Influence of a temperature shock on the synthesis efficiency of surfactants by Rhodococcus pyridinivorans 5Ap bacteria
https://doi.org/10.29235/1029-8940-2023-68-3-224-233
Abstract
It was found that the synthesis of surfactants by R. pyridinivorans 5Ap bacteria can be increased by exposing them to a short temperature shock (55 °C for 20 minutes) after 24 hour cultivation in a minimal medium containing molasses (3 %) and hexadecane (2 %) (9 % increase in the emulsification index). Gene activation encoding global regulators of cell metabolism, including those performing a protective function under stress, was recorded in this cultivation mode. In particular, the mRNA amount determining the synthesis of the alternative transcription factor SigH increased 90.8 times and containing in the promoters its binding sites fmdB cochaperone – 59.3 times, hsp22.5 chaperone – 81.1 times, and the trxB gene encoding thioredoxin reductase – 73.1 times. In addition, it was shown that the transcriptional activation of groEL1, groEL2 and dnaJ genes determining the synthesis of heat shock proteins was 2.2, 2.6 and 4.4 times, respectively. The obtained results suggest that an increase in the alternative factor sigma H synthesis, which activates protective cellular metabolism, as well as structural, heat shock proteins under short temperature stress, leads to an increased production of surfactants, which can be used to optimize the synthesis of these secondary metabolites for biotechnological use.
About the Authors
H. BukliarevichBelarus
Hanna A. Bukliarevich – Junior Researcher.
4, Nezavisimosti Ave., 220030, Minsk
M. A. Titok
Belarus
Marina A. Titok – D. Sc. (Biol.), Professor.
4, Nezavisimosti Ave., 220030, Minsk
References
1. Nazari M. T., Simon V., Machado B. S., Crestani L., Marchezi G., Concolato G., Ferrari V., Colla L. M., Piccin J. S. Rhodococcus: A promising genus of actinomycetes for the bioremediation of organic and inorganic contaminants. Journal of Environmental Management, 2022, vol. 323, art. 116220. https://doi.org/10.1016/j.jenvman.2022.116220
2. da Rosa C. F. C., Freire D. M. G., Ferraz H. C. Biosurfactant microfoam: Application in the removal of pollutants from soil. Journal of Environmental Chemical Engineering, 2015, vol. 3, no. 1, pp. 89–94. https://doi.org/10.1016/j.jece.2014.12.008
3. Sarubbo L. A., Rocha Jr B. R., Luna J. M., Rufino R. D., Santos V. A., Banat I. M. Some aspects of heavy metals contamination remediation and role of biosurfactants. Chemistry and Ecology, 2015, vol. 31, no. 8, pp. 707–723. https://doi.org/10.1080/02757540.2015.1095293
4. Silva R. de C. F. S., Almeida D. G., Rufino R. D., Luna J. M., Santos V. A., Sarubbo L. A. Applications of biosurfactants in the petroleum industry and the remediation of oil spills. International Journal of Molecular Sciences, 2014, vol. 15, no. 7, pp. 12523–12542. https://doi.org/10.3390/ijms150712523
5. Campos J. M., Stamford T. L. M., Sarubbo L. A., de Luna J. M., Rufino R. D., Banat I. M. Microbial biosurfactants as additives for food industries. Biotechnology Progress, 2013, vol. 29, no. 5, pp. 1097–1108. https://doi.org/10.1002/btpr.1796
6. Gupta P. L., Rajput M., Oza T., Trivedi U., Sanghvi G. Eminence of microbial products in cosmetic industry. Natural Products and Bioprospecting, 2019, vol. 9, no. 4, pp. 267–278. https://doi.org/10.1007/s13659-019-0215-0
7. Rodrigues L., Banat I. M., Teixeira J., Oliveira R. Biosurfactants: potential applications in medicine. Journal of Antimicrobial Chemotherapy, 2006, vol. 57, no. 4, pp. 609–618. https://doi.org/10.1093/jac/dkl024
8. Bertrand B., Martínez-Morales F., Rosas-Galván N. S., Morales-Guzmán D., Trejo-Hernández M. R. Statistical design, a powerful tool for optimizing biosurfactant production: a review. Colloids and Interfaces, 2018, vol. 2, no. 3, p. 36. https://doi.org/10.3390/colloids2030036
9. Ghribi D., Zouari N., Jaoua S. Improvement of bioinsecticides production through adaptation of Bacillus thuringiensis cells to heat treatment and NaCl addition. Journal of Applied Microbiology, 2005, vol. 98, no. 4, pp. 823–831. https://doi.org/10.1111/j.1365-2672.2004.02490.x
10. Bukliarevich H. A., Titok M. A. Role of the structural and functional genes encoding heat shock proteins in biosurfactant synthesis by Rhodococcus pyridinivorans 5Ap. Microbiology, 2023, vol. 92, no. 3.
11. Chaturongakul S., Raengpradub S., Palmer M. E., Bergholz T. M., Orsi R. H., Hu Y., Ollinger J., Wiedmann M., Boor K. J. Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors σB, σC, σH, and σL in Listeria monocytogenes. Applied and Environmental Microbiology, 2011, vol. 77, no. 1, pp. 187–200. https://doi.org/10.1128/AEM.00952-10
12. Tian Y., Yu C., Shen Z. Overproduction of the Escherichia coli chaperones GroEL-GroES in Rhodococcus ruber improves the activity and stability of cell catalysts harboring a nitrile hydratase. Journal of Microbiology and Biotechnology, 2016, vol. 26, no. 2, pp. 337–346. https://doi.org/10.4014/jmb.1509.09084
13. Chen Y., Jiao S., Wang M., Chen J., Yu H. A novel molecular chaperone GroEL2 from Rhodococcus ruber and its fusion chimera with nitrile hydratase for co-enhanced activity and stability. Chemical Engineering Science, 2018, vol. 192, pp. 235–243. https://doi.org/10.1016/j.ces.2018.07.045
14. Pirog T. P., Shevchuk T. A., Klimenko I. A. Intensification of surfactant synthesis in Rhodococcus erythropolis EK-1 cultivated on hexadecane. Applied Biochemistry and Microbiology, 2010, vol. 46, no. 6, pp. 599–606. https://doi.org/10.1134/S0003683810060074
15. Kuyukina M. S., Ivshina I. B., Philp J. C., Christofi N., Dunbar S. A., Ritchkova M. I. Recovery of Rhodococcus biosurfactants using methyl tertiary-butyl ether extraction. Journal of Microbiological Methods, 2001, vol. 46, no. 2, pp. 149– 156. https://doi.org/10.1016/s0167-7012(01)00259-7
16. DuBois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 1956, vol. 28, no. 3, pp. 350–356. https://doi.org/10.1021/ac60111a017
17. Cooper D. G., Goldenberg B. G. Surface-active agents from two Bacillus species. Applied and Environmental Microbiology, 1987, vol. 53, no. 2, pp. 224–229. https://doi.org/10.1128/aem.53.2.224-229.1987
18. Pfaffl M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 2001, vol. 29, no. 9, p. e45. https://doi.org/10.1093/nar/29.9.e45
19. Bukliarevich H. A., Gurinovich A. S., Filonov A. E., Titok M. A. Molecular genetic and functional analysis of the genes encoding alkane 1-monooxygenase synthesis in members of the genus Rhodococcus. Microbiology, 2023, vol. 92, no. 2, pp. 242–255. https://doi.org/10.1134/S0026261722603311
20. Liu H., Xu J., Liang R., Liu J. Characterization of the medium- and long-chain n-alkanes degrading Pseudomonas aeruginosa strain SJTD-1 and its alkane hydroxylase genes. PLoS ONE, 2014, vol. 9, no. 8, p. e105506. https://doi.org/10.1371/journal.pone.0105506
21. Malkapuram S. T., Sharma V., Gumfekar S. P., Sonawane S., Sonawane S., Boczkaj G., Seepana M. M. A review on recent advances in the application of biosurfactants in wastewater treatment. Sustainable Energy Technologies and Asses s- ments, 2021, vol. 48, art. 101576. https://doi.org/10.1016/j.seta.2021.101576
22. Becker S. H., Ulrich K., Dhabaria A., Ueberheide B., Beavers W., Skaar E. P., Iyer L. M., Aravind L., Jakob U., Darwin K. H. Mycobacterium tuberculosis Rv0991c is a redox-regulated molecular chaperone. mBio, 2020, vol. 11, no. 4, p. e01545–20. https://doi.org/10.1128/mBio.01545-20
23. Ballal A., Manna A. C. Control of thioredoxin reductase gene (trxB) transcription by SarA in Staphylococcus aureus. Journal of Bacteriology, 2010, vol. 192, no. 1, art. 336. https://doi.org/10.1128/JB.01202-09
24. Štěpánek V., Dostálová H., Busche T., Blumenstein J., Grulich M., Plašil L., Rucká L., Nešvera J., Pátek M. Sigma regulatory network in Rhodococcus erythropolis CCM2595. FEMS Microbiology Letters, 2022, vol. 369, no. 1, art. fnac014. https://doi.org/10.1093/femsle/fnac014
25. Abomoelak B., Marcus S. A., Ward S. K., Karakousis P. C., Steinberg H., Talaat A. M. Characterization of a novel heat shock protein (Hsp22.5) involved in the pathogenesis of Mycobacterium tuberculosis. Journal of Bacteriology, 2011, vol. 193, no. 14, pp. 3497–3505. https://doi.org/10.1128/JB.01536-10
26. Ortiz de Orué Lucana D., Wedderhoff I., Groves M. R. ROS-mediated signalling in bacteria: zinc-containing Cys-XX-Cys redox centres and iron-based oxidative stress. Journal of Signal Transduction, 2012, vol. 2012, p. 605905. https://doi.org/10.1155/2012/605905