Skip to main content
Log in

Dibenzothiophene desulfurization capability and evolutionary divergence of newly isolated bacteria

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Metabolically microorganisms are diverse, and they are capable of transforming almost every known group of chemical compounds present in coal and oil in various forms. In this milieu, one of the important microbial metabolic processes is the biodesulfurization [cleavage of carbon–sulfur (C–S) bond] of thiophenic compounds, such as dibenzothiophene (DBT), which is the most abundant form of organic sulfur present in fossil fuels. In the current study, ten newly isolated bacterial isolates, designated as species of genera Gordonia, Amycolatopsis, Microbacterium and Mycobacterium, were enriched from different samples in the presence of DBT as a sole source of organic sulfur. The HPLC analysis of the DBT grown cultures indicated the consumption of DBT and accumulation of 2-hydroxybiphenyl (2-HBP). Detection of 2-HBP, a marker metabolite of 4S (sulfoxide–sulfone–sulfinate–sulfate) pathway, suggested that the newly isolated strains harbored metabolic activity for DBT desulfurization through the cleavage of C–S bond. The maximum 2-HBP formation rate was 3.5 µmol/g dry cell weight (DCW)/h. The phylogenetic analysis of the new isolates showed that they had diverse distribution within the phylogenetic tree and formed distinct clusters, suggesting that they might represent strains of already reported species or they were altogether new species. Estimates of evolutionary divergence showed high level of nucleotide divergence between the isolates within the same genus. The new isolates were able to use a range of heterocyclic sulfur compounds, thus making them suitable candidates for a robust biodesulfurization system for fossil fuels.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abin Fuentes A, Leung JC, Mohamed MES, Wang DIC, Prather KLJ (2014) Rate limiting step analysis of the microbial desulfurization of dibenzothiophene in a model oil system. Biotechnol Bioeng 111:876–884

    Article  CAS  PubMed  Google Scholar 

  • Aggarwal S, Karimi IA, Ivan GR (2013) In silico modeling and evaluation of Gordonia alkanivorans for biodesulfurization. Mol BioSyst 9:2530–2540

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Alves L, Salgueiro R, Rodrigues C, Mesquita E, Matos J, Girio FM (2005) Desulfurization of dibenzothiophene, benzothiophene, and other thiophene analogs by a newly isolated bacterium, Gordonia alkanivorans strain 1B. Appl Biochem Biotechnol 120:199–208

    Article  CAS  PubMed  Google Scholar 

  • Arenskötter M, Bröker D, Steinbüchel A (2004) Biology of the metabolically diverse genus Gordonia. Appl Environ Microbiol 70:3195–3204

    Article  PubMed  PubMed Central  Google Scholar 

  • Ausbel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1995) Short protocols in molecular biology, 3rd edn. Wiley, New York

    Google Scholar 

  • Bhatia S, Sharma DK (2010) Biodesulfurization of dibenzothiophene, its alkylated derivatives and crude oil by a newly isolated strain Pantoea agglomerans D23W3. Biochem Eng J 50:104–109

    Article  CAS  Google Scholar 

  • Boniek D, Figueiredo D, Pylro VS, Duarte GF (2010) Characterization of bacterial strains capable of desulphurization in soil and sediment samples from Antarctica. Extremophiles 14:475–481

    Article  CAS  PubMed  Google Scholar 

  • Buzanello EB, Rezende RP, Sousa FMO, Marques ELS, Loguercio LL (2014) A novel Bacillus pumilus related strain from tropical landfarm soil is capable of rapid dibenzothiophene degradation and biodesulfurization. BMC Microbiol 14(1):257

    PubMed  PubMed Central  Google Scholar 

  • Chen H, Zhang WJ, Chen JM, Cai YB, Li W (2008) Desulfurization of various organic sulfur compounds and the mixture of DBT+ 4, 6-DMDBT by Mycobacterium sp. ZD-19. Bioresour Technol 99:3630–3634

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Cai YB, Zhang WJ, Li W (2009) Methoxylation pathway in biodesulfurization of model organosulfur compounds with Mycobacterium sp. Bioresour. Technol 100:2085–2087

    Article  CAS  PubMed  Google Scholar 

  • Eriksen J (2008) Soil sulfur cycling in temperate agricultural system. In: Sulfur: a missing link between soils, crops, and nutrition. ASA-CSSA-SSSA

  • Gallagher JR, Olson ES, Stanley DC (1993) Microbial desulfurization of dibenzothiophene: a sulfur-specific pathway. FEMS Microbiol Lett 107:31–35

    Article  CAS  PubMed  Google Scholar 

  • Gupta N, Roychoudhury PK, Deb JK (2005) Biotechnology of desulfurization of diesel: prospects and challenges. Appl Microbiol Biotechnol 66:356–366

    Article  CAS  PubMed  Google Scholar 

  • Gurtler V, Mayall BC, Seviour R (2004) Can whole genome analysis refine the taxonomy of the genus Rhodococcus? FEMS Microbiol Rev 28:377–403

    Article  CAS  PubMed  Google Scholar 

  • Izumi Y, Ohshiro T, Ogino H, Hine Y (1994) Selective desulfurization of dibenzothiophene by Rhodococcus erythropolis D-1. Appl Environ Microbiol 60(1):223–226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kayser KJ, Cleveland L, Park HS, Kwak JH, Kolhatkar A, Kilbane JJ II (2002) Isolation and characterization of a moderate thermophile, Mycobacterium phlei GTIS10, capable of dibenzothiophene desulfurization. Appl Microbiol Biotechnol 59:737–746

    Article  CAS  PubMed  Google Scholar 

  • Kertesz MA (2000) Riding the sulfur cycle–metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol Rev 24:135–175

    CAS  PubMed  Google Scholar 

  • Kilbane JJ (1990) Sulfur-specific microbial-metabolism of organic-compounds. Resour Conserv Recycl 3(2–3):69–79

    Article  Google Scholar 

  • Kilbane JJ (1991) Bacterial produced extracts and enzymes for cleavage of organic C–S bonds. European Patent No. 0445896A2

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

    Article  CAS  PubMed  Google Scholar 

  • Li W, Zhang Y, Wang MD, Shi Y (2005) Biodesulfurization of dibenzothiophene and other organic sulfur compounds by a newly isolated Microbacterium strain ZD-M2. FEMS Microbiol Lett 247:45–50

    Article  CAS  PubMed  Google Scholar 

  • Li F, Zhang Z, Feng J, Cai X, Xu P (2007) Biodesulfurization of DBT in tetradecane and crude oil by a facultative thermophilic bacterium Mycobacterium goodii X7B. J Biotechnol 127:222–228

    Article  CAS  PubMed  Google Scholar 

  • Maass D, Todescato D, Moritz DE, Oliveira JV, Oliveira D, Ulson de Souza AA, Guelli Souza SM (2015) Desulfurization and denitrogenation of heavy gas oil by Rhodococcus erythropolis ATCC 4277. Bioprocess Biosyst Eng 38(8):1447–1453

    Article  CAS  PubMed  Google Scholar 

  • Mohamed ME-S, Al-Yacoub ZH, Vedakumar JV (2015) Biocatalytic desulfurization of thiophenic compounds and crude oil by newly isolated bacteria. Front Microbiol 6:1–12

    Article  Google Scholar 

  • Monticello DJ (2000) Biodesulfurization and the upgrading of petroleum distillates. Curr Opin Biotechnol 11:540–546

    Article  CAS  PubMed  Google Scholar 

  • Monticello DJ, Finnerty WR (1985) Microbial desulfurization of fossil fuels. Annu Rev Microbiol 39:371–389

    Article  CAS  PubMed  Google Scholar 

  • Nekodzuka S, Nakajima-Kambe T, Nomura N, Lu J, Nakahara T (1997) Specific desulfurization of dibenzothiophene by Mycobacterium sp. strain G3. Biocatal Biotransform 15:17–27

    Article  CAS  Google Scholar 

  • Nuhu AA (2013) Bio-catalytic desulfurization of fossil fuels: a mini review. Rev Environ Sci Biotechnol 12:9–23

    Article  CAS  Google Scholar 

  • Ohshiro T, Suzuki K, Izumi Y (1996) Regulation of dibenzothiophene degrading enzyme activity of Rhodococcus erythropolis D-1. J Ferment Bioeng 81:121–124

    Article  CAS  Google Scholar 

  • Oldfield C, Pogrebinsky O, Simmonds J, Olson ES, Kulpa CF (1997) Elucidation of the metabolic pathway for dibenzothiophene desulphurization by Rhodococcus sp. strain IGTS8 (ATCC 53968). Microbiology 143:2961–2973

    Article  CAS  PubMed  Google Scholar 

  • Rashtchi M, Mohebali GH, Akbarnejad MM, Towfighi J, Rasekh B, Keytash A (2006) Analysis of biodesulfurization of model oil system by the bacterium, strain RIPI-22. Biochem Eng J 29:169–173

    Article  CAS  Google Scholar 

  • Soleimani M, Bassi A, Margaritis A (2007) Biodesulphurization of refractory organic sulfur compounds in fossil fuels. Biotechnol Adv 25(6):570–596

    Article  CAS  PubMed  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) A place for DNA-DNA reassociation and 16S ribosomal-RNA sequence-analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Stoner DL, Wey JE, Barrett KB, Jolley JG, Wright RB, Dugan PR (1990) Modification of water-soluble coal-derived products by dibenzothiophene-degrading microorganisms. Appl Environ Microbiol 56:2667–2676

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Matsui T, Konishi J, Maruhashi K, Kurane R (2002) Biodesulfurization of benzothiophene and dibenzothiophene by a newly isolated Rhodococcus strain. Appl Microbiol Biotechnol 59:325–328

    Article  CAS  PubMed  Google Scholar 

  • Ting MA, Shanshan LI, Guoqiang LI, Renjing WANG, Fenglai LIANG, Rulin LIU (2006) Cloning and expressing DBT (dibenzothiophene) monooxygenase gene (dsz C) from Rhodococcus sp. DS-3 in Escherichia coli. Front Biol China 4:375–380

    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(12):e84386

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research work was supported by the International Foundation for Science, Stockholm, Sweden, through a grant to Dr. Nasrin Akhtar (Research Grant Agreement No. F/5379-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nasrin Akhtar.

Ethics declarations

Conflict of interests

The authors declare that they have no conflict of interests.

Additional information

Communicated by Matthias Boll.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akhtar, N., Ghauri, M.A. & Akhtar, K. Dibenzothiophene desulfurization capability and evolutionary divergence of newly isolated bacteria. Arch Microbiol 198, 509–519 (2016). https://doi.org/10.1007/s00203-016-1209-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-016-1209-5

Keywords

Navigation