkane two phase cultures were mediated by GroEL2 overexpression, Microbes Environ., 2014, vol. 29, pp. 346–352.

    Article  Google Scholar 

  32. te Riele, H., Michel, B., and Ehrlich, S.D., Single-stranded plasmid DNA in Bacillus subtilis and Staphylococcus aureus, Proc. Natl. Acad. Sci. U. S. A., 1986, vol. 83, pp. 2541–2545.

    Article  CAS  Google Scholar 

  33. Tomas, C.A., Welker, N.E., and Papoutsakis, E.T., Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell’s transcriptional program, Appl. Environ. Microbiol., 2003, vol. 69, pp. 4951–4965.

    Article  CAS  Google Scholar 

  34. van der Geize, R., Hessels, G.I., van Gerwen, R., van der Meijden, P., and Dijkhuizen, L. Unmarked gene deletion mutagenesis of kstD, encoding 3-ketosteroid Delta1-dehydrogenase, in Rhodococcus erythropolis SQ1 using sacB as counter-selectable marker, FEMS Microbiol. Lett., 2001, vol. 205, pp. 197–202.

    Article  CAS  Google Scholar 

Download references

Funding

The study was supported by the Belarusian Republican Foundation for -Fundamental Research (project no. B18-070).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. A. Bukliarevich.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

Translated by D. Timchenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bukliarevich, H.A., Charniauskaya, M.I., Akhremchuk, A.E. et al. Effect of the Structural and Regulatory Heat Shock Proteins on Hydrocarbon Degradation by Rhodococcus pyridinivorans 5Ap. Microbiology 88, 573–579 (2019). https://doi.org/10.1134/S0026261719050023

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261719050023

Keywords:

Navigation