Enhanced Petroleum Removal by Potent Biosurfactant Producer Bacillus Subtilis CC9 Strain Isolated from an Oil Field
Year 2023,
Volume: 51 Issue: 2, 141 - 152, 01.04.2023
Sezen Bılen Ozyurek
,
Kaan Soyuer
Abstract
This study aimed to enhance the removal of petroleum with potent biosurfactant producing bacterial strains (Bacillius subtilis CC9, Enterobacter asburiae WMB1, Klebsiella oxytoca Rizhao 536-1, and Acinetobacter pittii PgBE252) isolated from an oil field. The biosurfactant production was determined by different screening methods such as hemolytic activity, drop-collapse, oil spreading, BATH, emulsification index and surface tension. While the presence of biosurfactant was detected with individual bacterial strain, B. subtilis CC9 strain was found to be quite effective on petroleum degradation (92%) with a high yield of biosurfactant production (0.95 ±0.05 g L-1). The degradation rate constant and half-life period of B. subtilis CC9 strain were calculated as K = 2.533 day−1, t1/2 = 0.273. It has been clearly shown with GC/MS analysis that B. subtilis CC9 strain was effective on the removal of long chain n-alkanes (C31 - C35) as well as short and medium chains. The FT-IR analysis also approved the presence of aliphatic and peptide moieties of biosurfactant extracted from B. subtilis CC9 strain. It is remarkably pointed out with this study that high yield of biosurfactant producing B. subtilis CC9 strain can be used in advanced petroleum bioremediation studies as an alternative to chemical surfactants.
Supporting Institution
The Scientific and Technological Research Council of Turkey
Project Number
1910B011900736
Thanks
This work was supported by 2209-A-Research Project Support Program for Undergraduate Students, The Scientific and Technological Research Council of Turkey.
References
- 1. A.A. Befkadu, Q. Chen, Surfactant-enhanced soil washing for removal of petroleum hydrocarbons from contaminated soils: A review, Pedosphere, 28 (2018) 383–410.
- 2. A.P. Karlapudi, T.C. Venkateswarulu, J. Tammineedi, L. Kanumuri, B.K. Ravuru, V. Dirisala, V.P. Kodali, Role of biosurfactants in bioremediation of oil pollution-a review, Petroleum, 4 (2018) 241-249.
- 3. E.M. Rodrigues, A.V. Novaes de Carvalho Teixeira, D.W. Cesar, M.R. Tótola, Strategy to improve crude oil biodegradation in oligotrophic aquatic environments: W/O/W fertilized emulsions and hydrocarbonoclastic bacteria, Braz. J. Microbiol., 51 (2020) 1159–1168.
- 4. R.N. Montagnolli, P.R.M. Lopes, E.D. Bidoia, Assessing Bacillus subtilis biosurfactant effects on the biodegradation of petroleum products, Environ. Monit. Assess., 187(2015) 1-17.
- 5. E. Gakpe, P.K.S.M. Rahman, A.A.M. Hatha, Microbial biosurfactants: Review. J. Mar. Atmos. Res., 3 (2007) 1-17.
- 6. F.S. Silva, D.G. Almeida, R.D. Rufino, J.M. Luna, V.A. Santos, L.A. Sarubbo, Applications of biosurfactants in the petroleum industry and the remediation of oil spills, Int. J. Mol. Sci., 15 (2014) 12523-12542.
- 7. A. Khan, A. Butt, Biosurfactants and their potential applications for microbes and mankind: An overview, Middle East J. Bus., 11 (2016) 9-18.
- 8. E. Shoeb, N. Ahmed, J. Akhter, U. Badar, K. Siddiqui, F.A. Ansari, M. Waqar, S. Imtiaz, N. Akhtar, Q.A. Shaikh, R. Baig, S. Butt, S. Khan, S. Khan, S. Hussaim, B. Ahmed, M.A. Ansari, Screening and characterization of biosurfactant-producing bacteria isolated from the Arabian Sea coast of Karachi, Turk J. Biol., 39 (2015) 210-216.
- 9. H. Zhou, J. Chen, Z. Yang, B. Qin, Y. Li, X. Kong, Biosurfactant production and characterization of Bacillus sp. ZG0427 isolated from oil contaminated soil, Ann. Microbiol., 65 (2015) 2255-2264.
- 10. S.N. Al-Bahry, Y.M. Al-Wahaibi, A.E. Elshafie, A.S. Al-Bemani, S.J. Joshi, H.S. Al-Akhmari, H.S. Al-Sulaimani, Biosurfactant production by Bacillus subtilis B20 using date molasses and its possible application in enhanced oil recovery, Int. Biodeterior. Biodegrad. 81 (2013) 141–146.
- 11. R.T. Bachmann, A.C. Johnson, R.G.J. Edyvean, Biotechnology in the petroleum industry: an overview, Int. Biodeterior. Biodegrad., 86 (2014) 225–237.
- 12. D.G. De Almeida, R.C.F. Soares Da Silva, J.M. Luna, R.D. Rufino, V.A. Santos, I.M. Banat, L.A. Sarubbo, Biosurfactants: Promising molecules for petroleum biotechnology advances, Front. Microbiol., 7 (2016) 1-14.
- 13. J. Liu, Y. Chen, R. Xu, Y. Jia, Biosurfactants: Promising molecules for petroleum biotechnology advances, Indian J. Microbiol., 53 (2013) 168–174.
- 14. D. Sharma, M.J. Ansari, A. Al-Ghamdi, N. Adgaba, K.A. Khan, V. Pruthi, N. Al-Waili, Biosurfactant production by Pseudomonas aeruginosa DSVP20 isolated from petroleum hydrocarbon-contaminated soil and its physicochemical characterization, Environ. Sci. Pollut. Res., 22 (2015) 17636-17643.
- 15. A.M. Elazzazy, T.S. Abdelmoneim, O.A. Almaghrabi, Isolation and characterization of biosurfactant production under extreme environmental conditions by alkali-halo-thermophilic bacteria from Saudi Arabia, Saudi J. Biol. Sci., 22 (2015) 466-475.
- 16. S. Bilen Ozyurek, I. Seyis Bilkay, Determination of petroleum biodegradation by bacteria isolated from drilling fluid, waste mud pit and crude oil, Turkish J. Biochem., 42 (2017) 609-616.
- 17. K. Patowary, R. Patowary, M.C. Kalita, S. Deka, Characterization of biosurfactant produced during degradation of hydrocarbons using crude oil as sole source of carbon, Front. Microbiol., 8 (2017) 1-14.
- 18. J. Tanzadeh, M.F. Ghasemi, M. Anvari, K. Issazadeh, Biological removal of crude oil with the use of native bacterial consortia isolated from the shorelines of the Caspian Sea, Biotechnol. Biotechnol. Equip., 34 (2020) 361-374.
- 19. P. Parthipan, E. Preetham, L.L. Machuca, P.K.S.M. Rahman, K. Murugan, A. Rajasekar, Biosurfactant and degradative enzymes mediated crude oil degradation by bacterium Bacillus subtilis A1, Front. Microbiol. 8 (2017) 1-14.
- 20. I.M. Banat, The isolation of a thermophilic biosurfactant producing Bacillus sp., Biotechnol. Lett. 15 (1993) 591–594.
- 21. P. Carrillo, C. Mardaraz, S. Pitta-Alvarez, A.M. Giulietti, Isolation and selection of biosurfactant-producing bacteria, World J. Microbiol. Biotechnol., 12 (1996) 82–84.
22. A.A. Bodour, R.M. Miller-Maier, Application of modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms, J. Microbiol. Methods., 32 (1998) 273–280.
- 23. M. Hassanshahian, Isolation and characterization of biosurfactant producing bacteria from Persian Gulf (Bushehr provenance), Mar. Pollut. Bull., 86 (2014) 361-366.
- 24. M. Rosenberg, D. Gutnick, E. Rosenberg, Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity, FEMS Microbiol. Lett., 9 (1980) 29-33.
- 25. W. Van der Vegt, H. Van der Mei, J. Noordmans, Assessment of bacterial biosurfactant production through axisymmetrical drop shape-analysis by profile, Appl. Microbiol. Biotechnol. 35 (1991) 766–770.
- 26. G.A. Plaza, I. Zjawiony, I.M. Banat, Use of different methods for detection of thermophilic biosurfactant producing bacteria from hydrocarbon-contaminated and bioremediated soils, J. Pet. Sci. Eng., 50 (2006) 71-77.
- 27. F. Shahaliyan, A. Safahieh, H. Abyar, Evaluation of Emulsification Index in Marine Bacteria Pseudomonas sp. and Bacillus sp., Arab. J. Sci. Eng., 40 (2015) 1849–1854.
- 28. K.S.M. Rahman, T.J. Rahman, P. Lakshmanaperumalsamy, I.M. Banat, Towards efficient crude oil degradation by a mixed bacterial consortium, Bioresour. Technol., 85 (2002) 257–261.
- 29. S. Bilen Ozyurek, I. Seyis Bilkay, Comparison of petroleum biodegradation efficiencies of three different bacterial consortia determined in petroleum‑contaminated waste mud pit, SN Appl. Sci., 2 (2020) 1-12.
- 30. A. Al-Hawash, J.T. Alkooranee, H.A. Abbood, J. Zhang, J. Sun, X. Zhang, F. Ma, Isolation and characterization of two-crude oil degrading fungi strains from Rumila oil field, Biotechnol. Rep., 17 (2018) 104–109.
- 31. F.E. Mouafia, M.M.A. Elsouda, M.E. Moharam, Optimization of biosurfactant production by Bacillus brevis using response surface methodology, Biotechnol. Rep., 9 (2016) 31-37.
- 32. A. Nayarisseri, P. Singh, S. Kumar Singh, Screening, isolation, and characterization of biosurfactant producing Bacillus subtilis strain, Bioinformation, 14 (2018) 304-314.
- 33. A.N. Mwaura, B.N. Mbatia, E.K. Muge, P.W. Okanya, Screening and characterization of hydrocarbonoclastic bacteria isolated from oil-contaminated soils from auto garages, Int. J. Microbiol. Biotechnol., 3 (2018) 11-24.
- 34. O.O. Yusuf, N. Torimiro, S.A. Afolalu, A.A. Abioye, M.E. Emetere, S.O. Alayand, Evaluation of the effect of physicochemical parameters on the biodegradation of spent engine oil using selected oleophilic bacteria, IOP Conf. Series: Earth Environ. Sci. 655 (2021) 1-10.
- 35. D. Borah, K. Agarwal, A. Khataniar, D. Konwar, S.B. Gogoi, M. Kallel, A newly isolated strain of Serratia sp. from an oil spillage site of Assam shows excellent bioremediation potential. 3 Biotech, 9 (2019) 1-12.
- 36. M.M. Lazaroaie, Multiple responses of gram-positive and gram-negative bacteria to mixture of hydrocarbons, Braz. J. Microbiol., 41 (2010) 649-667.
- 37. A. Segura, A. Hurtado, B. Rivera, M.M. Lazaroaie, Isolation of new toluene-tolerant marine strains of bacteria and characterization of their solvent-tolerance properties, J. Appl. Microbiol., 104 (2008) 1408-1416.
- 38. N. Das, P. Chandran, Microbial degradation of petroleum hydrocarbon contaminants: An overview, Biotechnol. Res. Int., (2011) 1-13.
- 39. I.V. Nwaguma, C.B. Chikere, G.C. Okpokwasili, Isolation, characterization, and application of biosurfactant by Klebsiella pneumoniae strain IVN51 isolated from hydrocarbon-polluted soil in Ogoniland, Nigeria, Bioresour. Bioprocess., 3 (2016) 2-13.
- 40. T. Varadavenkatesan, V. Ramachandra Murty, Production of a lipopeptide biosurfactant by a novel Bacillus sp. and its applicability to enhanced oil recovery, ISRN Microbiol., (2013)1-8.
- 41. A.A. Bodour, R.M. Maier, Biosurfactants: types, screening methods and application. Encyclopedia of Environmental Microbiology, 2 (2002) Wiley, New York, 750–769.
42. N.H. Youssef, K.E. Duncan, D.P. Nagle, K.N. Savage, R.M. Knapp, M.J. McInerney, Comparison of methods to detect biosurfactant production by diverse microorganisms, J. Microbiol. Methods, 56 (2004) 339–346.
- 43. E.Z. Gomaa, R.M. El-Meihy, Bacterial biosurfactant from Citrobacter freundii MG812314.1 as a bioremoval tool of heavy metals from wastewater, Bull. Natl. Res. Cent., 43 (2019) 1-14.
- 44. M.O. Ilori, C.J. Amobi, A.C. Odocha, Factors affecting biosurfactant production by oil degrading Aeromonas sp., isolated from a tropical environment, Chemosphere, 61 (2005) 985–992.
- 45. S. Viramontes-Ramos, M.C. Portillo-Ruiz, M.L. Ballinas-Casarrubias, J.V. Torres-Muñoz, B.E. Rivera-Chavira, G.V. Nevárez-Moorillón, Selection of biosurfactant/bioemulsifier-producing bacteria from hydrocarbon-contaminated soil, Braz. J. Microbiol. 41 (2010) 668-675.
- 46. Q. Cai, B. Zhang, B. Chen, Z. Zhu, W. Lin, T. Cao, Screening of biosurfactant producers from petroleum hydrocarbon contaminated sources in cold marine environments, Mar. Pollut. Bull. 86 (2014) 402–410.
- 47. N. Krepsky, F.S. Da Silva, L.F. Fontana, M.A.C. Crapez, Alternative methodology for isolation of biosurfactant producing bacteria, Braz. J. Biol., 67 (2007) 117-124.
- 48. A. Singh, J.D. Van Hamme, O.P. Ward, Surfactants in microbiology and biotechnology: part 2. Application aspects, Biotechnol. Adv., 25 (2007) 99–121.
- 49. B. Chettri, N.A. Singha, A. Mukherjee, A.N. Rai, D. Chattopadhyay, A. Kumar Singh, Hydrocarbon degradation potential and competitive persistence of hydrocarbonoclastic bacterium Acinetobacter pittii strain ABC. Arch. Microbiol., 201 (2019) 1129-1140.
- 50. R. Pandey, P. Sharma, S. Rathee, H.P. Singh, D.R. Batish, B. Krishnamurthy, R. Kumar Kohli, Isolation and characterization of a novel hydrocarbonoclastic and biosurfactant producing bacterial strain: Fictibacillus phosphorivorans RP3, 3 Biotechnol., 11 (2021) 1-11.
- 51. X. Xu, W. Liu, S. Tian, W. Wang, Q. Qi, P. Jiang, X. Gao, F. Li, H. Li, H. Yu, Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis, Front. Microbiol., 9 (2018) 1-11.
- 52. S. Kleindienst, M. Seidel, K. Ziervogel, S. Grim, K. Loftis, S. Harrison, Chemical dispersants can suppress the activity of natural oil-degrading microorganisms, Proc. Natl. Acad. Sci. U.S.A.1, 12 (2015) 14900–14905.
- 53. S.J. Varjani, Microbial degradation of petroleum hydrocarbons, Bioresour. Technol., 223 (2017) 277–286.
- 54. H.P. Doddamani, H.Z. Ninnekar, Biodegradation of phenanthrene by a Bacillus species, Curr. Microbiol., 44 (2000) 11–14.
- 55. W.Q. Zhuang, J.H. Tay, A.M. Maszenan, S.T. Tay, Bacillus naphtovorans sp. nov. from oil-contaminated tropical marine sediments and its role in naphthalene biodegradation, Appl. Microbiol. Biotechnol., 58 (2002) 547–553.
- 56. C., Calvo, F.L. Toledo, J. Gonzalez-Lopez, Surfactant activity of a naphthalene degrading Bacillus pumilis strain isolated from oil sludge, J. Biotechnol., 109 (2004) 255–262.
- 57. N. Christova, L. Kabaivanova, L. Nacheva, P. Petrov, I. Stoineva, Biodegradation of crude oil hydrocarbons by a newly isolated biosurfactant producing strain, Biotechnol. Biotechnol. Equip., 33 (2019) 863–872.
- 58. E. Antoniou, S. Fodelianakis, E. Korkakaki, N. Kalogerakis, Biosurfactant production from marine hydrocarbon-degrading consortia and pure bacterial strains using crude oil as carbon source, Front. Microbiol. 6 (2015) 1-14.
- 59. R.M. Jain, K. Mody, N. Joshi, A. Mishra, B. Jha, Production and structural characterization of biosurfactant produced by alkaliphilic bacteria Klebsiella sp.: Evaluation of different carbon sources, Colloid Surf. B, 108 (2013) 199-204.
- 60. S. Mishra, S.N. Singh, Microbial degradation of n-hexadecane in mineral salt medium as mediated by degradative enzymes, Bioresour. Technol., 111 (2012) 148–154.
- 61. J.A. Viesser, M.H. Sugai-Guerios, L.C. Malucelli, M.R. Pincerati, S.G. Karp, L. Maranho, Petroleum-tolerant rhizospheric bacteria: Isolation, characterization, and bioremediation potential, Sci. Rep., 10 (2020) 1-11.
- 62. B. Yudano, M. Said, A. Sabaruddin Napoleon, Z. Fanani, Kinetics approach of biodegradation of petroleum contaminated soil by using indigenous isolated bacteria, J. Trop. Soil., 16 (2011) 33–38.
- 63. L. Kachieng’a, M.N.B. Momba, Kinetics of petroleum oil biodegradation by consortium of three protozoan isolates (Aspidisca sp., Trachelophyllum sp. and Peranema sp.), Biotechnol. Rep., 15 (2017) 125–131.
- 64. E. Vasileva-Tonkovaa, D. Galabova, E. Stoimenova, Z. Lalchev, Production and properties of biosurfactants from a newly isolated Pseudomonas fluorescens hw-6 growing on hexadecane, Z. Naturforsch C. J. Biosci., 61 (2006) 553-559.
- 65. J.F.B. Pereira, E.J. Gudiña, R. Costa, R. Vitorino, J.A. Teixeira, J.A.P. Coutinho, L.R. Rodrigues, Optimization and characterization of biosurfactant production by Bacillus subtilis isolates towards microbial enhanced oil recovery applications, Fuel, 111 (2013) 259–268.
- 66. A.F. Faria, D.S. Teodoro-Martinez, G.N. Oliveira Barbosa, B. Gontijo Vaz, I.S. Silva, J.S. Garcia, M. Rogério Tótolac, M.N. Eberlin, M. Grossman, O.L. Alves, L.R. Durranta, Production and structural characterization of surfactin (C14/Leu7) produced by Bacillus subtilis isolate LSFM-05 grown on raw glycerol from the biodiesel industry, Process. Biochem., 46 (2011) 1951-1957.
- 67. F.F.C. Barros, A.n. Ponezi, G.M. Pastore, Production of biosurfactant by Bacillus subtilis LB5a on a pilot scale using cassava wastewater as substrate, J. Ind. Microbiol. Biotechnol., 35 (2008) 1071–8.
- 68. D.A. Davis, H.C. Lynch, J. Varley, The application of foaming for the recovery of surfactin from Bacillus subtilis ATCC 21332 cultures, Enzyme Microb. Technol., 28 (2000) 346–54.
- 69. N.A. Al-Dhabi, G.A. Esmail, M.V. Arasu, Enhanced production of biosurfactant from Bacillus subtilis strain Al-dhabi-130 under solid-state fermentation using date molasses from Saudi Srabia for bioremediation of crude-oil-contaminated soils, Int. Env. Res. Pub. He., 17 (2020) 1-20.
- 70. A. Dwivedi, S. Chitranshi, A. Gupta, A. Kumar, J.L. Bhat, Assessment of the petroleum oil degradation capacity of indigenous bacterial species isolated from petroleum oil‑contaminated soil, Int. J Environ. Res., 13 (2019) 735–746.
- 71. S.J. Joshi, Y.M. Al-Wahaibi, S.N. Al-Bahry, A.E. Elshafie, A.S. Al-Bemani, A. Al-Bahri, M.S. Al-Mandhari, Production, characterization, and application of Bacillus licheniformis W16 biosurfactant in enhancing oil recovery, Front. Microbiol., 7 (2016) 1-14.
- 72. P. Talukdar, C. Sharma, A. Doley, K. Barua, A. Borah, P. Agarwal, P. Deori, Isolation and characterization of biosurfactant producing microorganisms from petroleum contaminated soil samples for EOR and bioremediation, Pet. Sci. Technol., 35 (2017) 2102-2108.
Year 2023,
Volume: 51 Issue: 2, 141 - 152, 01.04.2023
Sezen Bılen Ozyurek
,
Kaan Soyuer
Project Number
1910B011900736
References
- 1. A.A. Befkadu, Q. Chen, Surfactant-enhanced soil washing for removal of petroleum hydrocarbons from contaminated soils: A review, Pedosphere, 28 (2018) 383–410.
- 2. A.P. Karlapudi, T.C. Venkateswarulu, J. Tammineedi, L. Kanumuri, B.K. Ravuru, V. Dirisala, V.P. Kodali, Role of biosurfactants in bioremediation of oil pollution-a review, Petroleum, 4 (2018) 241-249.
- 3. E.M. Rodrigues, A.V. Novaes de Carvalho Teixeira, D.W. Cesar, M.R. Tótola, Strategy to improve crude oil biodegradation in oligotrophic aquatic environments: W/O/W fertilized emulsions and hydrocarbonoclastic bacteria, Braz. J. Microbiol., 51 (2020) 1159–1168.
- 4. R.N. Montagnolli, P.R.M. Lopes, E.D. Bidoia, Assessing Bacillus subtilis biosurfactant effects on the biodegradation of petroleum products, Environ. Monit. Assess., 187(2015) 1-17.
- 5. E. Gakpe, P.K.S.M. Rahman, A.A.M. Hatha, Microbial biosurfactants: Review. J. Mar. Atmos. Res., 3 (2007) 1-17.
- 6. F.S. Silva, D.G. Almeida, R.D. Rufino, J.M. Luna, V.A. Santos, L.A. Sarubbo, Applications of biosurfactants in the petroleum industry and the remediation of oil spills, Int. J. Mol. Sci., 15 (2014) 12523-12542.
- 7. A. Khan, A. Butt, Biosurfactants and their potential applications for microbes and mankind: An overview, Middle East J. Bus., 11 (2016) 9-18.
- 8. E. Shoeb, N. Ahmed, J. Akhter, U. Badar, K. Siddiqui, F.A. Ansari, M. Waqar, S. Imtiaz, N. Akhtar, Q.A. Shaikh, R. Baig, S. Butt, S. Khan, S. Khan, S. Hussaim, B. Ahmed, M.A. Ansari, Screening and characterization of biosurfactant-producing bacteria isolated from the Arabian Sea coast of Karachi, Turk J. Biol., 39 (2015) 210-216.
- 9. H. Zhou, J. Chen, Z. Yang, B. Qin, Y. Li, X. Kong, Biosurfactant production and characterization of Bacillus sp. ZG0427 isolated from oil contaminated soil, Ann. Microbiol., 65 (2015) 2255-2264.
- 10. S.N. Al-Bahry, Y.M. Al-Wahaibi, A.E. Elshafie, A.S. Al-Bemani, S.J. Joshi, H.S. Al-Akhmari, H.S. Al-Sulaimani, Biosurfactant production by Bacillus subtilis B20 using date molasses and its possible application in enhanced oil recovery, Int. Biodeterior. Biodegrad. 81 (2013) 141–146.
- 11. R.T. Bachmann, A.C. Johnson, R.G.J. Edyvean, Biotechnology in the petroleum industry: an overview, Int. Biodeterior. Biodegrad., 86 (2014) 225–237.
- 12. D.G. De Almeida, R.C.F. Soares Da Silva, J.M. Luna, R.D. Rufino, V.A. Santos, I.M. Banat, L.A. Sarubbo, Biosurfactants: Promising molecules for petroleum biotechnology advances, Front. Microbiol., 7 (2016) 1-14.
- 13. J. Liu, Y. Chen, R. Xu, Y. Jia, Biosurfactants: Promising molecules for petroleum biotechnology advances, Indian J. Microbiol., 53 (2013) 168–174.
- 14. D. Sharma, M.J. Ansari, A. Al-Ghamdi, N. Adgaba, K.A. Khan, V. Pruthi, N. Al-Waili, Biosurfactant production by Pseudomonas aeruginosa DSVP20 isolated from petroleum hydrocarbon-contaminated soil and its physicochemical characterization, Environ. Sci. Pollut. Res., 22 (2015) 17636-17643.
- 15. A.M. Elazzazy, T.S. Abdelmoneim, O.A. Almaghrabi, Isolation and characterization of biosurfactant production under extreme environmental conditions by alkali-halo-thermophilic bacteria from Saudi Arabia, Saudi J. Biol. Sci., 22 (2015) 466-475.
- 16. S. Bilen Ozyurek, I. Seyis Bilkay, Determination of petroleum biodegradation by bacteria isolated from drilling fluid, waste mud pit and crude oil, Turkish J. Biochem., 42 (2017) 609-616.
- 17. K. Patowary, R. Patowary, M.C. Kalita, S. Deka, Characterization of biosurfactant produced during degradation of hydrocarbons using crude oil as sole source of carbon, Front. Microbiol., 8 (2017) 1-14.
- 18. J. Tanzadeh, M.F. Ghasemi, M. Anvari, K. Issazadeh, Biological removal of crude oil with the use of native bacterial consortia isolated from the shorelines of the Caspian Sea, Biotechnol. Biotechnol. Equip., 34 (2020) 361-374.
- 19. P. Parthipan, E. Preetham, L.L. Machuca, P.K.S.M. Rahman, K. Murugan, A. Rajasekar, Biosurfactant and degradative enzymes mediated crude oil degradation by bacterium Bacillus subtilis A1, Front. Microbiol. 8 (2017) 1-14.
- 20. I.M. Banat, The isolation of a thermophilic biosurfactant producing Bacillus sp., Biotechnol. Lett. 15 (1993) 591–594.
- 21. P. Carrillo, C. Mardaraz, S. Pitta-Alvarez, A.M. Giulietti, Isolation and selection of biosurfactant-producing bacteria, World J. Microbiol. Biotechnol., 12 (1996) 82–84.
22. A.A. Bodour, R.M. Miller-Maier, Application of modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms, J. Microbiol. Methods., 32 (1998) 273–280.
- 23. M. Hassanshahian, Isolation and characterization of biosurfactant producing bacteria from Persian Gulf (Bushehr provenance), Mar. Pollut. Bull., 86 (2014) 361-366.
- 24. M. Rosenberg, D. Gutnick, E. Rosenberg, Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity, FEMS Microbiol. Lett., 9 (1980) 29-33.
- 25. W. Van der Vegt, H. Van der Mei, J. Noordmans, Assessment of bacterial biosurfactant production through axisymmetrical drop shape-analysis by profile, Appl. Microbiol. Biotechnol. 35 (1991) 766–770.
- 26. G.A. Plaza, I. Zjawiony, I.M. Banat, Use of different methods for detection of thermophilic biosurfactant producing bacteria from hydrocarbon-contaminated and bioremediated soils, J. Pet. Sci. Eng., 50 (2006) 71-77.
- 27. F. Shahaliyan, A. Safahieh, H. Abyar, Evaluation of Emulsification Index in Marine Bacteria Pseudomonas sp. and Bacillus sp., Arab. J. Sci. Eng., 40 (2015) 1849–1854.
- 28. K.S.M. Rahman, T.J. Rahman, P. Lakshmanaperumalsamy, I.M. Banat, Towards efficient crude oil degradation by a mixed bacterial consortium, Bioresour. Technol., 85 (2002) 257–261.
- 29. S. Bilen Ozyurek, I. Seyis Bilkay, Comparison of petroleum biodegradation efficiencies of three different bacterial consortia determined in petroleum‑contaminated waste mud pit, SN Appl. Sci., 2 (2020) 1-12.
- 30. A. Al-Hawash, J.T. Alkooranee, H.A. Abbood, J. Zhang, J. Sun, X. Zhang, F. Ma, Isolation and characterization of two-crude oil degrading fungi strains from Rumila oil field, Biotechnol. Rep., 17 (2018) 104–109.
- 31. F.E. Mouafia, M.M.A. Elsouda, M.E. Moharam, Optimization of biosurfactant production by Bacillus brevis using response surface methodology, Biotechnol. Rep., 9 (2016) 31-37.
- 32. A. Nayarisseri, P. Singh, S. Kumar Singh, Screening, isolation, and characterization of biosurfactant producing Bacillus subtilis strain, Bioinformation, 14 (2018) 304-314.
- 33. A.N. Mwaura, B.N. Mbatia, E.K. Muge, P.W. Okanya, Screening and characterization of hydrocarbonoclastic bacteria isolated from oil-contaminated soils from auto garages, Int. J. Microbiol. Biotechnol., 3 (2018) 11-24.
- 34. O.O. Yusuf, N. Torimiro, S.A. Afolalu, A.A. Abioye, M.E. Emetere, S.O. Alayand, Evaluation of the effect of physicochemical parameters on the biodegradation of spent engine oil using selected oleophilic bacteria, IOP Conf. Series: Earth Environ. Sci. 655 (2021) 1-10.
- 35. D. Borah, K. Agarwal, A. Khataniar, D. Konwar, S.B. Gogoi, M. Kallel, A newly isolated strain of Serratia sp. from an oil spillage site of Assam shows excellent bioremediation potential. 3 Biotech, 9 (2019) 1-12.
- 36. M.M. Lazaroaie, Multiple responses of gram-positive and gram-negative bacteria to mixture of hydrocarbons, Braz. J. Microbiol., 41 (2010) 649-667.
- 37. A. Segura, A. Hurtado, B. Rivera, M.M. Lazaroaie, Isolation of new toluene-tolerant marine strains of bacteria and characterization of their solvent-tolerance properties, J. Appl. Microbiol., 104 (2008) 1408-1416.
- 38. N. Das, P. Chandran, Microbial degradation of petroleum hydrocarbon contaminants: An overview, Biotechnol. Res. Int., (2011) 1-13.
- 39. I.V. Nwaguma, C.B. Chikere, G.C. Okpokwasili, Isolation, characterization, and application of biosurfactant by Klebsiella pneumoniae strain IVN51 isolated from hydrocarbon-polluted soil in Ogoniland, Nigeria, Bioresour. Bioprocess., 3 (2016) 2-13.
- 40. T. Varadavenkatesan, V. Ramachandra Murty, Production of a lipopeptide biosurfactant by a novel Bacillus sp. and its applicability to enhanced oil recovery, ISRN Microbiol., (2013)1-8.
- 41. A.A. Bodour, R.M. Maier, Biosurfactants: types, screening methods and application. Encyclopedia of Environmental Microbiology, 2 (2002) Wiley, New York, 750–769.
42. N.H. Youssef, K.E. Duncan, D.P. Nagle, K.N. Savage, R.M. Knapp, M.J. McInerney, Comparison of methods to detect biosurfactant production by diverse microorganisms, J. Microbiol. Methods, 56 (2004) 339–346.
- 43. E.Z. Gomaa, R.M. El-Meihy, Bacterial biosurfactant from Citrobacter freundii MG812314.1 as a bioremoval tool of heavy metals from wastewater, Bull. Natl. Res. Cent., 43 (2019) 1-14.
- 44. M.O. Ilori, C.J. Amobi, A.C. Odocha, Factors affecting biosurfactant production by oil degrading Aeromonas sp., isolated from a tropical environment, Chemosphere, 61 (2005) 985–992.
- 45. S. Viramontes-Ramos, M.C. Portillo-Ruiz, M.L. Ballinas-Casarrubias, J.V. Torres-Muñoz, B.E. Rivera-Chavira, G.V. Nevárez-Moorillón, Selection of biosurfactant/bioemulsifier-producing bacteria from hydrocarbon-contaminated soil, Braz. J. Microbiol. 41 (2010) 668-675.
- 46. Q. Cai, B. Zhang, B. Chen, Z. Zhu, W. Lin, T. Cao, Screening of biosurfactant producers from petroleum hydrocarbon contaminated sources in cold marine environments, Mar. Pollut. Bull. 86 (2014) 402–410.
- 47. N. Krepsky, F.S. Da Silva, L.F. Fontana, M.A.C. Crapez, Alternative methodology for isolation of biosurfactant producing bacteria, Braz. J. Biol., 67 (2007) 117-124.
- 48. A. Singh, J.D. Van Hamme, O.P. Ward, Surfactants in microbiology and biotechnology: part 2. Application aspects, Biotechnol. Adv., 25 (2007) 99–121.
- 49. B. Chettri, N.A. Singha, A. Mukherjee, A.N. Rai, D. Chattopadhyay, A. Kumar Singh, Hydrocarbon degradation potential and competitive persistence of hydrocarbonoclastic bacterium Acinetobacter pittii strain ABC. Arch. Microbiol., 201 (2019) 1129-1140.
- 50. R. Pandey, P. Sharma, S. Rathee, H.P. Singh, D.R. Batish, B. Krishnamurthy, R. Kumar Kohli, Isolation and characterization of a novel hydrocarbonoclastic and biosurfactant producing bacterial strain: Fictibacillus phosphorivorans RP3, 3 Biotechnol., 11 (2021) 1-11.
- 51. X. Xu, W. Liu, S. Tian, W. Wang, Q. Qi, P. Jiang, X. Gao, F. Li, H. Li, H. Yu, Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis, Front. Microbiol., 9 (2018) 1-11.
- 52. S. Kleindienst, M. Seidel, K. Ziervogel, S. Grim, K. Loftis, S. Harrison, Chemical dispersants can suppress the activity of natural oil-degrading microorganisms, Proc. Natl. Acad. Sci. U.S.A.1, 12 (2015) 14900–14905.
- 53. S.J. Varjani, Microbial degradation of petroleum hydrocarbons, Bioresour. Technol., 223 (2017) 277–286.
- 54. H.P. Doddamani, H.Z. Ninnekar, Biodegradation of phenanthrene by a Bacillus species, Curr. Microbiol., 44 (2000) 11–14.
- 55. W.Q. Zhuang, J.H. Tay, A.M. Maszenan, S.T. Tay, Bacillus naphtovorans sp. nov. from oil-contaminated tropical marine sediments and its role in naphthalene biodegradation, Appl. Microbiol. Biotechnol., 58 (2002) 547–553.
- 56. C., Calvo, F.L. Toledo, J. Gonzalez-Lopez, Surfactant activity of a naphthalene degrading Bacillus pumilis strain isolated from oil sludge, J. Biotechnol., 109 (2004) 255–262.
- 57. N. Christova, L. Kabaivanova, L. Nacheva, P. Petrov, I. Stoineva, Biodegradation of crude oil hydrocarbons by a newly isolated biosurfactant producing strain, Biotechnol. Biotechnol. Equip., 33 (2019) 863–872.
- 58. E. Antoniou, S. Fodelianakis, E. Korkakaki, N. Kalogerakis, Biosurfactant production from marine hydrocarbon-degrading consortia and pure bacterial strains using crude oil as carbon source, Front. Microbiol. 6 (2015) 1-14.
- 59. R.M. Jain, K. Mody, N. Joshi, A. Mishra, B. Jha, Production and structural characterization of biosurfactant produced by alkaliphilic bacteria Klebsiella sp.: Evaluation of different carbon sources, Colloid Surf. B, 108 (2013) 199-204.
- 60. S. Mishra, S.N. Singh, Microbial degradation of n-hexadecane in mineral salt medium as mediated by degradative enzymes, Bioresour. Technol., 111 (2012) 148–154.
- 61. J.A. Viesser, M.H. Sugai-Guerios, L.C. Malucelli, M.R. Pincerati, S.G. Karp, L. Maranho, Petroleum-tolerant rhizospheric bacteria: Isolation, characterization, and bioremediation potential, Sci. Rep., 10 (2020) 1-11.
- 62. B. Yudano, M. Said, A. Sabaruddin Napoleon, Z. Fanani, Kinetics approach of biodegradation of petroleum contaminated soil by using indigenous isolated bacteria, J. Trop. Soil., 16 (2011) 33–38.
- 63. L. Kachieng’a, M.N.B. Momba, Kinetics of petroleum oil biodegradation by consortium of three protozoan isolates (Aspidisca sp., Trachelophyllum sp. and Peranema sp.), Biotechnol. Rep., 15 (2017) 125–131.
- 64. E. Vasileva-Tonkovaa, D. Galabova, E. Stoimenova, Z. Lalchev, Production and properties of biosurfactants from a newly isolated Pseudomonas fluorescens hw-6 growing on hexadecane, Z. Naturforsch C. J. Biosci., 61 (2006) 553-559.
- 65. J.F.B. Pereira, E.J. Gudiña, R. Costa, R. Vitorino, J.A. Teixeira, J.A.P. Coutinho, L.R. Rodrigues, Optimization and characterization of biosurfactant production by Bacillus subtilis isolates towards microbial enhanced oil recovery applications, Fuel, 111 (2013) 259–268.
- 66. A.F. Faria, D.S. Teodoro-Martinez, G.N. Oliveira Barbosa, B. Gontijo Vaz, I.S. Silva, J.S. Garcia, M. Rogério Tótolac, M.N. Eberlin, M. Grossman, O.L. Alves, L.R. Durranta, Production and structural characterization of surfactin (C14/Leu7) produced by Bacillus subtilis isolate LSFM-05 grown on raw glycerol from the biodiesel industry, Process. Biochem., 46 (2011) 1951-1957.
- 67. F.F.C. Barros, A.n. Ponezi, G.M. Pastore, Production of biosurfactant by Bacillus subtilis LB5a on a pilot scale using cassava wastewater as substrate, J. Ind. Microbiol. Biotechnol., 35 (2008) 1071–8.
- 68. D.A. Davis, H.C. Lynch, J. Varley, The application of foaming for the recovery of surfactin from Bacillus subtilis ATCC 21332 cultures, Enzyme Microb. Technol., 28 (2000) 346–54.
- 69. N.A. Al-Dhabi, G.A. Esmail, M.V. Arasu, Enhanced production of biosurfactant from Bacillus subtilis strain Al-dhabi-130 under solid-state fermentation using date molasses from Saudi Srabia for bioremediation of crude-oil-contaminated soils, Int. Env. Res. Pub. He., 17 (2020) 1-20.
- 70. A. Dwivedi, S. Chitranshi, A. Gupta, A. Kumar, J.L. Bhat, Assessment of the petroleum oil degradation capacity of indigenous bacterial species isolated from petroleum oil‑contaminated soil, Int. J Environ. Res., 13 (2019) 735–746.
- 71. S.J. Joshi, Y.M. Al-Wahaibi, S.N. Al-Bahry, A.E. Elshafie, A.S. Al-Bemani, A. Al-Bahri, M.S. Al-Mandhari, Production, characterization, and application of Bacillus licheniformis W16 biosurfactant in enhancing oil recovery, Front. Microbiol., 7 (2016) 1-14.
- 72. P. Talukdar, C. Sharma, A. Doley, K. Barua, A. Borah, P. Agarwal, P. Deori, Isolation and characterization of biosurfactant producing microorganisms from petroleum contaminated soil samples for EOR and bioremediation, Pet. Sci. Technol., 35 (2017) 2102-2108.