Abstract
Biodesulfurization is emerging as a valuable technology for the desulfurization of dibenzothiophene (DBT) and its alkylated substitutes, which are otherwise regarded as refractory to other physical and chemical desulfurizing techniques. The inability of the currently identified pure cultures and artificial microbial consortia due to lower desulfurization rate and product inhibition issues has compelled the researcher to look for an alternative solution. Thus, in the present study, an indigenously isolated microbial consortium was employed to tackle the desulfurization issue. Herein, we isolated several kinds of DBT desulfurizing natural microbial consortia from hydrocarbon-contaminated soil samples by conventional enrichment technique. The most effective desulfurizing microbial consortium was sequenced through illumine sequencing technique. Finally, the effect of the products of the desulfurizing pathway (such as 2-hydroxybiphenyl (2-HBP) and sulfate (SO4−2) was evaluated on the growth and desulfurization capability of the isolated consortium. The outcomes of Gibb’s assay analysis showed that six isolates followed the “4S” pathway and converted DBT to 2-HBP. Among the isolates, I5 showed maximum growth rate (1.078 g/L dry cell weight) and desulfurization activity (about 77% as indicated by HPLC analysis) and was considered for further in-depth experimentation. The analysis of 16S rRNA by high-throughput sequencing approach of the I5 isolate revealed five types of bacterial phyla including Proteobacteria, Bacteroidetes, Firmicutes, Patescibacteria, and Actinobacteria (in order of abundance). The isolate showed significant tolerance to the inhibitory effect of both 2-HBP and SO4−2 and maintained growth in the presence of even about 1.0 mM initial concentration of both products. This clearly suggests that the isolate can be an efficient candidate for future in-depth desulfurization studies of coal and other fossil fuels.
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References
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(1):95–102. https://doi.org/10.1111/j.1574-6968.2009.01797x
Akhtar N, Akhtar K, Ghauri MA (2018) Biodesulfurization of thiophenic compounds by a 2-hydroxybiphenyl-resistant Gordonia sp. HS126-4N carrying dszABC genes. Curr Microbiol 75:597–603. https://doi.org/10.1007/s00284-017-1422-8
Al-Jailawi MH, Al-Faraas AF, Yahia AI (2015) Isolation and identification of dibenzothiophene biodesulfurizing bacteria. Am J Biosci Bioeng 3(5):40–46. https://doi.org/10.11648/j.bio.20150305.13
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
Ansari F, Prayuenyong P, Tothill I (2007) Biodesulphurization of dibenzothiophene by Shewanella putrefaciens NCIMB 8768. J Biol Phys Chem 7(2):75–78. https://doi.org/10.4024/20708.jbpc.07.02
Ashutosh B, Madhuri KL, Ashok M, Ravindra NS, Koushalya D (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. https://doi.org/10.1016/S1001-0742(10)60504-9
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(3):104–109. https://doi.org/10.1016/j.bej.2010.04.001
Bhatia B, Sharma DK (2012) Thermophilic desulfurization of dibenzothiophene and different petroleum oils by Klebsiella sp. 13T. Environ Sci Pollut Res 19:3491–3497. https://doi.org/10.1007/s11356-012-0884-2
Bordoloi NK, Bhagowati P, Chaudhuri MK, Mukherjee AK (2016) Proteomics and metabolomics analyses to elucidate the desulfurization pathway of Chelatococcus sp. PLoS One 11(4):e0153547. https://doi.org/10.1371/journal.pone.0153547
Chen H, Zhang WJ, Cai YB, Zhang Y, Li W (2008) Elucidation of 2-hydroxybiphenyl effect on dibenzothiophene desulfurization by Microbacterium sp. strain ZD-M2. Bioresour Technol 99:6928–6933. https://doi.org/10.1016/j.biortech.2008.01.033
Chen S, Sun S, Zhao C, Liu Q, Zang M (2019) Bio-desulfurization of model oil using growing cells of Gordonia sp. SC-10. Pet Sci Technol 37(8):907–912. https://doi.org/10.1080/10916466.2019.1575862
Etemadifar Z, Cappello S, Zarkesh-Esfahani SH (2014) Characteristics of dibenzothiophene desulfurization by Rhodococcus erythropolis R1 and its Dsz-negative mutant. Biol J Microorganism 2(8):1–14
Ghazali FM, Noor R, Rahman ZA, Salleh AB, Basri M (2004) Biodegradation of hydrocarbons in soil by microbial consortium. Int Biodeterior Biodegrad 54:61–67. https://doi.org/10.1016/j.ibiod.2004.02.002
Ghosh A, Sujata A, Pandey BD (2015) Microbial biodesulphurisation of coal. In: Microbiology for minerals, metals, materials and the environment. CRC Press, p 1–32
Gojgic-Cvijovic GD, Milic JS, Solevic TM, Beskoski VP, Ilic MV, Djokic LS, Narancic TM, Vrvic MM (2012) Biodegradation of petroleum sludge and petroleum polluted soil by a bacterial consortium: a laboratory study. Biodegradation 23:1–14. https://doi.org/10.1007/s10532-011-9481-1
González N, Simarro R, Molina MC, Bautista LF, Delgado L, Villa JA (2011) Effect of surfactants on PAH biodegradation by a bacterial consortium and on the dynamics of the bacterial community during the process. Bioresour Technol 102:9438–9446. https://doi.org/10.1016/j.biortech.2011.07.066
Ismail W, El-Sayed WS, Abdul Raheem AS, Mohamed ME, El Nayal AM (2016) Biocatalytic desulfurization capabilities of a mixed culture during non-destructive utilization of recalcitrant organosulfur compounds. Front Microbiol 7(266):1–14. https://doi.org/10.3389/fmicb.2016.00266
Khan J, Ali MI, Jamal A, Huang Z, Achakzai JK, Nasir N, Qureshi MZ (2022a) Optimizing the metabolic performance of mixed bacterial culture towards dibenzothiophene desulfurization under the effect of varying nutrient and environmental factors. Pol J Environ Stud 31(5):4167–4175. https://doi.org/10.15244/pjoes/147650
Khan J, Ali MI, Jamal A, Ahmad M, Achakzai JK, Zafar M (2022b) Response of mixed bacterial culture towards dibenzothiophene desulfurization under the influence of surfactants and microscopically (SEM and TEM) characterized magnetic Fe3O4 nanoparticles. Microsc Res Tech. https://doi.org/10.1002/jemt.24230
Krishna KR, Philip L (2008) Biodegradation of lindane, methyl parathion and carbofuran by various enriched bacterial isolates. J Environ Sci Health Part B 43(2):157–171. https://doi.org/10.1080/03601230701795155
Maass D, Todescato D, Moritz DE, Oliveira JV, Oliveira D, Ulson de Souza AA, Guelli Souza SMA (2015) Desulfurization and denitrogenation of heavy gas oil by Rhodococcus erythropolis ATCC 4277. Bioprocess Biosyst Eng 38(8):1447–1453. https://doi.org/10.1007/s00449-015-1386-7
Magdy ESM, Zakariya HAY, John VV (2015) Biocatalytic desulfurization of thiophenic compounds and crude oil by newly isolated bacteria. Front Microbiol 6(112):1–12. https://doi.org/10.3389/fmicb.2015.00112
Mao DP, Zhou Q, Chen CY, Quan ZX (2012) Coverage evaluation of universal bacterial primers using the metagenomic datasets. BMC Microbiol 12(1):1–8
Marks CR, Callaghan AM (2018) Surface and subsurface coal environments: from environmental formation and chemistry to microbial communities. In: McGenity T (ed) Microbial communities utilizing hydrocarbons and lipids: members, metagenomics and ecophysiology. Handbook of hydrocarbon and lipid microbiology. Springer, Cham, p 1–23 Doi:https://doi.org/10.1007/978-3-319-60063-5_9-1
Martinez I, Santos VE, Alcon A, Garcia-Ochoa F (2015) Enhancement of the biodesulfurization capacity of Pseudomonas putida CECT5279 by co-substrate addition. Process Biochem 50:119–124. https://doi.org/10.1016/j.procbio.2014.11.001
Mohebali G, Ball AS (2016) Biodesulfurization of diesel fuels–past, present, and future perspectives. Inter Biodeterior Biodegradation 110:163–180. https://doi.org/10.1016/j.ibiod.2016.03.011
Mohebali G, Ball AS, Rasekh B, Kaytash A (2007) Biodesulfurization potential of a newly isolated bacterium, Gordonia alkanivorans RIPI90A. Enzyme Microb Technol 40:578–584. https://doi.org/10.1016/j.emzmictec.2006.05.012
Nassar HN, El-Gendy NS, Abo-State MA, Moustafa YM, Mehdy 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. https://doi.org/10.13005/bbra/1090
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). Microbiol 143(9):2961–2973
Papizadeh M, Ardakani MR, Motamedi H, Rasouli I, Zarei M (2011) C–S targeted biodegradation of dibenzothiophene by Stenotrophomonas sp. NISOC-04. Appl Biochem Biotechnol 165:938–948. https://doi.org/10.1007/s12010-011-9310-3
Papizadeh M, Ardakani MR, Motamedi H (2017) Growth-phase dependent biodesulfurization of dibenzothiophene by Enterobacter sp. strain NISOC-03. Pollution 3(1):101–111. https://doi.org/10.7508/pj.2017.01.010
Prayuenyong P (2001) Biodesulphurisation of coal. Doctoral dissertation, Thesis of Doctor of Philosophy, Institute of Bioscience and Technology
Raheb J, Hajipour MJ, Memari B (2010) Increasing of biodesulfurization activity of newly recombinant Pseudomonas aeruginosa ATCC 9027 by cloning the flavin reductase gene. Int J Biotechnol Biochem 6(2):219–230
Sadare OO, Obazu F, Daramola MO (2017) Biodesulfurization of petroleum distillates—current status, opportunities and future challenges. Environments 4(85):1–20. https://doi.org/10.3390/environments4040085
Silva TAL, Schwartz M, Souza PM, Garrard I, Campos-Takaki GM, Tambourgi EB (2018) Desulfurization of dibenzothiophene by Pseudomonas flourescens (UCP 1514) leading to the production of biphenyl. Recent Insights Pet Sci Eng. https://doi.org/10.5772/intechopen.70430
Soleimani M, Bassi A, Margaritis A (2007) Biodesulfurization of refractory organic sulfur compounds in fossil fuels. Biotechnol Adv 25(6):570–596. https://doi.org/10.1016/j.biotechadv.2007.07.003
Vega F, Alonso-Fariñas B, Baena-Moreno FM, Rodríguez JA, Navarrete B (2019) Technologies for control of sulfur and nitrogen compounds and particulates in coal combustion and gasification. In: New trends in coal conversion. Woodhead Publishing, p 141–173 Doi:https://doi.org/10.1016/B978-0-08-102201-6.00006-6
Xu J, Liu X, Song C, Du Z, Wang F, Luo J, Chen X, Zhou A (2019) Biodesulfurization of high sulfur coal from Shanxi: optimization of the desulfurization parameters of three kinds of bacteria. Energy Sources A Recovery Util Environ Eff 42(18):2297–2315. https://doi.org/10.1080/15567036.2019.1675821
Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated canadian high arctic soils. PLoS One 7(1):1–10. https://doi.org/10.1371/journal.pone.0030058
Acknowledgements
The author (Javed Khan) is thankful to the Higher Education Commission of Pakistan for giving the opportunity of a Ph.D. fellowship under the title MS Leading to Ph.D. under Aghaz e Haqooq e Balochistan Package. Likewise, the authors also acknowledge the funding facility provided by the Higher Education Commission of Pakistan under the research grant program (Project ID 4568) named National Research Program for Universities (NRPU).
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MIA supervisor of JK design the study and reviewed the manuscript. JK performed the experiments, analyzed the data, and wrote the manuscript. AJ, JKA, JHS, and AH helped in writing and reviewing the manuscript. All the authors read and approved the final manuscript.
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The authors declare that they have no conflict of interest. This study was commenced after getting approval from the Institutional Review Board of Quaid-e-Azam University, Islamabad, Pakistan. Written consent forms were filled out by all the members participating in this study.
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Khan, J., Ali, M.I., Jamal, A. et al. Assessment of the dibenzothiophene desulfurization potential of indigenously isolated bacterial consortium IQMJ-5: a different approach to safeguard the environment. Arch Microbiol 205, 95 (2023). https://doi.org/10.1007/s00203-023-03429-8
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DOI: https://doi.org/10.1007/s00203-023-03429-8