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Characterization of Truncated dsz Operon Responsible for Dibenzothiophene Biodesulfurization in Rhodococcus sp. FUM94

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Abstract

Numerous desulfurizing bacteria from the Rhodococcus genus harbor conserved dsz genes responsible for the degradation of sulfur compounds through 4S pathway. This study describes a newly identified desulfurizing bacterium, Rhodococcus sp. FUM94, which unlike previously identified strains encodes a truncated dsz operon. DNA sequencing revealed a frameshift mutation in the dszA gene, which led to an alteration of 66 amino acids and deletion of other C-terminal 66 amino acids. The resulting DszA polypeptide was shorter than DszA in Rhodococcus sp. IGTS8 reference strain. Despite the truncation, desulfurizing activity of the operon was observed and attributed to the removal of an overlap of dszA and dszB genes, and lack of active site in the altered region. Desulfurization experiments resulted in specific production rate of 6.3 mmol 2-hydroxy biphenyl (kgDCW)−1 h−1 at 2 g l−1 biocatalyst concentration and 68.8% biodesulfurization yield at 20 g l−1 biocatalyst concentration, both at 271 μM dibenzothiophene concentration which is comparable to similar wild-type biocatalysts.

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  • 25 January 2018

    The original version of this article unfortunately contained a mistake in the caption of Figs. 5 and 6.

References

  1. McFarland, B. L. (1999). Biodesulfurization. Current Opinion in Microbiology, 2, 257–264. https://doi.org/10.1016/S1369-5274(99)80045-9.

    Article  CAS  Google Scholar 

  2. Borgne, L. S., & Quintero, R. (2003). Biotechnological processes for the refining of petroleum. Fuel Processing Technology, 81, 155–169. https://doi.org/10.1016/S0378-3820(03)00007-9.

    Article  Google Scholar 

  3. Boniek, D., Figueiredo, D., dos Santos, A. F. B., & Stoianoff, M. A. R. (2015). Biodesulfurization: a mini review about the immediate search for the future technology. Clean Technologies and Environmental Policy, 17, 29–37. https://doi.org/10.1007/s10098-014-0812-x.

    Article  Google Scholar 

  4. Kilbane, J. J. (1990). Sulfur-specific microbial metabolism of organic compounds. Resources, Conservation and Recycling, 3, 69–79. https://doi.org/10.1016/0921-3449(90)90046-7.

    Article  Google Scholar 

  5. Denome, S. A., Olson, E. S., & Young, K. D. (1993). Identification and cloning of genes involved in specific desulfurization of dibenzothiophene by Rhodococcus sp. strain IGTS8. Applied and Environmental Microbiology, 59, 2837–2843.

    CAS  Google Scholar 

  6. Denome, S. A., Oldfield, C., Nash, L. J., & Young, K. D. (1994). Characterization of the desulfurization genes from Rhodococcus sp. strain IGTS8. Journal of Bacteriology, 176, 6707–6716. https://doi.org/10.1128/jb.176.21.6707-6716.1994.

    Article  CAS  Google Scholar 

  7. Piddington, C. S., Kovacevich, B. R., & Rambosek, J. (1995). Sequence and molecular characterization of a DNA region encoding the dibenzothiophene desulfurization operon of Rhodococcus sp. strain IGTS8. Applied and Environmental Microbiology, 61, 468–475.

    CAS  Google Scholar 

  8. Gray, K. A., Pogrebinsky, O. S., Mrachko, G. T., Xi, L., Monticello, D. J., & Squires, C. H. (1996). Molecular mechanisms of biocatalytic desulfurization of fossil fuels. Nature Biotechnology, 14, 1705–1709. https://doi.org/10.1038/nbt1296-1705.

    Article  CAS  Google Scholar 

  9. Tanaka, Y., Matsui, T., Konishi, J., Maruhashi, K., & Kurane, R. (2002). Biodesulfurization of benzothiophene and dibenzothiophene by a newly isolated Rhodococcus strain. Applied Microbiology and Biotechnology, 59, 325–328. https://doi.org/10.1007/s00253-002-0985-9.

    Article  CAS  Google Scholar 

  10. Yu, B., Xu, P., Shi, Q., & Ma, C. (2006). Deep desulfurization of diesel oil and crude oils by a newly isolated Rhodococcus erythropolis strain. Applied and Environmental Microbiology, 72, 54–58. https://doi.org/10.1128/AEM.72.1.54-58.2006.

    Article  CAS  Google Scholar 

  11. Mohebali, G., Ball, A. S., Rasekh, B., & Kaytash, A. (2007). Biodesulfurization potential of a newly isolated bacterium, Gordonia alkanivorans RIPI90A. Enzyme and Microbial Technology, 40, 578–584. https://doi.org/10.1016/j.enzmictec.2006.05.012.

    Article  CAS  Google Scholar 

  12. Davoodi-Dehaghani, F., Vosoughi, M., & Ziaee, A. A. (2010). Biodesulfurization of dibenzothiophene by a newly isolated Rhodococcus erythropolis strain. Bioresource Technology, 101, 1102–1105. https://doi.org/10.1016/j.biortech.2009.08.058.

    Article  CAS  Google Scholar 

  13. Denis-Larose, C., Labbe, D., Bergeron, H., Jones, A., Greer, C. W., Hawari, J., Grossman, M. J., Sankey, B. M., & Lau, P. C. K. (1997). Conservation of plasmid-encoded dibenzothiophene desulfurization genes in several Rhodococci. Applied and Environmental Microbiology, 63, 2915–2919.

    CAS  Google Scholar 

  14. Duarte, G. F., Rosado, A. S., Seldin, L., De Araujo, W., & Van Elsas, J. D. (2001). Analysis of bacterial community structure in sulfurous-oil-containing soils and detection of species carrying dibenzothiophene desulfurization (dsz) genes. Applied and Environmental Microbiology, 67, 1052–1062. https://doi.org/10.1128/AEM.67.3.1052-1062.2001.

    Article  CAS  Google Scholar 

  15. Kilbane, J. J., & Robbins, J. (2007). Characterization of the dszABC genes of Gordonia amicalis F.5.25.8 and identification of conserved protein and DNA sequences. Applied Microbiology and Biotechnology, 75, 843–851.

    Article  CAS  Google Scholar 

  16. Li, G. Q., Li, S. S., Zhang, M. L., Wang, J., Zhu, L., Liang, F. L., Liu, R. L., & Ma, T. (2008). Genetic rearrangement strategy for optimizing the dibenzothiophene biodesulfurization pathway in Rhodococcus erythropolis. Applied and Environmental Microbiology, 74, 971–976. https://doi.org/10.1128/AEM.02319-07.

    Article  CAS  Google Scholar 

  17. Izumi, Y., Ohshiro, T., Ogino, H., Hine, Y., & Shimao, M. (1994). Selective desulfurization of dibenzothiophene by Rhodococcus erythropolis D-1. Applied and Environmental Microbiology, 60, 223–226.

    CAS  Google Scholar 

  18. Sambrook, J., & Russell, D. W. (2001). Molecular cloning: a laboratory manual (Third ed.). Cold Spring Harbor: Cold Spring Harbor Laboratory.

    Google Scholar 

  19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–685. https://doi.org/10.1038/227680a0.

    Article  CAS  Google Scholar 

  20. Maghsoudi, S., Vossoughi, M., Kheirolomoom, A., Tanaka, E., & Katoh, S. (2001). Biodesulfurization of hydrocarbons and diesel fuels by Rhodococcus sp. strain P32C1. Biochemical Engineering Journal, 8, 151–156. https://doi.org/10.1016/S1369-703X(01)00097-3.

    Article  CAS  Google Scholar 

  21. Caro, A., Boltes, K., Leton, P., & Garcia-Calvo, E. (2007). Dibenzothiophene biodesulfurization in resting cell conditions by aerobic bacteria. Biochemical Engineering Journal, 35, 191–197. https://doi.org/10.1016/j.bej.2007.01.013.

    Article  CAS  Google Scholar 

  22. Oldfield, C., Pogrebinsky, O., Simmonds, J., Olson, E. S., & Kulpa, C. F. (1997). Elucidation of the metabolic pathway for dibenzothiophene desulfurization by Rhodococcus sp. strain IGTS8 (ATCC 53968). Microbiology, 143, 2961–2973. https://doi.org/10.1099/00221287-143-9-2961.

    Article  CAS  Google Scholar 

  23. Kaufman, E. R., Harkins, J. B., & Borole, A. P. (1998). Comparison of batchstirred and electrospray reactors for biodesulfurization of dibenzothiophene in crude oil and hydrocarbon feedstock. Applied Biochemistry and Biotechnology, 73, 127–144. https://doi.org/10.1007/BF02785650.

    Article  CAS  Google Scholar 

  24. del Olmo, C. H., Alcon, A., Santos, V. E., & Garcia-ochoa, F. (2005). Modeling the production of a Rhodococcus erythropolis IGTS8 biocatalyst for DBT biodesulfurization: influence of media composition. Enzyme and Microbial Technology, 37, 157–166. https://doi.org/10.1016/j.enzmictec.2004.06.016.

    Article  Google Scholar 

  25. Caro, A., Leton, P., Garcia-calvo, E., & Setti, L. (2007). Enhancement of dibenzothiophene biodesulfurization using β-cyclodextrins in oil-to-water media. Fuel, 86, 2632–2636. https://doi.org/10.1016/j.fuel.2007.02.033.

    Article  CAS  Google Scholar 

  26. Wang, P., Humphrey, A. E., & Krawiec, S. (1996). Kinetic analyses of desulfurization of dibenzotiophene by Rhodococcus erythropolis in continuous cultures. Applied and Environmental Microbiology, 62, 3066–3068.

    CAS  Google Scholar 

  27. Ohshiro, T., Hirata, T., & Izumi, Y. (1996). Desulfurization of dibenzothiophene derivatives by whole cells of Rhodococcus erythropolis H-2. FEMS Microbiology Letters, 142, 65–70. https://doi.org/10.1111/j.1574-6968.1996.tb08409.x.

    Article  CAS  Google Scholar 

  28. Yan, H., Kishimoto, M., Omasa, T., Katakura, Y., Suga, K. I., Okumura, K., & Yoshikawa, O. (2000). Increase in desulfurization activity of Rhodococcus erythropolis KA2-5-1 using ethanol feeding. Journal of Bioscience and Bioengineering, 89, 361–366. https://doi.org/10.1016/S1389-1723(00)88959-8.

    Article  CAS  Google Scholar 

  29. Guerinik, K., & Al-Mutawah, Q. (2003). Isolation and characterization of oil-desulfurizing bacteria. World Journal of Microbiology and Biotechnology, 19, 941–945. https://doi.org/10.1023/B:WIBI.0000007327.72618.0f.

    Article  CAS  Google Scholar 

  30. Yang, J., & Marison, I. W. (2005). Two-stage process design for the biodesulphurisation of a model diesel by a newly isolated Rhodococcus globerulus DAQ3. Biochemical Engineering Journal, 27, 77–82. https://doi.org/10.1016/j.bej.2005.08.012.

    Article  CAS  Google Scholar 

  31. Yang, J., Hu, Y., Zhao, D., Wang, S., Lau, P. C. K., & Marison, I. W. (2007). Two-layer continuous-process design for the biodesulfurization of diesel oils under bacterial growth conditions. Biochemical Engineering Journal, 37, 212–218. https://doi.org/10.1016/j.bej.2007.04.012.

    Article  CAS  Google Scholar 

  32. Li, G. Q., Ma, T., Li, S. S., Li, H., Liang, F. L., & Liu, R. L. (2007). Improvement of dibenzothiophene desulfurization activity by removing the gene overlap in the dsz operon. Bioscience, Biotechnology, and Biochemistry, 71, 849–854.

    Article  CAS  Google Scholar 

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Acknowledgements

Some experiments were performed in the Biotechnology Laboratory of the Faculty of Veterinary Medicine, and in the Genetic Engineering Laboratory of the Research Institute of Biotechnology, Ferdowsi University of Mashhad.

Funding

This work was supported by the Ferdowsi University of Mashhad, Graduate Students Research Fund, Grant No. 3/22025. The sponsor had no involvement in the study design; collection, analysis, and interpretation of the data; writing the report; and decision for submission.

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Authors and Affiliations

  1. Department of Chemical Engineering, Ferdowsi University of Mashhad, Azadi Square, Pardis Campus, Mashhad, 9177948944, Iran

    Somayeh Khosravinia, Mahmood A. Mahdavi & Reza Gheshlaghi

  2. Embryonic and Stem Cell Biology and Biotechnology Research Group, Institute of Biotechnology, Ferdowsi University of Mashhad, Azadi Square, Mashhad, 9177948944, Iran

    Hesam Dehghani

  3. Division of Biotechnology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Azadi Square, Mashhad, 9177948944, Iran

    Hesam Dehghani

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  1. Somayeh Khosravinia
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  2. Mahmood A. Mahdavi
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Correspondence to Mahmood A. Mahdavi.

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The authors declare no personal or financial conflict of interest. All authors approved the final version of the manuscript. SK conducted the experiments, MAM designed and supervised the study, RG contributed the experimental setup, and HD supervised some experiments and contributed to the interpretation of results.

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A correction to this article is available online at https://doi.org/10.1007/s12010-018-2703-9.

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Khosravinia, S., Mahdavi, M.A., Gheshlaghi, R. et al. Characterization of Truncated dsz Operon Responsible for Dibenzothiophene Biodesulfurization in Rhodococcus sp. FUM94. Appl Biochem Biotechnol 184, 885–896 (2018). https://doi.org/10.1007/s12010-017-2596-z

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