Enrichment and Identification of Phenanthrene-Degrading Bacteria Isolated from the Oil-Stained Engine Sediment in the Mangrove Swamps of Thailand
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Published:
Mar 19, 2021
Keywords:
Biodegradation Mangrove Phenanthrene-degrading bacteria Polycyclic aromatic hydrocarbon
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Abstract
Polycyclic aromatic hydrocarbons (PAHs) are persistent pollutants that contaminate various environments. The biodegradation method conducted by bacteria is a promising alternative approach to remediate PAHs. Mangrove bacteria play a role in biogeochemical cycles and are able to degrade PAHs. The aims of this study included the enrichment, isolation, and characterization of phenanthrene (or tricyclic PAH)-degrading bacteria from some oil-stained engine sediments in a mangrove swamp in Rayong Province, Thailand. Ten isolated phenanthrenedegrading bacteria with a high ability for biodegradation were phenotypically and genetically identified. They are considered proteobacteria in the genera of Achromobacter, Comamonas, and Pseudomonas. The phenanthrene biodegradation results revealed that Pseudomonas sp. strain MP6-0207 could degrade phenanthrene 52.35 ± 0.28% of 100 mg/L of phenanthrene supplemented in saline Bushnell Haas Medium within 7 days. Its cells could adhere to the hydrophobic structure of phenanthrene with a BATH value of 45.17 ± 0.29% and produced biosurfactant to solubilize phenanthrene with E24 value of 32.33 ± 2.52%. The knowledge gained from this study offers a novel report on the isolation of phenanthrene-degrading bacteria from the mangrove swamp in Rayong Province, Thailand and could be used for future PAHs bioremediation in the contaminated sites.
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Chantarasiri, A. (2021). Enrichment and Identification of Phenanthrene-Degrading Bacteria Isolated from the Oil-Stained Engine Sediment in the Mangrove Swamps of Thailand. Applied Science and Engineering Progress, 14(2), 206–218. https://doi.org/10.14416/j.asep.2020.04.003
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Research Articles
References
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[26] A. Ferbiyanto, I. Rusmana, and R. Raffiudin, “Characterization and identification of cellulolytic bacteria from gut of worker Macrotermes gilvus,” HAYATI Journal of Biosciences, vol. 22, no. 4, pp. 197–200, Oct. 2015.
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[38] X. T. Jiang, X. Peng, G. H. Deng, H. F. Sheng, Y. Wang, H. W. Zhou, and N. F. Y. Tam, “Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland,” Microbial Ecology, vol. 66, no. 1, pp. 96– 104, Jul. 2013.
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[2] G. Zhang, X. Guo, Y. Zhu, X. Liu, Z. Han, K. Sun, L. Ji, Q. He, and L. Han, “The effects of different biochars on microbial quantity, microbial community shift, enzyme activity, and biodegradation of polycyclic aromatic hydrocarbons in soil,” Geoderma, vol. 328, pp. 100–108, Oct. 2018.
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[5] Z. Cui, G. Xu, W. Gao, Q. Li, B. Yang, G. Yang, and L. Zheng, “Isolation and characterization of Cycloclasticus strains from Yellow Sea sediments and biodegradation of pyrene and fluoranthene by their syntrophic association with Marinobacter strains,” International Biodeterioration & Biodegradation, vol. 91, pp. 45–51, Jul. 2014.
[6] R. H. Peng, A. S. Xiong, Y. Xue, X. Y. Fu, F. Gao, W. Zhao, Y. S. Tian, and Q. H. Yao, “Microbial biodegradation of polyaromatic hydrocarbons,” FEMS Microbiology Reviews, vol. 32, no. 6, pp. 927–955, Nov. 2008.
[7] N. Supaka, P. Pinphanichakarn, K. Pattaragulwanit, S. Thaniyavarn, T. Omori, and K. Juntongjin, “Isolation and characterization of a phenanthrenedegrading Sphingomonas sp. strain P2 and its ability to degrade fluoranthene and pyrene via cometabolism,” ScienceAsia, vol. 27, no. 1, pp. 21– 28, Mar. 2001.
[8] M. G. Waigi, F. Kang, C. Goikavi, W. Ling, and Y. Gao, “Phenanthrene biodegradation by sphingomonads and its application in the contaminated soils and sediments: A review,” International Biodeterioration & Biodegradation, vol. 104, pp. 333–349, Oct. 2015.
[9] Z. D. Umar, N. A. A. Aziz, S. Z. Zulkifli, and M. Mustafa, “Effective phenanthrene and pyrene biodegradation using Enterobacter sp. MM087 (KT933254) isolated from used engine oil contaminated soil,” Egyptian Journal of Petroleum, vol. 27, no. 3, pp. 349–359, Sep. 2018.
[10] M. Hassanshahian, G. Emtiazi, R. K. Kermanshahi, and S. Cappello, “Comparison of oil degrading microbial communities in sediments from the Persian Gulf and Caspian Sea,” Soil and Sediment Contamination, vol. 19, no. 3, pp. 277–291, Apr. 2010.
[11] A. K. Haritash and C. P. Kaushik, “Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): A review,” Journal of Hazardous Materials, vol. 169, no. 1–3, pp. 1–15, Sep. 2009.
[12] P. Tiralerdpanich, P. Sonthiphand, E. Luepromchai, O. Pinyakong, and P. Pokethitiyook, “Potential microbial consortium involved in the biodegradation of diesel, hexadecane and phenanthrene in mangrove sediment explored by metagenomics analysis,” Marine Pollution Bulletin, vol. 133, pp. 595–605, Aug. 2018.
[13] R. Boonyatumanond, G. Wattayakorn, A. Togo, and H. Takada, “Distribution and origins of polycyclic aromatic hydrocarbons (PAHs) in riverine, estuarine, and marine sediments in Thailand,” Marine Pollution Bulletin, vol. 52, no. 8, pp. 942– 956, Aug. 2006.
[14] A. Chantarasiri, “Aquatic Bacillus cereus JD0404 isolated from the muddy sediments of mangrove swamps in Thailand and characterization of its cellulolytic activity,” Egyptian Journal of Aquatic Research, vol. 41, no. 3, pp. 257–264, 2015.
[15] A. Chantarasiri, P. Boontanom, and N. Nuiplot, “Isolation and characterization of Lysinibacillus sphaericus BR2308 from coastal wetland in Thailand for the biodegradation of lignin,” AACL Bioflux, vol. 10, no. 2, pp. 200–209, Apr. 2017.
[16] A. C. F. Dias, F. D. Andreote, F. Dini-Andreote, P. T. Lacava, A. L. B. Sá, I. S. Melo, J. L. Azevedo, and W. L. Araújo, “Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment,” World Journal of Microbiology and Biotechnology, vol. 25, no. 7, pp. 1305–1311, Jul. 2009.
[17] Y. Tian, H. J. Liu, T. L. Zheng, K. K. Kwon, S. J. Kim, and C. L. Yan, “PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China,” Marine Pollution Bulletin, vol. 57, no. 6–12, pp. 707–715, 2008.
[18] H. W. Zhou, T. G. Luan, F. Zou, and N. F. Y. Tam, “Different bacterial groups for biodegradation of three- and four-ring PAHs isolated from a Hong Kong mangrove sediment,” Journal of Hazardous Materials, vol. 152, no. 3, pp. 1179–1185, Apr. 2008.
[19] H. W. Zhou, A. H. Y. Wong, R. M. K. Yu, Y. D. Park, Y. S. Wong, and N. F. Y. Tam, “Polycyclic aromatic hydrocarbon-induced structural shift of bacterial communities in mangrove sediment,” Microbial Ecology, vol. 58, pp. 153–160, 2009.
[20] C. Guo, Z. Dang, Y. Wong, and N. F. Y. Tam, “Biodegradation ability and dioxgenase genes of PAH-degrading Sphingomonas and Mycobacterium strains isolated from mangrove sediments,” International Biodeterioration & Biodegradation, vol. 64, no. 6, pp. 419–426, Sep. 2010.
[21] W. Wongwongsee, P. Chareanpat, and O. Pinyakong, “Abilities and genes for PAH biodegradation of bacteria isolated from mangrove sediments from the central of Thailand,” Marine Pollution Bulletin, vol. 74, no. 1, pp. 95–104, Sep. 2013.
[22] N. F. Y. Tam, L. Ke, X. H. Wang, and Y. S. Wong, “Contamination of polycyclic aromatic hydrocarbons in surface sediments of mangrove swamps,” Environmental Pollution, vol. 114, no. 2, pp. 255–263, Sep. 2001.
[23] S. Das and H. R. Dash, “Exp. 6.6 Spectrophotometric analysis of bioremediation of polycyclic aromatic hydrocarbons by bacteria,” in Microbial Biotechnology- A Laboratory Manual for Bacterial Systems, 1st ed., New Delhi: Springer India, 2015, pp. 229–231.
[24] R. J. Goodyear and F. Vernon, “Spectrophotometric determination of pyrene, fluoranthrene and phenanthrene in anthracene oil,” Analytical Letters, vol. 3, no. 6, pp. 299–306, 1970.
[25] A. A. Dashti, M. M. Jadaon, A. M. Abdulsamad, and H. M. Dashti, “Heat treatment of bacteria: A simple method of DNA extraction for molecular techniques,” Kuwait Medical Journal, vol. 41, no. 2, pp. 117–122, 2009.
[26] A. Ferbiyanto, I. Rusmana, and R. Raffiudin, “Characterization and identification of cellulolytic bacteria from gut of worker Macrotermes gilvus,” HAYATI Journal of Biosciences, vol. 22, no. 4, pp. 197–200, Oct. 2015.
[27] M. Gouy, S. Guindon, and O. Gascuel, “SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building,” Molecular Biology and Evolution, vol. 27, no. 2, pp. 221–224, Feb. 2010.
[28] C. W. Zoueki, N. Tufenkji, and S. Ghoshal, “A modified microbial adhesion to hydrocarbons assay to account for the presence of hydrocarbon droplets,” Journal of Colloid and Interface Science, vol. 344, no. 2, pp. 492–496, Apr. 2010.
[29] D. J. Brenner, N. R. Krieg, and J. T. Stanley “Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria,” in Bergey’s Manual of Systematic Bacteriology Volume 2 : The Proteobacteria, 2nd ed., G. Garrity, Ed. New York: Springer, 2005, pp. 658–661.
[30] R. F. Al-Thani, D. A. M. Abd-El-Haleem, and M. Al-Shammri, “Isolation and characterization of polyaromatic hydrocarbons-degrading bacteria from different Qatari soils,” African Journal of Microbiology Research, vol. 3, no. 11, pp. 761– 766, Nov. 2009.
[31] N. Hou, N. Zhang, T. Jia, Y. Sun, Y. Dai, Q. Wang, D. Li, Z. Luo, and C. Li, “Biodegradation of phenanthrene by biodemulsifier-producing strain Achromobacter sp. LH-1 and the study on its metabolisms and fermentation kinetics,” Ecotoxicology and Environmental Safety, vol. 163, pp. 205–214, Nov. 2018.
[32] J. N. Tiwari, M. M. K. Reddy, D. K. Patel, S. K. Jain, R. C. Murthy, and N. Manickam, “Isolation of pyrene degrading Achromobacter xylooxidans and characterization of metabolic product,” World Journal of Microbiology and Biotechnology, vol. 26, no. 10, pp. 1727–1733, Oct. 2010.
[33] D. J. Brenner, N. R. Krieg, and J. T. Stanley “Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria,” in Bergey’s Manual of Systematic Bacteriology Volume 2 : The Proteobacteria, 2nd ed., G. Garrity, Ed. New York: Springer, 2005, pp. 689–695.
[34] A. Willems and P. De Vos, “Comamonas,” in The Prokaryotes, 3rd ed., M. Dworkin, Ed. New York: Springer, 2006, pp. 723–736.
[35] A. K. Goyal and G. J. Zylstra, “Molecular cloning of novel genes for polycyclic aromatic hydrocarbon degradation from Comamonas testosteroni GZ39,” Applied and Environment Microbiology, vol. 62, no. 1, pp. 230–236, Jan. 1996.
[36] D. J. Brenner, N. R. Krieg, and J. T. Stanley “Part B: The Gammaproteobacteria,” in Bergey’s Manual of Systematic Bacteriology Volume 2 : The Proteobacteria, 2nd ed., G. Garrity, Ed. New York: Springer, 2005, pp. 323–378.
[37] S. Rabodonirina, R. Rasolomampianina, F. Krier, D. Drider, D. Merhaby, S. Net, and B. Ouddane, “Degradation of fluorene and phenanthrene in PAHs-contaminated soil using Pseudomonas and Bacillus strains isolated from oil spill sites,” Journal of Environmental Management, vol. 232, pp. 1–7, Feb. 2019.
[38] X. T. Jiang, X. Peng, G. H. Deng, H. F. Sheng, Y. Wang, H. W. Zhou, and N. F. Y. Tam, “Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland,” Microbial Ecology, vol. 66, no. 1, pp. 96– 104, Jul. 2013.
[39] S. Zhang, Z. Hu, and H. Wang, “Metagenomic analysis exhibited the co-metabolism of polycyclic aromatic hydrocarbons by bacterial community from estuarine sediment,” Environmental International, vol. 129, pp. 308–319, Aug. 2019.
[40] S. Lamichhane, K. C. Bal Krishna, and R. Surukkalige, “Surfactant-enhanced remediation of polycyclic aromatic hydrocarbons: A review,” Journal of Environmental Management, vol. 199, pp. 46–61, Sep. 2017.
[41] S. Sun, Y. Wang, T. Zang, J. Wei, H. Wu, C. Wei, G. Qiu, and F. Li, “A biosurfactant-producing Pseudomonas aeruginosa S5 isolated from coking wastewater and its application for bioremediation of polycyclic aromatic hydrocarbons,” Bioresource Technology, vol. 281, pp. 421–428, Jun. 2019.
[42] M. Rosenborg, “Bacterial adherence to hydrocarbons: A useful technique for studying cell surface hydrophobicity,” FEMS Microbiology Letters, vol. 22, no. 3, pp. 289–295, May. 1984.
[43] M. Woźniak-Karczewska, K. Myszka, A. Sznajdrowska, A. Szulc, A. Zgoła-Grześkowiak, Ł. Ławniczak, P. F. X. Corvini, and Ł. Chrzanowski, “Isolation of rhamnolipids-producing cultures from faeces: Influence of interspecies communication on the yield of rhamnolipid congeners,” New Biotechnology, vol. 36, pp. 17–25, May. 2017.
[44] G. S. Reddy, B. Mahendran, and R. S. Reddy, “Screening and optimization of Achromobacter xylosoxidans GSMSR13B producing bacteria,” Journal
[45] K. Saisa-ard, A. Saimmai, and S. Maneerat, “Characterization and phylogenetic analysis of biosurfactant-producing bacteria isolated from palm oil contaminated soils,” Songklanakarin Journal of Science and Technology, vol. 36, no. 2, pp. 163–175, 2014.
[46] H. Tebyanian, M. Hassanshahian, and A. Kariminik, “Hexadecane-degradation by Teskumurella and Stenotrophomonas strains isolated from hydrocarbon contaminated soils,” Jundishapur Journal of Microbiology, vol. 6, no. 7, p. e9182, Sep. 2013.
[47] R. C. John, J. P. Essien, S. B. Akpan, and G. C. Okpokwasili, “Polycyclic aromatic hydrocarbondegrading bacteria from aviation fuel spill site at Ibeno, Nigeria,” Bulletin of Environmental Contamination and Toxicology, vol. 88, no. 6, pp. 1014–1019, Jun. 2012.