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Biodesulfurization of refractory sulfur compounds in petro-diesel by a novel hydrocarbon tolerable strain Paenibacillus glucanolyticus HN4

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Abstract

One of the main precursors of air pollution and acid rains is the presence of the recalcitrant thiophenic compounds, for example dibenzothiophene (DBT) and its derivatives in transportation fuels. In an attempt to achieve the worldwide regulations of ultra-low sulfur transportation fuels without affecting its hydrocarbon skeleton, a biphasic medium containing 100 mg/L DBT dissolved in n-hexadecane (1/4 oil/water v/v) used for enrichment and isolation of selective biodesulfurizing bacterium from an oil-polluted sediment sample collected from Egyptian Red Sea shoreline. The isolated bacterium is facultative anaerobe, motile, spore-former, and mesophile. It is genetically identified as Paenibacillus glucanolyticus strain HN4 (NCBI Gene Bank Accession No. MT645230). HN4 desulfurized DBT as a model of the recalcitrant thiophenic compounds without affecting its hydrocarbon skeleton via the 4S-pathway producing 2-hydroxybiphenyl (2-HBP) as a dead end product. HN4 substantiated to be a hydrocarbon tolerant, biosurfactants(s) producer, and endorsed unique enzymatic system capable of desulfurizing broad range of thiophenic compounds and expressed an efficient desulfurization activity against the recalcitrant alkylated DBTs. As far our knowledge, it is the first reported BDS study using P. glucanolyticus. Statistical optimization based on One-Factor-At-A-Time (OFAT) technique and response surface methodology (RSM) applied for elucidation of mathematical model correlations describing and optimizing the effect of different physicochemical parameters on batch biphasic BDS process. That illustrated an approximate increase in BDS efficiency by 1.34 fold and recorded 94% sulfur removal in biphasic batch process at optimum operation conditions of 120 h, 0.14 wt% S-content model oil (DBT dissolved in n-hexadecane), 33.5 °C, pH7 and 1/1 oil/water phase ratio, and 147 rpm. Resting cells of HN4 in a biphasic reactor (1/1 v/v) decreased the sulfur content of a refractory thiophenic model oil (thiophene, benzothiophene, DBT, and alkylated DBT dissolved in n-hexadecane) from 0.14 to 0.027 wt%, and petro-diesel from 0.2 to 0.04 wt%, within 120 h, keeping the calorific value of the treated fuel intact. Consequently, that novel strain could be recommended as a promising candidate for BDS as complementary to hydrodesulfurization process in oil refinery.

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References

  • Abid MF, Ahmed SM, AbuHamid WH, Ali SM (2019) Study on novel scheme for hydrodesulfurization of middle distillates using different types of catalyst. J King Saud Univ Eng Sci 31:144–151

    Google Scholar 

  • Abin-Fuentes A, Leung J, Mohamed M, Wang D, Prather K (2014) Rate-limiting step analysis of the microbial desulfurization of dibenzothiophene in a model oil system. Biotechnol Bioeng 111(5):876–884

    Article  CAS  Google Scholar 

  • Acero J, Berdugo C, Mogollón L (2003) Biodesulfurization process evaluation with a Gordona rubropertinctus strain. CT F Cienc Tecnol Futuro 2(4):43–54

    CAS  Google Scholar 

  • Agarwal P, Sharma DK (2010) Comparative studies on the biodesulfurization of crude oil with other desulfurization techniques and deep desulfurization through integrated processes. Energy Fuel 24(1):518–524

    Article  CAS  Google Scholar 

  • Akhtar N, Akhtar K, Ghauri MA (2018) Biodesulfurization of thiophenic compounds by a 2-hydroxybiphenyl-resistant Gordonia sp. HS126-4 N carrying dszABC genes. Curr Microbiol 75:597–603

    Article  CAS  Google Scholar 

  • Alcon A, Santos VE, Martin AB, Yustos P, Garcia-Ochoa F (2005) Biodesulfurization of DBT with pseudomonas putida CECT5279 by resting cells influence of cell growth time on reducing equivalent concentration and Hpac activity. Biochem Eng 26:168–175

    Article  CAS  Google Scholar 

  • Ali HR, Ismail DA, El-Gendy NS (2014) The biotreatment of oil-polluted seawater by biosurfactant producer halotolerant Pseudomonas aeruginosa Asph2. Energ Source Part A 36:1429–1436

    Article  CAS  Google Scholar 

  • Amin GA, Bazaid SA, El-Halim MA (2013) Two-stage immobilized cell bioreactor with Bacillus subtilis and Rhodococcus erythropolis for the simultaneous production of biosurfactant and biodesulfurization of model oil. Pet Sci Technol 31(21):2250–2257

    Article  CAS  Google Scholar 

  • ASTM D240 – 19 “Standard test method for heat of combustion of liquid hydrocarbon fuels by bomb calorimeter”.

  • ASTM D4294 - 03 “Standard test method for sulfur in petroleum and petroleum products by energy-dispersive X-ray fluorescence spectrometry”.

  • Bahuguna A, Lily MK, Munjal A, Singh RN, Dangwal K (2011) Desulfurization of dibenzothiophene (DBT) by a novel strain Lysinibacillus sphaericus DMT-7 isolated from diesel contaminated soil. J Environ Sci 23(6):975–982

    Article  CAS  Google Scholar 

  • Bailey JE, Ollis DF (1986) Biochemical engineering fundamental 2nd ed. McGraw-Hill, New York, USA

    Google Scholar 

  • Barrios SMY (2011) Bioremediation: a tool for the management of oil pollution in marine ecosystems. Biotecnol Apl 28:69–76

    Google Scholar 

  • Bhanjadeo MM, Rath K, Gupta D, Pradhan N, Biswal SK, Mishra BK, Subudhi U (2018) Differential desulfurization of dibenzothiophene by newly identified MTCC strains: influence of operon array. PLoS One 13(3):e0192536. https://doi.org/10.1371/journal.pone.0192536

    Article  CAS  Google Scholar 

  • Bordoloi NK, Rai SK, Chaudhuri MK, Mukherjee AK (2014) Deep-desulfurization of dibenzothiophene and its derivatives present in diesel oil by a newly isolated bacterium Achromobacter sp. to reduce the environmental pollution from fossil fuel combustion. Fuel Process Technol 119:236–244

    Article  CAS  Google Scholar 

  • Calzada J, Zamarro MT, Alcón A (2009) Analysis of dibenzothiophene desulfurization in a recombinant pseudomonas putida strain. Appl Environ Microbiol 75(3):875–877

    Article  CAS  Google Scholar 

  • Canales C, Eyzaguirre J, Baeza P, Aballay P, Ojeda J (2018) Kinetic analysis for biodesulfurization of dibenzothiophene using R. rhodochrous adsorbed on silica. Ecol Chem Eng S 25(4):549–556

    CAS  Google Scholar 

  • Caro A, Boltes K, Leton P, García-Calvo E (2008) Biodesulfurization of dibenzothiophene by growing cells of Pseudomonas putida CECT 5279 in biphasic media. Chemosphere 73:663–669

    Article  CAS  Google Scholar 

  • Caro A, Boltes K, Letón P, García-Calvo E (2007) Dibenzothiophene biodesulfurization in resting cell conditions by aerobic bacteria. Biochem Eng J 35:191–197

    Article  CAS  Google Scholar 

  • Chen S, Zhao C, Liu Q, Zang M, Liu C, Zhang Y (2018) Thermophilic biodesulfurization and its application in oil desulfurization. Appl Microbiol Biotechnol 102:9089–9103

    Article  CAS  Google Scholar 

  • Chen S, Zhao C, Liu Q, Zhang X, Sun S, Zang M (2019) Biodesulfurization of diesel oil in oil–water two phase reaction system by Gordonia sp. SC-10. Biotechnol Lett 41:547–554

    Article  CAS  Google Scholar 

  • Davoodi-Dehaghani F, Vosoughi M, Ziaee AA (2010) Biodesulfurization of dibenzothiophene by a newly isolated Rhodococcus erythropolis strain. Bioresour Technol 101:1102–1105

    Article  CAS  Google Scholar 

  • Derikvand P, Etemadifar Z, Saber H (2015) Sulfur removal from dibenzothiophene by newly isolated Paenibacillus validus strain PD2 and process optimization in aqueous and biphasic (model-oil) systems. Pol J Microbiol 64(1):47–54

    Article  Google Scholar 

  • Dinamarca MA, Rojas A, Baeza P, Espinoza G, Ibacache-Quiroga C, Ojeda J (2014) Optimizing the biodesulfurization of gas oil by adding surfactants to immobilized cell systems. Fuel 116:237–241

    Article  CAS  Google Scholar 

  • El-Gendy NS, Nassar HN, Abu Amr SS (2014) Factorial design and response surface optimization for enhancing a biodesulfurization process. Pet Sci Technol 32(14):1669–1679

    Article  CAS  Google Scholar 

  • El-Gendy NS, Nassar HN (2015) Kinetic modeling of the bioremediation of diesel oil polluted seawater using Pseudomonas aeruginosa NH1. Energ Source Part A 37(11):1147–1163

    Article  CAS  Google Scholar 

  • Folsom BR, Schieche DR, Digrazia PM, Werner J, Palmer S (1999) Microbial desulfurization of alkylated dibenzothiophenes from a hydrodesulfurized middle distillate by Rhodococcus erythropolis I-19. Appl Environ Microbiol 65(11):4967–4972

    Article  CAS  Google Scholar 

  • Furuya T, Kirimura K, Kino K, Usami S (2001) Thermophilic biodesulfurization of dibenzothiophene and its derivatives by Mycobacterium Phlei WU-F1. FEMS Microb Lett 24:129–133

    Article  Google Scholar 

  • Ghafari S, Baboli Z, Neisi A, Mirzaee SA, Soltani RDC, Saeedi R, Abtahi M, Jorfi S (2019) Surfactant-enhanced bioremediation of n-hexadecane-contaminated soil using halo-tolerant bacteria Paenibacillus glucanolyticus sp. strain T7-AHV isolated from marine environment. Chem Biochem Eng Q 33(1):111–123

    Article  CAS  Google Scholar 

  • Gunam IBW, Yaku Y, Hirano M (2006) Biodesulfurization of alkylated forms of dibenzothiophene and benzothiophene by Sphingomonas subarctica T7b. J Biosci Bioeng 101:322–327

    Article  CAS  Google Scholar 

  • Heidarinasab A, Soltanieh M, Ardjmand M, Ahmadpanahi H, Bahmani M (2016) Comparison of Mo/MgO and Mo/ɣ-Al2O3 catalysts: impact of support on the structure and dibenzothiophene hydrodesulfurization reaction pathways. Int J Environ Sci Technol 13:1065–1076

    Article  CAS  Google Scholar 

  • Ismail W, El-Said W, Raheem ASA, Mohamed ME, El Nayal AM (2016) Biocatalytic desulfurization capabilities of a mixed culture during non-destructive utilization of recalcitrant organosulfur compounds. Front Microbiol 7:1–14

    Google Scholar 

  • Kaufman EN, Harkins JB, Borole AP (1998) Comparison of batchstirred and electrospray reactors for biodesulfurization of dibenzothiophene in crude oil and hydrocarbon feedstocks. Appl Biochem Biotechnol 73(2/3):27–144

    Google Scholar 

  • Kawaguchi H, Kobayashi H, Sato K (2012) Metabolic engineering of hydrophobic Rhodococcus opacus for biodesulfurization in oil-water biphasic reaction mixtures. J Biosci Bioeng 113:360–366

    Article  CAS  Google Scholar 

  • Kim YJ, Chang JH, Cho K, Ryu HW, Chang YK (2004) A physiological study on growth and dibenzothiophene (DBT) desulfurization characteristics of Gordonia sp. CYKS1. Korean J Chem Eng 21:436–441

    Article  CAS  Google Scholar 

  • Kobayashi M, Horiuchi K, Yoshikawa O, Hirasawa K, Ishii Y, Fujino K, Sugiyama H, Maruhashi K (2001) Kinetic analysis of microbial desulfurization of model and light gas oils containing multiple alkyl debenzothiophenes. Biosci Biotechnol Biochem 65(2):298–304

    Article  CAS  Google Scholar 

  • Kobayashi M, Onaka T, Ishii Y, Konishi J, Takaki M, Okada H, Ohta Y, Koizumi K, Suzuki M (2000) Desulfurization of alkylated forms of both dibenzothiophene and benzothiophene by a single bacterial strain. FEMS Microbiol Lett 87:123–126

    Article  Google Scholar 

  • Konishi J, Ishii Y, Onaka T, Okumura K, Suzuki M (1997) Thermophilic carbon-sulfur-bond-targeted biodesulfurization. Appl Environ Microbiol 63(8):3164–3169

    Article  CAS  Google Scholar 

  • Konishi J, Onaka T, Ishii Y, Suzuki M (2000) Demonstration of the carbon-sulfur bond targeted desulfurization of benzothiophene by thermophilic Paenibacillus sp. strain A11-2 capable of desulfurizing dibenzothiophene. FEMS Microbiol Lett 187:151–154

    Article  CAS  Google Scholar 

  • Lateef SA, Ajumobi OO, Onaiz SA (2019) Enzymatic desulfurization of crude oil and its fractions: a mini review on the recent progresses and challenges. Arab J Sci Eng 44:5181–5193

    Article  CAS  Google Scholar 

  • Lee HK, Khaine I, Kwak MJ, Jang JH, Lee TY, Lee JK, Kim IR, Kim WI, Oh KS, Woo SY (2017) The relationship between SO2 exposure and plant physiology: a mini review. Hortic Environ Biotechnol 58(6):523–529

    Article  CAS  Google Scholar 

  • Li F, Xu P, Feng J, Meng L, Zheng Y, Luo L, Ma C (2006) Microbial desulfurization of gasoline in a Mycobacterium goodii X7B immobilized-cell system. Appl Environ Microbiol 71:276–281

    Article  CAS  Google Scholar 

  • Li W, Jiang X (2013) Enhancement of bunker oil biodesulfurization by adding surfactant. World J Microbiol Biotechnol 29:103–108

    Article  CAS  Google Scholar 

  • Luo MF, Xing JM, Gou ZX, Li S, Liu HZ, Chen JY (2003) Desulfurization of dibenzothiophene by lyophilized of Pseudomonas delafieldii R-8 in the presence of dodecane. Biochem Eng J 13:1–6

    Article  CAS  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 38:1447–1453

    Article  CAS  Google Scholar 

  • Martínez I, Mohamed ME, Rozas D, García JL, Díaz E (2016) Engineering synthetic bacterial consortia for enhanced desulfurization and revalorization of oil sulfur compounds. Metab Eng 35:46–54

    Article  CAS  Google Scholar 

  • Matsubara TT, Ohshiro T, Nishina Y, Izumi Y (2001) Purification, characterization, and over expression of flavin reductase involved in dibenzothiophene desulfurization by Rhodococcus erythropolis D-1. Appl Environ Microbiol 67:1179–1184

    Article  CAS  Google Scholar 

  • Mohamed ME, Al-Yacoub ZH, Vedakumar JV (2015) Biocatalytic desulfurization of thiophenic compounds and crude oil by newly isolated bacteria. Front Microbiol 6:112. https://doi.org/10.3389/fmicb.2015.00112

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Monticello DJ, Kilbane JJ (1994). Microemulsion process for direct biocatalytic desulfurization of organosulfur molecules. US Patent 5,358,870.

  • Nakashima N, Tamur T (2004) A novel system for expressing recombinant proteins over a wide temperature range from 4 to 35°C. Biotechnol Bioeng 86:136–148

    Article  CAS  Google Scholar 

  • Nassar HN, Deriase SF, El-Gendy NS (2017) Statistical optimization of biomass production and biodesulfurization activity of Rhodococcus erythropolis HN2. Pet Sci Technol 35(20):1951–1959

    Article  CAS  Google Scholar 

  • Nassar HN, El-Gendy NS, Abo-State MA, Mostafa YM, Mahdy HM, El-Temtamy SA (2013) Desulfurization of dibenzothiophene by a novel strain Brevibacillus invocatus C19 isolated from Egyptian coke. Biosci Biotechnol Res Asia 10(1):29–46

    Article  CAS  Google Scholar 

  • Ohshiro T, Hirata T, Hashimoto I, Izumi Y (1996) Characterization of dibenzothiophene desulfurization reaction by whole cells of Rhodococcus erythropolis H-2 in the presence of hydrocarbon. J Ferment Bioeng 82:610–612

    Article  CAS  Google Scholar 

  • Ohshiro T, Nakura S, Ishii Y, Kino K, Kirimura K, Izumi Y (2009) Novel reactivity of dibenzothiophene monooxygenase from Bacillus subtilis WU-S2B. Biosci Biotechnol Biochem 73:2128–2130

    Article  CAS  Google Scholar 

  • Onaka T, Konishi J, Ishii Y, Maruhashi K (2001) Desulfurization characteristics of thermophilic Paenibacillus sp. strain A11-2 against asymmetrically alkylated dibenzothiophenes. J Biosci Bioeng 92(2):193–196

    Article  CAS  Google Scholar 

  • Porto B, Maass D, Oliveira JV, de Oliveira D, Yamamoto CI, Ulson de Souza AA, Ulson de Souza SMAG (2018) Heavy gas oil biodesulfurization using a low-cost bacterial consortium. J Chem Technol Biotechnol 93:2359–2363

    Article  CAS  Google Scholar 

  • Sadare OO, Obazu F, Daramola MO (2017) Biodesulfurization of petroleum distillates—current status, opportunities and future challenges. Environments 4:85. https://doi.org/10.3390/environments4040085

    Article  Google Scholar 

  • Sharma R, Singh J, Verma N (2020) A novel spectrophotometric method for simultaneous estimation of dibenzothiophene and 2-hydroxybiphenyl in their mixed spectrum and its application in screening of specific biodesulfurizing microbes. 3 Biotech 10:153 https://doi.org/10.1007/s13205-020-2138-1.

  • Setti L, Lanzarini G, Pifferi PG (1995) Dibenzothiophene biodegradation by a Pseudomonas sp. in model solutions. Process Biochem 30(8):721–728

    Article  CAS  Google Scholar 

  • Soleimani M, Bassi A, Margaritis A (2007) Sulfur compounds in fossil fuels. Biotechnol Adv 25(6):570–596

    Article  CAS  Google Scholar 

  • Su T, Su J, Liu S, Zhang C, He J, Huang H, Xu S, Gu L (2018) Structural and biochemical characterization of BdsA from Bacillus subtilis WU-S2B, a key enzyme in the “4S” desulfurization pathway. Front Microbiol 9:231. https://doi.org/10.3389/fmicb.2018.00231

    Article  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  Google Scholar 

  • Tao F, Liu Y, Luo Q, Su F, Xu Y, Li F, Yu B, Ma C, Xu P (2011) Novel organic solvent-responsive expression vectors for biocatalysis: application for development of an organic solvent-tolerant biodesulfurizing strain. Bioresour Technol 102:9380–9387

    Article  CAS  Google Scholar 

  • Tao F, Yu B, Xu P, Ma CQ (2006) Biodesulfurization in biphasic systems containing organic solvents. Appl Environ Microbiol 72:4604–4609

    Article  CAS  Google Scholar 

  • Wang J, Davaadelger B, Salazar JK, Butler RR III, Pombert J-F, Kilbane JJ, 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 

  • Zhang S-H, 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 

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Authors and Affiliations

  1. Petroleum Biotechnology Lab., Department of Process Design and Development, Egyptian Petroleum Research Institute (EPRI), Nasr City, Cairo, 11727, Egypt

    Hussein N. Nassar & Nour Sh. El-Gendy

  2. Department of Microbiology, Faculty of Pharmacy, October University for Modern Sciences and Arts (MSA), 6th of October City, Giza, 12566, Egypt

    Hussein N. Nassar

  3. Nanobiotechnology Program, Faculty of Nanotechnology for Postgraduate Studies, Cairo University, Sheikh Zayed Branch Campus, Sheikh Zayed City, Giza, 12588, Egypt

    Hussein N. Nassar & Nour Sh. El-Gendy

  4. Faculty of Engineering, Karabuk University, Demir Campus, 78050 Karabuk, Turkey

    Salem S. Abu Amr

  5. Center of Excellence, October University for Modern Sciences and Arts (MSA), 6th of October City, Giza, 12566, Egypt

    Nour Sh. El-Gendy

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  1. Hussein N. Nassar
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  2. Salem S. Abu Amr
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  3. Nour Sh. El-Gendy
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Contributions

HNN conducted the isolation of the bacteria and its identification, all the microbiological and biodesulfurization experiments, all the analysis to follow up the biodesulfurization efficiency, and the kinetic analysis and its validation. SSA performed the statistical analysis. NShE conceived and designed the research, interpreted, analysed, and discussed the obtained data and wrote the manuscript, and all authors commented on previous versions of the manuscript. Finally, all authors read and approved the manuscript.

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Correspondence to Nour Sh. El-Gendy.

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Nassar, H.N., Abu Amr, S.S. & El-Gendy, N.S. Biodesulfurization of refractory sulfur compounds in petro-diesel by a novel hydrocarbon tolerable strain Paenibacillus glucanolyticus HN4. Environ Sci Pollut Res 28, 8102–8116 (2021). https://doi.org/10.1007/s11356-020-11090-7

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