Skip to main content
Log in

Biodesulfurization: a model system for microbial physiology research

  • REVIEW
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Biological desulfurization (biodesulfurization) of dibenzothiophene (DBT) by the 4S pathway is a model system for an enviromentally benign way to lower the sulfur content of petroleum. Despite a large amount of effort the efficiency of the 4S pathway is still too low for a commercial oil biodesulfurization process, but the 4S pathway could potentially be used now for commercial processes to produce surfactants, antibiotics, polythioesters and other chemicals and for the detoxification of some chemical warfare agents. Proteins containing disulfide bonds are resistant to temperature, pH, and solvents, but the production of disulfide-rich proteins in microbial hosts is challenging. The study of the 4S pathway can provide insights as to how to maximize the production of disulfide-rich proteins. Engineering of the operon encoding the 4S pathway to contain a greater content of methionine and cysteine may be able to link use of DBT as a sole sulfur source to increasing 4S pathway activity by increasing the nutritional demand for sulfur. This strategy could result in the development of biocatalysts suitable for use in an oil biodesulfurization process, but the study of the 4S pathway can also lead to a better understanding of microbial physiology to optimize activity of a mult-step co-factor-requiring pathway, as well as the production of highly stable industrially relevant enzymes for numerous applications.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aggarwal S, Karimi IA, Kilbane JJ II, Lee DY (2012) Roles of sulfite oxidoreductase and sulfite reductase in improving desulfurization by Rhodococcus erythopolis. Mol BioSyst 8:2724–2732

    Article  CAS  Google Scholar 

  • Akhtar N, Ghauri MA, Anwar MA, Akhtar K (2009) Analysis of the dibenzothiophene metabolic pathway in a newly isolated Rhodococcus spp. FEMS Microbiol Lett 301:95–102

  • Alves L, Paixao SM, Pacheco R, Ferreira AF, Silva CM (2015) Biodesulfurization of fossil fuels: energy, emissions and cost analysis. RSC Adv 5:34047–34057

    Article  CAS  Google Scholar 

  • Bhasarkar JB, Dikshit PK, Moholkar VS (2015) Ultrasound assisted biodesulfurization of liquid fuel using free and immobilized cells of Rhodococcus rhodochrous MTCC 3552: a mechanistic investigation. Bioresour Technol 187:369–378

    Article  CAS  Google Scholar 

  • Biotechnology Market (2014) Biopharmacy, bioservices bioagriculture, bioindustrial, fermentation, DNA sequencing, tissue engineering, regeneration, analysis and segment forecasts to 2020. Grand View Research Inc, San Francisco

    Google Scholar 

  • Blair JMA, Weber MA, Baylay AJ, Ogbolu DO, Piddock LJV (2015) Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13:42–51

    Article  CAS  Google Scholar 

  • Boniek D, Figueredo D, Batista dos Santos AF, de Resende Stoianoff MA (2015) Biodesulfurization: a mini review about the immediate search for the future technology. Clean Technol Environ Policy 17:29–37

    Article  Google Scholar 

  • Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229

    Article  CAS  Google Scholar 

  • Chivers CJ (2015) Large stockpiles of VX and other chemical warfare agents are known to exist in Russia. New York Times, New York

    Google Scholar 

  • Debabov VG (2010) Microbial desulfurization of motor fuel. Appl Biochem Microbiol 46:733–738

    Article  CAS  Google Scholar 

  • Frillingos S, Sahin-Toth M, Wu J, Kaback HR (1998) Cys-scanning mutagenesis: a novel approach to structure-function relationships in polytopic membrane proteins. FASEB J 12:1281–1299

    CAS  Google Scholar 

  • Gopal GJ, Kumar A (2013) Strategies for the production of recombinant protein in Escherichia coli. Protein J 32:419–425

    Article  CAS  Google Scholar 

  • Jiang B, Yang H, Zhang L, Zhang R, Sun Y, Huang Y (2016) Efficient oxidative desulfurization of diesel fuel using amide-based ionic liquids. Chem Eng J 283:89–96

    Article  CAS  Google Scholar 

  • Kaspar AA, Reichert JM (2013) Future directions for peptide therapeutics development. Drug Discov Today 18:807–817

    Article  CAS  Google Scholar 

  • Kayser KJ, Cleveland L, Park H-S, Kwak J-H, Kolhatkar A, Kilbane JJ II (2002) Isolation and characterization of a moderate thermophile, Mycobacterium phlei GTIS10, capable of dibenzothiophene desulfurization. Appl Microbiol Biotechnol 59:737–745

    Article  CAS  Google Scholar 

  • Khairy H, Wubbeler JH, Steinbuchel A (2015) Biodegradation of the organic disulfide 4,4′-dithiodibutyric acid by Rhodococcus spp. Appl Environ Microbiol 81:8294–8306

    CAS  Google Scholar 

  • Kilbane JJ II (2006) Microbial biocatalyst developments to upgrade fossil fuels. Curr Opin Biotechnol 17:305–314

    Article  CAS  Google Scholar 

  • Kilbane JJ II (2016) Future applications of biotechnology to the energy industry. Front Microbiol 7(Article 86):1–4

    Google Scholar 

  • Kilbane JJ II, Jackowski K (1996) Biocatalytic detoxification of 2-chloroethyl ethyl sulfide. J Chem Technol Biotechnol 65:370–374

    Article  CAS  Google Scholar 

  • Kirimura K, Harada K, Iwasawa H, Tanaka T, Iwasaki Y, Furuya T, Ishii Y, Kino K (2004) Identification and functional analysis of the genes encoding dibenzothiophene-desulfurizing enzymes from thermophilic bacteria. Appl Microbiol Biotechnol 65:703–713

    Article  CAS  Google Scholar 

  • Klint JK, Senff S, Saez NJ, Seshadri R, Lau HY, Bende NS, Undheim EAB, Rash LD, Mobli M, King GF (2013) Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PloS One 8:e63865

    Article  CAS  Google Scholar 

  • Kurosawa K, Boccazzi P, deAlmeida NM, Sinskey AJ (2010) High-cell-density batch fermentation of Rhodococcus opacus PO630 using a high glucose concentration for triacylglycerol production. J Biotechnol 147:212–218

    Article  CAS  Google Scholar 

  • Li C-H, Chan T-H (2007) Comprehensive organic reactions in aqueous media. Wiley-Interscience, Wiley, Hoboken, NJ

    Book  Google Scholar 

  • Li FL, Xu P, Ma CQ, Luo LL, Wang XS (2003) Deep desulfurization of a hydrodesulfurization-treated diesel oil by a facultative thermophilic Mycobacterium sp. X7B. FEMS Microbiol Lett 223:301–307

    Article  CAS  Google Scholar 

  • Liaud N, Rosso M-N, Fabre N, Crapart S, Herpoel-Gimbert I, Sigoillot J-C, Raouche S, Levasseur A (2015) L-lactic acid production by Aspergillus braziliensis overexpressing the heterologous ldha gene from Rhizopus oryzae. Microb Cell Fact 14:66

    Article  Google Scholar 

  • Liu JL, Goldman ER, Zabetakis D, Walper SA, Turner KR, Shriver-Lake LC, Anderson GP (2015) Enhanced production of a single domain antibody with an engineered stabilizing extra disulfide bond. Microb Cell Fact 14:158

    Article  Google Scholar 

  • Marisch K, Bayer K, Cserjan-Puschmann M, Luchner M, Striedner G (2013) Evaluation of three industrial Escherichia coli strains in fed-batch cultivations during high-level SOD protein production. Microb Cell Fact 12:58

    Article  CAS  Google Scholar 

  • Northfield SE, Wang CK, Schroeder CI, Durek T, Kan MW, Swedberg JE, Craik DJ (2014) Disulfide-rich macrocyclic peptides as templates in drug design. Eur J Med Chem 77:248–257

    Article  CAS  Google Scholar 

  • Ohnishi S, Hays A, Hagenbuch B (2014) Cysteine scanning mutagenesis of transmembrane domain 10 in organic anion transporting polypeptide 1B1. Biochemistry 53:2261–2270

    Article  CAS  Google Scholar 

  • Ohshiro T, Ishii Y, Matsubara K, Ueda K, Izumi Y, Kino K, Kirimura K (2005) Dibenzothiophene desulfurizing enzymes from moderately thermophilic bacterium Bacillus subtilis WU-S2B: purification, characterization and over-expression. J Biosci Bioeng 100:266–273

    Article  CAS  Google Scholar 

  • Onaka T, Kobayashi M, Ishii Y, Konishi J, Matuhashi K (2001) Selective cleavage of the two C-S bonds in asymmetrically alkylated dibenzothiophenes by Rhodococcus erythropolis KA2-5-1. J Biosci Bioeng 92:80–82

    Article  CAS  Google Scholar 

  • Pan J, Wu F, Wang J, Xu L, Khayyat NH, Stark BC, Kilbane JJ II (2013) Enhancement of desulfurization activity by enzymes of the Rhodococcus dsz operon through coexpression of a high sulfur peptide and directed evolution. Fuel 112:385–390

    Article  CAS  Google Scholar 

  • Paul M, van der Donk WA (2005) Chemical and enzymatic synthesis of lanthionines. Mini Rev Org Chem 2:23–37

    Article  CAS  Google Scholar 

  • Prokop Z, Oplustil F, DeFrank J, Damborsky J (2006) Enzymes fight chemical weapons. Biotechnol J 1:1370–1380

    Article  CAS  Google Scholar 

  • Stanislaus A, Marafi A, Rana MS (2010) Recent advances in the science and technology of ultra low sulfur diesel (ULSD) production. Catal Today 15:1–68

    Article  Google Scholar 

  • Vecchiarelli AG, Funnell BE (2013) Probing the N-terminus of ParB using cysteine-scanning mutagenesis and thiol modification. Plasmid 70:86–93

    Article  CAS  Google Scholar 

  • Wang W, Ma T, Lian K, Zhang Y, Tian H, Ji K, Li G (2013) Genetic analysis of benzothiophene biodesulfurization pathway of Gordonia terrae strain C-6. PloS One 8:e84386

    Article  Google Scholar 

  • Wang J, Davaadelger B, Salazar JK, Butler RR, Pombert JF, Kilbane JJ II, Stark BC (2015) Isolation and characterization of an interactive culture of two Paenibacillus species with moderately thermophilic desulfurization ability. Biotechnol Lett 37:2201–2211

    Article  CAS  Google Scholar 

  • Yacoub HA, El-Hamidy SM, Mahmoud MM, Baeshen MN, Almehdar HA, Uversky VN, Redwan EM, Al-Maghrabi OA, Elazzaz AM (2016) Biocidal activity of chicken defensin-9 against microbial pathogens. Biochem Cell Biol 94:176–187

  • Yu B, Tao F, Li F, Hou J, Tang H, Ma C, Xu P (2015) Complete genome sequence of Mycobacterium goodie X7B, a facultative thermophilic biodesulfurization bacterium with industrial potential. J Biotechnol 212:56–57

    Article  CAS  Google Scholar 

  • Zhang SH, Chen H, Li W (2013) Kinetic analysis of biodesulfurization of model oil containing multiple alkyl dibenzothiophenes. Appl Microbiol Biotechnol 97:2193–2200

    Article  CAS  Google Scholar 

  • Zhang J, Quan C, Wang C, Wu H, Li Z, Ye Q (2016) Systematic manipulation of glutathione metabolism in Escherichia coli for improved glutathione production. Microb Cell Fact 15:38

    Article  Google Scholar 

  • Zhou Y, Liu P, Gan Y, Sandoval W, Katakam AK, Reichelt M, Rangell L, Reilly D (2016) Enhancing full-length antibody production by signal peptide engineering. Microb Cell Fact 15:47

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John J. Kilbane II.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kilbane, J.J., Stark, B. Biodesulfurization: a model system for microbial physiology research. World J Microbiol Biotechnol 32, 137 (2016). https://doi.org/10.1007/s11274-016-2084-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-016-2084-6

Keywords

Navigation