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References

  1. Bahuguna, A., M. K. Lily, A. Munjal, R. N. Singh, and K. Dangwal. 2011. Desulfurization of dibenzothiophene (DBT) by a novel strain Lysinibacillus sphaericus DMT-7 isolated from diesel contaminated soil. J. Environ. Sci. 23: 975-982.
    CrossRef
  2. Chang, J. H., Y. K. Chang, K. S. Cho, and H. N. Chang. 2000. Desulfurization of model oils by resting cells of Gordonia sp. Biotechnol. Lett. 22: 193-196.
    CrossRef
  3. Dursun, A. Y. and O. Tepe. 2005. Internal mass transfer effect on biodegradation of phenol by Ca-alginate immobilized Ralstonia eutropha. J. Hazard. Mater. 126: 105-111.
    Pubmed CrossRef
  4. Fernandes, P., P. Vidinha, T. Ferreira, H. Silvestre, J. M. S. Cabral, and D. M. F. Prazeres. 2002. Use of free and immobilized Pseudomonas putida cells for the reduction of a thiophene derivative in organic media. J. Mol. Catal. B Enzym. 19: 353361.
    CrossRef
  5. Gallagher, J. R., S. S. Olson, and D. C. Stanley. 1993. Microbial desulfurization of benzothiophene: A sulfur specific pathway. FEMS Microbiol. Lett. 107: 31-36.
    Pubmed CrossRef
  6. Giuliano, M., C. Schiraldi, C. Maresca, V. Esposito, and M. D. Rosa. 2003. Immobilized Proteus mirabilis in poly(vinyl alcohol) cryogels for l (−)-carnitine production. Enzyme Microb. Technol. 32: 507-512.
    CrossRef
  7. Gray, K A., O. S. Pogrebinsky, G. T. Mrachko, L. Xi, D. J. Monticello, and C. H. Squires. 1996. Molecular mechanisms of biocatalytic desulfurization of fossil fuels. Nat. Biotechnol. 14:1705-1709.
    Pubmed CrossRef
  8. Guerinik, K. and Q. Al-Mutawah. 2003. Isolation and characterization of oil-desulfurizing bacteria. World J. Microbiol. Biotechnol. 19: 941-945.
    CrossRef
  9. Gunam, I. B. W., Y. Yaku, M. Hirano, K. Yamamura, F. Tomita, T. Sone, and K. Asano. 2006. Biodesulfurization of alkylated forms of dibenzothiophene and benzothiophene by Sphingomonas subarctica T7b. J. Biosci. Bioeng. 101: 322-327.
    Pubmed CrossRef
  10. Guobin, S., X. Jianmin, Z. Huaiying, and L. Huizhou. 2005. Deep desulfurization of hydrodesulfurized diesel oil by Pseudomonas delafieldii R-8. J. Chem. Technol. Biotechnol. 80: 420-424.
    CrossRef
  11. Hernández-Maldonado, A. J. and R. T. Yang. 2003. Desulfurization of commercial liquid fuels by selective adsorption via πcomplexation with Cu(I)-Y zeolite. Ind. Eng. Chem. Res. 42:3103-3110.
    CrossRef
  12. Kaufman, E. N., J. B. Harkins, and A. P. Borole. 1998. Comparison of batch stirred and electrospray reactors for biodesulfurization of dibenzothiophene in crude oil and hydrocarbon feedstocks. Appl. Biochem. Biotechnol. 73: 127144.
    CrossRef
  13. Kayser, K. J., B. A. Bielaga-Jone, K. Jackowski, O. Odusan, and J. J. Kilbane II. 1993. Utilization of organosulfur compounds by axenic and mixed cultures of Rhodococcus rhodochrous IGTS8. J. Gen. Microbiol. 39: 3123-3129.
    CrossRef
  14. Kayser, K. J., L. Cleveland, H. S. Park, J. H. Kwak, A. Kolhatkar, and J. J. Kilbane II. 2002. Isolation and characterization of a moderate thermophile, Mycobacterium phlei GTIS10, capable of dibenzothiophene desulfurization. Appl. Microbiol. Biotechnol. 59: 737-745.
    Pubmed CrossRef
  15. Kertesz, M. A. 1999. Riding the sulfur cycle metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol. Rev. 24: 135-175.
  16. Kim, B.-H., P.-K. Shin, J.-U. Na, D.-H. Park, and S.-H. Bang. 1996. Microbial petroleum desulfurization. J. Microbiol. Biotechnol. 6: 299-308.
  17. Kim, H. Y., T. S. Kim, and A. B. H. Kim. 1991. Isolation and characterization of a dibenzothiophene degrading sulfate-reducing soil bacterium. J. Microbiol. Biotechnol. 1: 1-5.
  18. Kobayashi, M., K. Horiuchi, O. Yoshikawa, K. Hirasawa, Y. Ishii, K. Fujino, et al. 2001. Kinetic analysis of microbial desulfurization of model and light gas oils containing multiple alkyl dibenzothiophenes. Biosci. Biotechnol. Biochem. 65: 298304.
    Pubmed CrossRef
  19. Konishi, J., Y. Ishii, T. Onaka, K. Okumura, and M. Suzuki. 1997. Thermophilic carbon-sulfur-bond-targeted biodesulfurization. Appl. Environ. Microbiol. 63: 3164-3169.
    Pubmed PMC
  20. Li, F., P. Xu, J. Feng, L. Meng, Y. Zheng, L. Luo, and C. Ma. 2005. Microbial desulfurization of gasoline in a Mycobacterium goodie X7B immobilized-cell system. Appl. Environ. Microbiol. 71: 276-281.
    Pubmed PMC CrossRef
  21. Li, Q., C. Kang, and C. Zhang. 2005. Waste water produced from an oilfield and continuous treatment with an oil-degrading bacterium. Process Biochem. 40: 873-877.
    CrossRef
  22. Lijun, X., W. Bochu, L. Zhimin, D. Chuanren, W. Qinghong, and L. Liu. 2005. Linear alkyl benzene sulfonate (LAS) degradation by immobilized Pseudomonas aeroginosa under low intensity ultrasound. Colloids Surf. B Biointerfaces 40: 25-29.
    Pubmed CrossRef
  23. Lu, J., T. Nakajima-Kambe, T. Shigeno, A. Ohbo, N. Nomura, and T. Nakahara. 1999. Biodegradation of dibenzothiophene and 4,6-dimethyldibenzothiophene by Sphingomonas pauchimobilis strain TZS-7. J. Biosci. Bioeng. 88: 293-299.
    CrossRef
  24. Luo, M. F., J. M. Xing, Z. X. Gou, S. Li, H. Z. Liu, and J. Y. Chen. 2003. Desulfurization of dibenzothiophene by lyophilized cells of Pseudomonas delafieldii R-8 in the presence of dodecane. Biochem. Eng. J. 13: 1-6.
    CrossRef
  25. Maghsoudi, S., A. Kheirolomoom, M. Vossoughi, E. Tanaka, and S. Katoh. 2001. Biodesulfurization of hydrocarbon by Rhodococcus sp. strain P32C1. Biochem. Eng. J. 8: 151-156.
    CrossRef
  26. Matsui, T., K. Hirasawa, K. Koizumi, K. Maruhashi, and R. Kurane. 2001. Optimization of the copy of number of dibenzothiophene desulfurizing genes to increase the desulfurization activity of recombinant Rhodococcus sp. Biotechnol. Lett. 23: 1715-1718.
    CrossRef
  27. Naito, M., T. Kawamoto, K. Fujino, M. Kobayashi, K. Maruhashi, and A. Tanaka. 2001. Long-term repeated biodesulfurization by immobilized Rhodococcus erythopolis KA2-5-1 cells. Appl. Microbiol. Biotechnol. 55: 374-378.
    Pubmed CrossRef
  28. Noda, K., K. Watanabe, and K. Maruhashi. 2003. Isolation of a recombinant desulfurizing 4,6-dipropyl dibenzothiophene in ntetradecane. J. Biosci. Bioeng. 95: 354-360.
    Pubmed
  29. Ohshiro, T., T. Hirata, and Y. Izumi. 1996. Desulfurization of dibenzothiophene derivates by whole cells of Rhodococcus erythopolis H-2. FEMS Microbiol. Lett. 142: 65-70.
    CrossRef
  30. Omori, T., L. Monna, Y. Saiki, and T. Kodama. 1992. Desulfurization of dibenzothiophene by Corynebacterium sp. strain SY1. Appl. Environ. Microbiol. 58: 911-915.
    Pubmed PMC
  31. Park, S. J., I.-S. Lee, Y. K. Chang, and S. Y. Lee. 2003. Desulfurization of dibenzothiophene and diesel oil by metabolically engineered Escherichia coli. J. Microbiol. Biotechnol. 13: 578583.
  32. Schiller, J. E. and D. R. Mathiason 1997. Separation method for coal-derived solids and heavy liquids. Anal. Chem. 49: 12251228
  33. Silveira, S. T., S. Gemelli, J. Segalin, and A. Brandelli. 2012. Immobilization of keratinolytic metalloprotease from Chryseobacterium sp. strain kr6 on glutaraldehyde-activated chitosan. J. Microbiol. Biotechnol. 22: 818-825.
    Pubmed CrossRef
  34. Szczesna-Antczak, M., T. Antczak, and S. Bielecki. 2004. Stability of extracellular proteinase productivity by Bacillus subtilis cells immobilized in PVA-cryogel. Enzyme Microb. Technol. 34: 168-176.
    CrossRef
  35. Tanaka, Y., T. Matsui, J. Konishi, K. Maruhashi, and R. Kurane. 2002. Biodesulfurization of benzothiophene and dibenzothiophene by a newly isolated Rhodococcus strain. Appl. Microbiol. Biotechnol. 59: 325-328.
    Pubmed CrossRef
  36. Watanabe, K., K. Noda, J. Konishi, and K. Maruhashi. 2003. Desulfurization of 2,4,6,8-tetraethyl dibenzothiophene by recombinant Mycobacterium sp. strain MR65. Biotechnol. Lett. 25: 1451-1456.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(4): 473-482

Published online April 28, 2013 https://doi.org/10.4014/jmb.1207.07070

Copyright © The Korean Society for Microbiology and Biotechnology.

Biodesulfurization of Dibenzothiophene and Its Derivatives Using Resting and Immobilized Cells of Sphingomonas subarctica T7b

Ida Bagus Wayan Gunam 1, Kenta Yamamura 2, I Nengah Sujaya 3, Nyoman Semadi Antara 1, Wayan Redi Aryanta 1, Michiko Tanaka 2, Fusao Tomita 4, Teruo Sone 2 and Kozo Asano 2*

1Laboratory of Bioindustry, Department of Agroindustrial Technology, Faculty of Agricultural Technology, Udayana University, Bali 80-362, Indonesia , 2Laboratory of Applied Microbiology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan, 3Laboratory of Bioscience and Biotechnology, Udayana University, Bali 80-362, Indonesia, 4The University of the Air, Hokkaido Study Center, Sapporo, Hokkaido 060-0817, Japan

Received: July 30, 2012; Accepted: December 1, 2012

Abstract

The desulfurization ability of Sphingomonas subarctica
T7b was evaluated using resting and immobilized cells
with dibenzothiophene (DBT), alkyl DBTs, and commercial
light gas oil (LGO) as the substrates. The resting cells of
S. subarctica T7b degraded 239.2 mg of the initial 250 mg
of DBT/l (1.36 mM) within 24 h at 27oC, while 127.5 mg of
2-hydroxybiphenyl (2-HBP)/l (0.75 mM) was formed,
representing a 55% conversion of the DBT. The DBT
desulfurization activity was significantly affected by the
aqueous-to-oil phase ratio. In addition, the resting cells of
S. subarctica T7b were able to desulfurize alkyl DBTs with
long alkyl chains, although the desulfurization rate
decreased with an increase in the total carbon number of
the alkylated DBTs. LGO with a total sulfur content of
280 mg/l was desulfurized to 152 mg/l after 24 h of reaction.
Cells immobilized by entrapment with polyvinyl alcohol
(PVA) exhibited a high DBT desulfurization activity,
including repeated use for more than 8 batch cycles
without loss of biodesulfurization activity. The stability of
the immobilized cells was better than that of the resting
cells at different initial pHs, higher temperatures, and for
DBT biodesulfurization in successive degradation cycles.
The immobilized cells were also easily separated from the
oil and water phases, giving this method great potential
for oil biodesulfurization.

Keywords: Biodesulfurization, dibenzothiophene, resting cells, immobilized cells, Sphingomonas subarctica

References

  1. Bahuguna, A., M. K. Lily, A. Munjal, R. N. Singh, and K. Dangwal. 2011. Desulfurization of dibenzothiophene (DBT) by a novel strain Lysinibacillus sphaericus DMT-7 isolated from diesel contaminated soil. J. Environ. Sci. 23: 975-982.
    CrossRef
  2. Chang, J. H., Y. K. Chang, K. S. Cho, and H. N. Chang. 2000. Desulfurization of model oils by resting cells of Gordonia sp. Biotechnol. Lett. 22: 193-196.
    CrossRef
  3. Dursun, A. Y. and O. Tepe. 2005. Internal mass transfer effect on biodegradation of phenol by Ca-alginate immobilized Ralstonia eutropha. J. Hazard. Mater. 126: 105-111.
    Pubmed CrossRef
  4. Fernandes, P., P. Vidinha, T. Ferreira, H. Silvestre, J. M. S. Cabral, and D. M. F. Prazeres. 2002. Use of free and immobilized Pseudomonas putida cells for the reduction of a thiophene derivative in organic media. J. Mol. Catal. B Enzym. 19: 353361.
    CrossRef
  5. Gallagher, J. R., S. S. Olson, and D. C. Stanley. 1993. Microbial desulfurization of benzothiophene: A sulfur specific pathway. FEMS Microbiol. Lett. 107: 31-36.
    Pubmed CrossRef
  6. Giuliano, M., C. Schiraldi, C. Maresca, V. Esposito, and M. D. Rosa. 2003. Immobilized Proteus mirabilis in poly(vinyl alcohol) cryogels for l (−)-carnitine production. Enzyme Microb. Technol. 32: 507-512.
    CrossRef
  7. Gray, K A., O. S. Pogrebinsky, G. T. Mrachko, L. Xi, D. J. Monticello, and C. H. Squires. 1996. Molecular mechanisms of biocatalytic desulfurization of fossil fuels. Nat. Biotechnol. 14:1705-1709.
    Pubmed CrossRef
  8. Guerinik, K. and Q. Al-Mutawah. 2003. Isolation and characterization of oil-desulfurizing bacteria. World J. Microbiol. Biotechnol. 19: 941-945.
    CrossRef
  9. Gunam, I. B. W., Y. Yaku, M. Hirano, K. Yamamura, F. Tomita, T. Sone, and K. Asano. 2006. Biodesulfurization of alkylated forms of dibenzothiophene and benzothiophene by Sphingomonas subarctica T7b. J. Biosci. Bioeng. 101: 322-327.
    Pubmed CrossRef
  10. Guobin, S., X. Jianmin, Z. Huaiying, and L. Huizhou. 2005. Deep desulfurization of hydrodesulfurized diesel oil by Pseudomonas delafieldii R-8. J. Chem. Technol. Biotechnol. 80: 420-424.
    CrossRef
  11. Hernández-Maldonado, A. J. and R. T. Yang. 2003. Desulfurization of commercial liquid fuels by selective adsorption via πcomplexation with Cu(I)-Y zeolite. Ind. Eng. Chem. Res. 42:3103-3110.
    CrossRef
  12. Kaufman, E. N., J. B. Harkins, and A. P. Borole. 1998. Comparison of batch stirred and electrospray reactors for biodesulfurization of dibenzothiophene in crude oil and hydrocarbon feedstocks. Appl. Biochem. Biotechnol. 73: 127144.
    CrossRef
  13. Kayser, K. J., B. A. Bielaga-Jone, K. Jackowski, O. Odusan, and J. J. Kilbane II. 1993. Utilization of organosulfur compounds by axenic and mixed cultures of Rhodococcus rhodochrous IGTS8. J. Gen. Microbiol. 39: 3123-3129.
    CrossRef
  14. Kayser, K. J., L. Cleveland, H. S. Park, J. H. Kwak, A. Kolhatkar, and J. J. Kilbane II. 2002. Isolation and characterization of a moderate thermophile, Mycobacterium phlei GTIS10, capable of dibenzothiophene desulfurization. Appl. Microbiol. Biotechnol. 59: 737-745.
    Pubmed CrossRef
  15. Kertesz, M. A. 1999. Riding the sulfur cycle metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol. Rev. 24: 135-175.
  16. Kim, B.-H., P.-K. Shin, J.-U. Na, D.-H. Park, and S.-H. Bang. 1996. Microbial petroleum desulfurization. J. Microbiol. Biotechnol. 6: 299-308.
  17. Kim, H. Y., T. S. Kim, and A. B. H. Kim. 1991. Isolation and characterization of a dibenzothiophene degrading sulfate-reducing soil bacterium. J. Microbiol. Biotechnol. 1: 1-5.
  18. Kobayashi, M., K. Horiuchi, O. Yoshikawa, K. Hirasawa, Y. Ishii, K. Fujino, et al. 2001. Kinetic analysis of microbial desulfurization of model and light gas oils containing multiple alkyl dibenzothiophenes. Biosci. Biotechnol. Biochem. 65: 298304.
    Pubmed CrossRef
  19. Konishi, J., Y. Ishii, T. Onaka, K. Okumura, and M. Suzuki. 1997. Thermophilic carbon-sulfur-bond-targeted biodesulfurization. Appl. Environ. Microbiol. 63: 3164-3169.
    Pubmed KoreaMed
  20. Li, F., P. Xu, J. Feng, L. Meng, Y. Zheng, L. Luo, and C. Ma. 2005. Microbial desulfurization of gasoline in a Mycobacterium goodie X7B immobilized-cell system. Appl. Environ. Microbiol. 71: 276-281.
    Pubmed KoreaMed CrossRef
  21. Li, Q., C. Kang, and C. Zhang. 2005. Waste water produced from an oilfield and continuous treatment with an oil-degrading bacterium. Process Biochem. 40: 873-877.
    CrossRef
  22. Lijun, X., W. Bochu, L. Zhimin, D. Chuanren, W. Qinghong, and L. Liu. 2005. Linear alkyl benzene sulfonate (LAS) degradation by immobilized Pseudomonas aeroginosa under low intensity ultrasound. Colloids Surf. B Biointerfaces 40: 25-29.
    Pubmed CrossRef
  23. Lu, J., T. Nakajima-Kambe, T. Shigeno, A. Ohbo, N. Nomura, and T. Nakahara. 1999. Biodegradation of dibenzothiophene and 4,6-dimethyldibenzothiophene by Sphingomonas pauchimobilis strain TZS-7. J. Biosci. Bioeng. 88: 293-299.
    CrossRef
  24. Luo, M. F., J. M. Xing, Z. X. Gou, S. Li, H. Z. Liu, and J. Y. Chen. 2003. Desulfurization of dibenzothiophene by lyophilized cells of Pseudomonas delafieldii R-8 in the presence of dodecane. Biochem. Eng. J. 13: 1-6.
    CrossRef
  25. Maghsoudi, S., A. Kheirolomoom, M. Vossoughi, E. Tanaka, and S. Katoh. 2001. Biodesulfurization of hydrocarbon by Rhodococcus sp. strain P32C1. Biochem. Eng. J. 8: 151-156.
    CrossRef
  26. Matsui, T., K. Hirasawa, K. Koizumi, K. Maruhashi, and R. Kurane. 2001. Optimization of the copy of number of dibenzothiophene desulfurizing genes to increase the desulfurization activity of recombinant Rhodococcus sp. Biotechnol. Lett. 23: 1715-1718.
    CrossRef
  27. Naito, M., T. Kawamoto, K. Fujino, M. Kobayashi, K. Maruhashi, and A. Tanaka. 2001. Long-term repeated biodesulfurization by immobilized Rhodococcus erythopolis KA2-5-1 cells. Appl. Microbiol. Biotechnol. 55: 374-378.
    Pubmed CrossRef
  28. Noda, K., K. Watanabe, and K. Maruhashi. 2003. Isolation of a recombinant desulfurizing 4,6-dipropyl dibenzothiophene in ntetradecane. J. Biosci. Bioeng. 95: 354-360.
    Pubmed
  29. Ohshiro, T., T. Hirata, and Y. Izumi. 1996. Desulfurization of dibenzothiophene derivates by whole cells of Rhodococcus erythopolis H-2. FEMS Microbiol. Lett. 142: 65-70.
    CrossRef
  30. Omori, T., L. Monna, Y. Saiki, and T. Kodama. 1992. Desulfurization of dibenzothiophene by Corynebacterium sp. strain SY1. Appl. Environ. Microbiol. 58: 911-915.
    Pubmed KoreaMed
  31. Park, S. J., I.-S. Lee, Y. K. Chang, and S. Y. Lee. 2003. Desulfurization of dibenzothiophene and diesel oil by metabolically engineered Escherichia coli. J. Microbiol. Biotechnol. 13: 578583.
  32. Schiller, J. E. and D. R. Mathiason 1997. Separation method for coal-derived solids and heavy liquids. Anal. Chem. 49: 12251228
  33. Silveira, S. T., S. Gemelli, J. Segalin, and A. Brandelli. 2012. Immobilization of keratinolytic metalloprotease from Chryseobacterium sp. strain kr6 on glutaraldehyde-activated chitosan. J. Microbiol. Biotechnol. 22: 818-825.
    Pubmed CrossRef
  34. Szczesna-Antczak, M., T. Antczak, and S. Bielecki. 2004. Stability of extracellular proteinase productivity by Bacillus subtilis cells immobilized in PVA-cryogel. Enzyme Microb. Technol. 34: 168-176.
    CrossRef
  35. Tanaka, Y., T. Matsui, J. Konishi, K. Maruhashi, and R. Kurane. 2002. Biodesulfurization of benzothiophene and dibenzothiophene by a newly isolated Rhodococcus strain. Appl. Microbiol. Biotechnol. 59: 325-328.
    Pubmed CrossRef
  36. Watanabe, K., K. Noda, J. Konishi, and K. Maruhashi. 2003. Desulfurization of 2,4,6,8-tetraethyl dibenzothiophene by recombinant Mycobacterium sp. strain MR65. Biotechnol. Lett. 25: 1451-1456.
    Pubmed CrossRef