Isolation and characterization of alkane hydrocarbons-degrading Delftia tsuruhatensis strain D9 from petroleum-contaminated soils

Abstract

A bacterial strain from petroleum-contaminated soil in south-eastern Turkey was isolated and characterized to determine the potential of alkane hydrocarbon biodegradation. Phenotypic characteristics and the sequence analysis of the 16S rRNA gene revealed that the strain D9 is a member of the Delfitia genus and most similar to Delftia tsuruhatensis (100%). The optimum pH and temperature values for the growth of D. tsuruhatensis strain D9 were found to be 9.0-10.0 and 35°C, respectively. The strain was found to grow in some single, medium and long-chain hydrocarbons such as decane, hexadecane, and squalene, tested by short-time incubation in basal medium (BM) in the presence of 1% hydrocarbon concentrations under optimum conditions. After incubation for 3 days, 65% of the single hydrocarbon hexadecane was degraded by the D. tsuruhatensis strain D9, revealed by GC-MS analysis. The biodegradation of petroleum hydrocarbons by D. tsuruhatensis strain D9 isolated and characterized in the present study shows that it can be a good candidate in the bioremediation process.

Keywords

• Alkane hydrocarbon-degrading bacterium
• Oil pollution
• 16S rRNA gene sequence analysis
• GC-MS analysis
• Delftia

References

1. Adams, G.O., Fufeyin, P.T., Okoro, S.E., Ehinomen, I. (2015). Bioremediation, biostimulation and bioaugmention: a review. International Journal of Environmental Bioremediation & Biodegradation, 3, 28-39. https://doi.org/ 10.12691/ijebb-3-1-5
2. Acer, Ö., Güven, K., Bekler, F.M., Gül-Güven, R. (2016). Isolation and characterization of long-chain alkane-degrading Acinetobacter sp. BT1A from oil-contaminated soil in Diyarbakır, in the Southeast of Turkey. Bioremediation Journal, 20(1), 80-87. https://doi.org/10.1080/10889868.2015.1096898
3. Acer, Ö., Güven, K., Poli, A., Donato, P.D., Leone Buono, L., Gül Güven, R., Nicolaus, B., Finore, I. (2020). Acinetobacter mesopotamicus sp. nov., petroleum-degrading bacterium, isolated from petroleum-contaminated soil in Diyarbakir, in the Southeast of Turkey. Current Microbiology, 77(2) ,3192-3200. https://doi.org/10.1007/s00284-020-02134-9
4. Chaerun, S. K, Tazaki, K., Asada, R., Kogure, K. (2004). Bioremediation of coast areas 5 years after the Nakhodka oil spill in the Sea of Japan: isolation and characterization of hydrocarbon-degrading bacteria. Environment International, 30(7), 911-922. https://doi.org/10.1016/j.envint.2004.02.007
5. Chen, W.M., Lin, Y.S., Sheu, D.S., Sheu, S.Y. (2012). Delftia litopenaei sp. nov., a poly-β-hydroxybutyrateaccumulating bacterium isolated from a fresh water shrimp culture pond. International Journal of Systematic and Evolutionary Microbiology, 62, 2315-2321. https://doi.org/10.1099/ijs.0.037507-0
6. Cheng, C., Zhou, W., Dong, X., Zhang, P., Zhou, K., Zhou, D., ... & Ying, J. (2021). Genomic Analysis of Delftia tsuruhatensis Strain TR1180 Isolated From A Patient From China With In4-Like Integron-Associated Antimicrobial Resistance. Frontiers in cellular and infection microbiology, 11: 663933. https://doi.org/10.3389/fcimb.2021.663933
7. Crone, T. J., & Tolstoy, M. (2010). Magnitude of the 2010 gulf of mexico oil leak. Science ,330-634. https://doi.org/10.1126/science.1195840
8. Costes, J.M., & Druelle, V. (1997). Polyciclic aromatic hydrocarbons in the environment: The rehabilitation of old industrial sites. Oil and Gas science and Technology, 52, 425-440. http://dx.doi.org/10.2516/ogst:1997051

9. Chu, W., & Kwan, C.Y. (2003). Remediation of contaminated soil by a solvent/surfactant system. Chemosphere, 53(1), 9-15.http://dx.doi.org/10.1016/S0045-6535(03)00389-8
10. Carro, L., Mulas, R., Pastor-Bueis, R., Blanco, D., Terrón, A.,Gonzalez-Andres, F., Peix, A. (2017). Delftia rhizosphaerae sp. nov. İsolated from the rhizosphere of Cistus ladanifer. International Journal of Systematic and Evolutionary Microbiology, 67, 1957-1960. https://doi.org/10.1099/ijsem.0.001892
11. Cappello, S., Santisi, S., Calogero, R., Hassanshahian, M., Yakimov, M.M. 2012. Characterization of oil-degrading bacteria isolated from bilge water. Water Air and Soil Pollution, 223, 3219-3226. https://doi.org/10.1007/s11270-012-1103-y
12. Dwivedi, A., Chitranshi, S., Gupta, A., Kumar, A., Lal B.J. (2019). Assessment of the petroleum oil degradation capacity of indigenous bacterial species isolated from petroleum oil contaminated soil. International Journal of Environmental Research, 13, 735-746. https://doi.org/10.1007/s41742-019-00210-y
13. Dussault, H.P. (1955). An improved technique for staining red halophilic bacteria. Journal of Bacteriol, 70, 484-485. https://doi.org/10.1128/jb.70.4.484-485.1955
14. Emtiazi, G., Saleh, T., Hassanshahian, M. (2009). The effect of bacterial glutathione s-transferase on morpholine degradation. Biotechnology Journal, 4, 202-205. https://doi.org/10.1002/biot.200800238
15. Fingas, M.F. (2011). Oil spill science and technology: prevention, response, and clean up, 1st. ed. GPP. Elesvier Inc, Burlington, MA 01803, USA.
16. Geng, L., Chen, M., Liang, Q., Liu, W., Zhang, W., Ping, S., Lu, W., Yan, Y., Wang, W, Takeo, M., Lin, M. (2009). Functional analysis of a putative regulatory gene, tadR, involved in aniline degradation in Delftia tsuruhatensis AD9. Archives of Microbiology, 191, 603-614. https://doi.org/10.1007/s00203-009-0488-5
17. Godini, K., Samarghandi , M.R, Zafari , D., Rahmani, A.R., Afkhami, A., Arabestani, M.R. (2018). Isolation and identification of new strains of crude oil degrading bacteria from Kharg Island, Iran. Petroleum Science and Technology, 869-874. https://doi.org/10.1080/10916466.2018.1447961
18. Hamme, D.J, Singh, A., Ward, O.P. (2003). Recent Advances in Petroleum Microbiology. Microbiology and Molecular Biology Reviews. 67(4), 503-549. https://journals.asm.org/doi/full/10.1128/MMBR.67.4.503-549.2003
19. Head, I.M., Jones, D.M., & Roling, W.F. (2006). Marine microorganisms make a meal of oil. Nature Reviews Microbiology, 4,173-182. https://doi.org/10.1038/nrmicro1348.
20. Jin, H.M., Kim, J.M., Lee H. J., Madsen, E. L., Jeon, C.O. (2012). Alteromonas as a keyagent of polycyclic aromatic hydrocarbon biodegradation in crude oil-contaminated coastal sediment. Environmental Science and Technology. 46(14), 7731-7740. https://doi.org/10.1021/es3018545
21. Jørgensen, N.O., Brandt, K.K, Nybroe, O., Hansen, M. (2009). Delftia lacustris sp. nov., a peptidoglycan-degrading bacterium from fresh water, and emended description of Delftia tsuruhatensis as a peptidoglycan-degradingbacterium. Intrnational Journal of Systematic and Evolutionary Microbiology, 59(9), 2195-2199. https://doi.org/10.1099/ijs.0.008375-0
22. Jurelevicius, D., Cotta, S.R., Peixoto, R., Rosado, A.S., Seldin, L. (2012). Distribution of alkane-degrading bacterial communities in soils from King George Island, Maritime Antarctic. European Journal of Soil Biology, 51, 37-44. https://doi.org/10.1016/j.ejsobi.2012.03.006
23. Koma, D., Hasumi, S., Motoki, K. (2003). Biodegradation of n-alkylcyclohexanebyco-oxidation via multiples path ways Acinetobacter sp. ODDK71. Journal of Bioscience and Bioengineering, 95, 641-644. http://dx.doi.org/10.1016/S1389-1723(03)80178-0
24. Khan, M.A.I., Biswas, B., Smith, E., Naidu, R., Megharaj, M. (2018). Toxicit yassessment of fresh and weathered petroleum hydrocarbons in contaminated soil-a review. Chemosphere, 212,755-767. https://doi.org/10.1016/j.chemosphere.2018.08.094
25. Kahng, H.Y., Kukor, J.J., Oh, K.H. (2000). Characterization of strain HY99, a novel microorganism capable of aerobic and anaerobic degradation of aniline. FEMS Microbiology Letters, 190 (2), 215-221. https://doi.org/10.1111/j.1574-6968.2000.tb09289.x
26. Liu, H., Xu, J., Liang, R., Liu, J. (2014). Characterization of the medium-and long-chain n-alkanes degrading Pseudomonas aeruginosa strain SJTD-1 and its alkane hydroxylase genes. PLoS ONE 9(8): e105506. https://doi.org/10.1371/journal.pone.0105506
27. Lenchi, N., Kebbouche-Gana, S., Servais, P., Lamine Gana, M., Llirós, M. (2020). Diesel biodegradation capacities and biosurfactant production in saline-alkaline conditions by Delftia sp NL1, isolated from an Algerian oil field. Geomicrobiology Journal, 37 (5):454-466. https://doi.org/10.1080/01490451.2020.1722769
28. Li, C.T., Yan, Z.F., Chu, X., Hussain, W.D., Yunus, Z., Hozzein, W.N., Li, W.J., Abaydulla G. (2015). Delftia deserti sp. nov., isolated from a desert soil sample. Antonie Van Leeuwenhoek, 107,1445-1450. http://dx.doi.org/10.1007/s10482-015-0440-4
29. Liu, Z., Yang, H., Huang, Z., Zhou, P., Liu S.J. (2002). Degradation of aniline by newly isolated, extremely aniline tolerant Delftia sp. AN3. Applied Microbiology and Biotechnology, 58(5),679-682. http://dx.doi.org/10.1007/s00253-002-0933-8
30. Mapelli, F., Scoma, A., Michoud, G., Aulenta, F., Boon, N., Borin, S., Kalogerakis, N., Daffonchio, D. (2017). Biotechnologies for marine oil spill cleanup: Indissoluble Ties with Microorganisms. Trends in Biotechnology, 35(9),860-870. https://doi.org/10.1016/j.tibtech.2017.04.003
31. Malatova, K. (2005). Isolation and characterization of hydrocarbon degrading bacteria from environmental habitats in western New York State. Rochester Institute of Technology. Rochester.https://scholarworks.rit.edu/cgi/viewcontent.cgi?referer=&httpsredir=1&article=9044&context=theses
32. Mittal, A., & Singh, P. (2009). Isolation of hydrocarbon-degrading bacteria from soils contaminated with crude oil spills. Indian Journal of Experimental Biology, 47(9), 760-765. https://pubmed.ncbi.nlm.nih.gov/19957890/
33. Medina-Bellver, J.I., Marın, P., Delgado, A., Rodríguez-Sánchez, A., Reyes, E., Ramos, J.L., Marqués, S. (2005). Evidencefor in Situ Crude Oil Biodegradation after the Prestige Oil Spill. Environmental Microbiology, 7,773-779. http://dx.doi.org/10.1111/j.1462-2920.2005.00742.x
34. Margesin, R., Labbe, D., Schinner, F., Greer, C. W, Whyte, L.G. (2003). Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Applied and Environmental Microbiology, 69(6), 3085-3092. http://dx.doi.org/ 10.1128/AEM.69.6.3085-3092.2003
35. Macaulay, B.M., Rees, D. (2014). Bioremediation of oilspills: a review of challenges for research advancement. Annals of Environmental Science, 8, 9-37. https://openjournals.neu.edu/aes/journal/article/view/v8art2
36. Muthukamalam, S., Sivagangavathi, S., Dhrishya, D., Rani, S.S. (2017). Characterization of dioxygenasesandbiosurfactantsproducedbycrudeoildegradingsoilbacteria. Brazilian Journal of Microbiology, 48(4), 637-647. http://dx.doi.org/10.1016/j.bjm.2017.02.007
37. Nie, M., Yin, X., Ren, C., Wang, Y., Xu, F., & Shen, Q. (2010). Novel rhamnolipid biosurfactants produced by a polycyclic aromatic hydrocarbon-degrading bacterium Pseudomonas aeruginosa strain NY3. Biotechnology advances, 28(5), 635-643. http://dx.doi.10.1016/j.biotechadv.2010.05.013
38. Nie, Y., Liang, J.L, Fang, H., Tang, Y.Q, Wu, X.L. (2014). Characterization of a Cyp153 alkane hydroxylase gene in a gram-positive Dietzia sp. DQ12- 45-1b and its team role with alkw1 in alkane degradation. Applied Microbiology and Biotechnology,98,163-173. http://dx.doi.org/10.1007/s00253-013-4821-1
39. Nkem, B.M., Halimoon, N., Yusoff, F.M., Johari, W.L.W., Zakaria, M. P., Medipally, S.R., Kannan, N. (2016). Isolation, identification and diesel-oil biodegradation capacities of indigenous hydrocarbon-degrading strains of Cellulosimicrobium cellulans and Acinetobacter baumannii from tarball at Terengganu beach, Malaysia. Marine Pollution Bulletin,107(1), 261-268. http://dx.doi.org/10.1016/j.marpolbul.2016.03.060
40. Ojo, O.A. (2006). Petroleum hydrocarbon utilization by native bacterial population from a wastewater canal Southwest Nigeria. African Journal of Biotechnology, 5(4), 333-337. https://www.ajol.info/index.php/ajb/article/view/137800
41. Peterson, C.H., Rice, S.D., Short, J. W., Esler, D., Bodkin, J.L., Ballachey, B.E., Irons, D.B. (2003). Long-termecosystem response to the exxon valdez oil spill. Science, 302, 2082-2086. https://doi.org/10.1126/science.1084282
42. Parales, P.E., & Haddock, J.D. (2004). Biocatalytic degradation of pollutants. Current Opinion in Biotechnology, 15(4),374-379. http://dx.doi.org/10.1016/j.copbio.2004.06.003
43. Pieper, D.H., Dos Santos, V.M., Golyshin, P.N. (2004). Genomic and mechanistic insight into the biodegradation of organic pollutant. Current Opinion in Biotechnology, 15, 215-224. http://dx.doi.org/10.1016/j.copbio.2004.03.008
44. Panda, S.K., Kar, R.N., Panda, C.R. (2013). Isolation and identification of petroleum hydrocarbon degrading microorganisms from oil contaminated environment. İnternational Journal of Environmental Sciences, 3(5),1314-1321.https://doi.org/10.6088/ijes.2013030500001
45. Razak, C.N.A., Wang, W., Rahman, S.H.S.A., Basri, M., Salleh, A.B. (1999). Isolation of the crude oil degrading marine Acinetobacter sp. Ell. Acta Scientific Biotechnology,19 (3):213-223. https://doi.org/10.1002/ABIO.370190307
46. Roy, A. S., Baruah, R., Borah, M., Singh, A. K., Boruah, H. P. D., Saikia, N., ... & Bora, T. C. (2014). Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. International Biodeterioration & Biodegradation, 94, 79-89. http://dx.doi.org/10.1016/j.ibiod.2014.03.024
47. Shigematsu, T., Yumihara, K., Ueda, Y., Numaguch, M., Morimura, S., Kida, K. (2003). Delftiatsuruhatensis sp. nov., a terephthalate-assimilating bacterium isolated from activated sludge. International Journal of Systematic and Evolutionary, 53(5), 1479-1483. https://doi.org/10.1099/ijs.0.02285-0
48. Sarkar, P., Roy, A., Pal, S., Mohapatra, B., Kazy, S.K, Maiti, M.K, Sar, P. (2017). Enrichment and characterization of hydrocarbon-degradingbacteria from petroleum refinery waste as potent bioaugmentation agent for in situ bioremediation. Bioresource Technology, 242:15-27. https://doi.org/10.1016/j.biortech.2017.05.010
49. Simaria, C., Pant, G., Sibi, G. (2015). Characterizationandevaluation of polycyclic aromatic hydrocarbon (Pah) degrading bacteria isolated from oil contaminated soil. Applied Microbiology: Open Access, 1:1. https://doi.org/10.4172/2471-9315.1000104
50. Sheludchenko, M.S., Kolomytseva, M.P, Travkin, V.M., Akimov, V.N., Goloveva, L.A. (2005). Degradation of aniline by Delftia tsuruhatensis 14S in batch and continuous processes. Applied Biochemistry and Microbiology, 41, 465-468. https://doi.org/10.1007/s10438-005-0083-8
51. Tremblay J., Yergeau, E., Fortin, N., Cobanli, S., Elias, M., King, T.L., Lee, K., Greer, C.W. (2017). Chemical dispersants enhance the nactivity of oil-and gas condensate-degrading marine bacteria. The ISME Journal, 11, 2793-2808. https://doi.org/10.1038/ismej.2017.129
52. Throne-Holst, M., Wentzel, A., Ellingsen, T.E., Kotlar, H.K., Zotchev, S.B. (2007). Identification of novel genes involved in long-chain n-alkane degradation by Acinetobacter sp. strain DSM 17874. Applied and Environmental Microbiology, 73(10),3327-3332. https://doi.org/10.1128/AEM.00064-07
53. Urata, M., Uchida, E., Nojiri, H., Omori, T., Obo, R., Miyaura, N., Ouchiyama, N. (2004). Genes involved in aniline degradation by Delftia acidovorans strain 7N and its distribution in the natural environment. Bioscience, Biotechnology, and Biochemistry, 68(12), 2457-2465. https://doi.org/10.1271/bbb.68.2457
54. Varjani, S.J., & Upasani, V.N. (2016). Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM 5514. Bioresource Technology, 222,195-201. https://doi.org/10.1016/j.biortech.2016.10.006
55. Varjani, S.J. (2017). Microbial degradation of petroleum hydrocarbons. Bioresource technology, 223, 277-286. https://doi.org/10.1016/j.biortech.2016.10.037
56. Vásquez-Piñeros, M.A., Martínez-Lavanchy P.M, Jehmlich, N., Pieper D.H, Rincón C.A, Harms, H., Junca, H., Heipieper, H.J. (2018). Delftia sp. LCW, a strain isolated from a constructed wetland shows novel properties for dimethylphenol isomers degradation. BMC Microbiology, 18:108. https://doi.org/10.1186/s12866-018-1255-z
57. Vacca, D., Bleam, W., Hickey, W.(2005). Isolation of soil bacteria adapted to degrade humic acid-sorbed phenanthrene. Applied and Environmental Microbiology, 71, 3797-380. https://doi.org/10.1128/AEM.71.7.3797-3805.2005
58. Wu, W., Huang, H., Ling, Z., Yu, Z., Jiang, Y., Liu, P., Li, X. (2016). Genome sequencing reveals mechanisms for heavy metal resistance and polycyclic aromatic hydrocarbon degradation in Delftia lacustris strain LZ-C. Ecotoxicology, 25, 234-247. https://doi.org/10.1007/s10646-015-1583-9
59. Wang, X.B, Chi, C.Q., Nie, Y., Tang, Y.Q., Tan, Y., Wu, G, Wu, X.L. (2011). Degradation of petroleum hydrocarbons (C6-C40) and crude oil by a novel Dietzia strain. Bioresource Technology, 102: 7755-7761. https://dx.doi.org/10.1016/j.biortech.2011.06.009
60. Wen, A., Fegan, M., Hayward, C., Chakraborty, S., Lindsay, I.S. (1999). Phylogeneticrelation ships among members of the Comamonadaceae ,and description of Delftia acidovorans (den Dooren de Jong 1926 and Tamaoka et al. 1987) gen. nov., comb. nov. International Journal of Systematic Bacteriology, 2, 567-576. https://doi.org/10.1099/00207713-49-2-567
61. Xiao, C., Ning, J., Hai Yan, H., Sun, X.D, Hu, J. (2009). Biodegradation of aniline by a newly isolated Delftia sp. XYJ6. Chinese Journal of Chemical Engineering,17(3), 500-505. https://doi.org/10.1016/S1004-9541(08)60237-2
62. Xu, X., Zhai, Z., Li, H., Wang, Q., Han, X., Yu, H. (2017). Synergeticeffect of bio-photocatalytichybrid system: g-C3N4, and Acinetobacter, sp. JLS1 for enhanced degradation of C16 alkane. Chemical Engineering Journal, 323, 520-529. https://doi.org/10.1016/j.cej.2017.04.138
63. Xu, X., Liu, W., Tian, S., Wang, W., Qi, Q., Jiang, P., ... & Yu, H. (2018). Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis. Frontiers in microbiology, 9, 2885. https://doi.org/10.3389/fmicb.2018.02885
64. Ye, J.X., Lin, T.H., Hu, J.T., Poudel, R., Cheng, Z.W., Zhang, S.H., Chen, J.M., Chen, D.Z. (2019). Enhancing chlorobenzene biodegradation by Delftia tsuruhatensis using a water-silicone oil biphasic system. International Journal of Environmental Research and Public Health,16(9), 1629. https://doi.org/10.3390/ijerph16091629
65. Zhang, Z., Hou, Z., Yang, C., Ma, C., Tao,F., Xu, P. (2011). Degradation of n-alkanes and polycyclic aromatic hydrocarbons in petroleum by a newly isolated Pseudomonas aeruginosa DQ8. Bioresource Technology, 102(5), 4111-4116. https://doi.org/10.1016/j.biortech.2010.12.064