Abstract
The contamination of the environment by crude oil and its by-products, mainly composed of aliphatic and aromatic hydrocarbons, is a widespread problem. Biodegradation by bacteria is one of the processes responsible for the removal of these pollutants. This study was conducted to determine the abilities of Burkholderia sp. B5, Cupriavidus sp. B1, Pseudomonas sp. T1, and another Cupriavidus sp. X5 to degrade binary mixtures of octane (representing aliphatic hydrocarbons) with benzene, toluene, ethylbenzene, or xylene (BTEX as aromatic hydrocarbons) at a final concentration of 100 ppm under aerobic conditions. These strains were isolated from an enriched bacterial consortium (Yabase or Y consortium) that prefer to degrade aromatic hydrocarbon over aliphatic hydrocarbons. We found that B5 degraded all BTEX compounds more rapidly than octane. In contrast, B1, T1 and X5 utilized more of octane over BTX compounds. B5 also preferred to use benzene over octane with varying concentrations of up to 200 mg/l. B5 possesses alkane hydroxylase (alkB) and catechol 2,3-dioxygenase (C23D) genes, which are responsible for the degradation of alkanes and aromatic hydrocarbons, respectively. This study strongly supports our notion that Burkholderia played a key role in the preferential degradation of aromatic hydrocarbons over aliphatic hydrocarbons in the previously characterized Y consortium. The preferential degradation of more toxic aromatic hydrocarbons over aliphatics is crucial in risk-based bioremediation.
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References
Adzigbli L, Bacosa HP, Deng Y (2018) Response of microbial communities to oil spill in the Gulf of Mexico. A review. Afr J Microbiol Res 12(23):536–545. https://doi.org/10.5897/AJMR2018.8843
Bacosa HP, Inoue C (2020) Heavy oil degrading Burkholderia and Pseudomonas strains: insights on the degradation potential of isolates and microbial consortia. Pal Sci 12:74–89
Bacosa HP, Suto K, Inoue C (2010) Preferential degradation of aromatic hydrocarbons in kerosene by a microbial consortium. Int Biodeterior Biodegrad 64:702–710. https://doi.org/10.1016/j.ibiod.2010.03.008
Bacosa HP, Suto K, Inoue C (2011) Preferential utilization of petroleum oil hydrocarbon components by microbial consortia reflects degradation pattern in aliphatic–aromatic hydrocarbon binary mixtures. World J Microbiol Biotechnol 27:1109–1117. https://doi.org/10.1007/s11274-010-0557-6
Bacosa HP, Suto K, Inoue C (2012) Bacterial community dynamics during the preferential degradation of aromatic hydrocarbons by a microbial consortium. Int Biodeterior Biodegrad 74:109–115. https://doi.org/10.1016/j.ibiod.2012.04.022
Bacosa HP, Suto K, Inoue C (2013) Degradation potential and microbial community structure of heavy-oil enriched microbial consortia from mangrove sediments in Okinawa, Japan. J Environ Sci Health A 48:835–846. https://doi.org/10.1080/10934529.2013.761476
Bacosa HP, Erdner D, Liu Z (2015) Differentiating the roles of photooxidation and biodegradation in the weathering of light louisiana sweet crude oil in surface water from the Deepwater Horizon site. Mar Pollut Bull 95:265–272. https://doi.org/10.1016/j.marpolbul.2015.04.005
Bacosa HP, Thyng KM, Plunkett S, Erdner DL, Liu Z (2016) The tarballs on Texas beaches following the 2014 Texas City “Y” spill: modeling, chemical, and microbiological studies. Mar Pollut Bull 109:236–244. https://doi.org/10.1016/j.marpolbul.2016.05.076
Bacosa HP, Erdner DL, Rosenheim B, Shetty P, Seitz K, Baker B, Liu Z (2018) Hydrocarbon degradation and response of seafloor sediment bacterial community in the northern Gulf of Mexico to light Louisiana sweet crude oil. ISME J 12:2532–2543. https://doi.org/10.1038/s41396-018-0190-1
Bacosa HP, Steichen JM, Kamalanathan M, Windham R, Lubguban A, Labonte M, Kaiser K, Hala D, Santschi PH, Quigg AS (2020) Polycyclic aromatic hydrocarbons (PAHs) and putative PAH degrading bacteria in Galveston Bay, Texas (USA) following the 2017 Hurricane Harvey. Environ Sci Pollut Res 27:34987–34999. https://doi.org/10.1371/journal.pone.0243734
Bacosa HP, Kang A, Lu K, Liu Z (2021) Initial oil concentration affects hydrocarbon biodegradation rates and bacterial community composition in seawater. Mar Pollut Bull 162:111867. https://doi.org/10.1016/j.marpolbul.2020.111867
Chaerun KS, Tazaki K, Asada R, Kogure K (2004) Bioremediation of coastal areas 5 years after the Nakhodka oil spill in the Sea of Japan: isolation and characterization of hydrocarbon-degrading bacteria. Environ Int 30:911–922. https://doi.org/10.1016/j.envint.2004.02.007
Chakraborty R, O’Connor SM, Chan E, Coates JD (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and xylene compounds by Dechloromonas strain RCB. Appl Environ Microbiol 71(12):8649–8655. https://doi.org/10.1128/AEM.71.12.8649-8655.2005
Dominguez JJ, Bacosa HP, Chien MF, Inoue C (2019) Enhanced degradation of polycyclic aromatic hydrocarbons (PAHs) in the rhizosphere of sudangrass (Sorghum × drummondii). Chemosphere 234:789–795. https://doi.org/10.1016/j.chemosphere.2019.05.290
El-Naas MH, Acio JA, El Telib AE (2014) Aerobic biodegradation of BTEX: progresses and prospects. J Environ Chem Eng 2(2):1104–1122. https://doi.org/10.1016/j.jece.2014.04.009
Evans M, Liu J, Bacosa H, Rosenheim BE, Liu Z (2017) Petroleum hydrocarbon persistence following the deepwater horizon oil spill as a function of shoreline energy. Mar Pollut Bull 115:47–56. https://doi.org/10.1016/j.marpolbul.2016.11.022
Gemmell B, Bacosa HP, Liu Z, Buskey EJ (2016) Can gelatinous zooplankton influence the fate of crude oil in marine environments? Mar Pollut Bull 113:483–487. https://doi.org/10.1016/j.marpolbul.2016.08.065
Gemmell B, Bacosa HP, Dickey B, Gemmell C, Alqasemi L, Buskey E (2018) Rapid alterations to marine microbiota communities following an oil spill. Ecotoxicology 27:505–515. https://doi.org/10.1007/s10646-018-1923-7
Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243. https://doi.org/10.1016/S0958-1669(00)00090-2
Greenwood PF, Wibrow S, George SJ, Tibbett M (2008) Sequential hydrocarbon biodegradation in a soil from arid coastal Australia, treated with oil under laboratory controlled conditions. Org Geochem 39:1336–1346. https://doi.org/10.1016/j.orggeochem.2008.05.005
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Heider J (2007) Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr Opin Chem Biol 11(2):188–194. https://doi.org/10.1016/j.cbpa.2007.02.027
Hennessee CT, Li QX (2016) Effects of polycyclic aromatic hydrocarbon mixtures on degradation, gene expression, and metabolite production in four mycobacterium species. Appl Environ Microbiol 82:3357–3369. https://doi.org/10.1128/AEM.00100-16
Juhasz AL, Stanley GA, Britz ML (2002) Metabolite repression inhibits degradation of benzo[a]pyrene and dibenz[a, h]anthracene by Stenotrophomonas maltophila VUN 10, 003. J Ind Microbiol Biotechnol 28:88–96. https://doi.org/10.1038/sj/jim/7000216
Kamalanathan M, Chiu MH, Bacosa HP, Schwehr K, Tsai SM, Doyle S, Yard A, Mapes S, Vasquez C, Bretherton L, Sylvan JB, Santschi P, Chin WC, Quigg A (2019) Role of polysaccharides in diatom Thalassiosira pseudonana and its associated bacteria in hydrocarbon presence. Plant Physiol 180(4):1898–1911. https://doi.org/10.1104/pp.19.00301
Laban NA, Selesi D, Jobelius C, Meckenstock RU (2009) Anaerobic benzene degradation by gram-positive sulfate-reducing bacteria. FEMS Microbiol Ecol 68:300–311. https://doi.org/10.1111/j.1574-6941.2009.00672.x
Lee SH, Jin HM, Lee HJ, Kim JM, Jeon CO (2012) Complete genome sequence of the BTEX-degrading bacterium Pseudoxanthomonas spadix BD-a59. J Bacteriol 194(2):544. https://doi.org/10.1128/JB.06436-11
Lee Y, Lee Y, Jeon CO (2019) Biodegradation of naphthalene, BTEX, and aliphatic hydrocarbons by Paraburkholderia aromaticivorans BN5 isolated from petroleum-contaminated soil. Sci Rep 9:860. https://doi.org/10.1038/s41598-018-36165-x
Liu J, Bacosa HP, Liu Z (2017) Potential environmental factors affecting oil-degrading bacterial populations in deep and surface waters of the northern Gulf of Mexico. Front Microbiol 7:2131. https://doi.org/10.3389/fmicb.2016.02131
Masekameni MD, Moolla R, Gulumian M, Brouwer D (2019) Risk assessment of benzene, toluene, ethyl benzene, and xylene concentrations from the combustion of coal in a controlled laboratory environment. Int J Environ Res Public Health 16(1):95. https://doi.org/10.3390/ijerph16010095
McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat Biosyst 8:1–19. https://doi.org/10.1186/2046-9063-8-10
Mesarch MB, Nakatsu CH, Nies L (2000) Development of catechol 2,3-dioxygenase-specific primers for monitoring bioremediation by competitive quantitative PCR. Appl Environ Microbiol 66(2):678–683. https://doi.org/10.1128/AEM.66.2.678-683.2000
Murphy D, Gemmell B, Vaccarri L, Li C, Bacosa HP, Evans M, Gemmell C, Harvey T, Jalali M, Niepa T (2016) An in-depth survey of the oil spill literature since 1968: long term trends and changes since deepwater horizon. Mar Pollut Bull 113:371–379. https://doi.org/10.1016/j.marpolbul.2016.10.028
Musat F, Widdel F (2008) Anaerobic degradation of benzene by a marine sulfate-reducing enrichment culture, and cell hybridization of the dominant phylotype. Environ Microbiol 10:10–19
Nichols D (2007) Cultivation gives context to the microbial ecologist. FEMS Microbiol Ecol 60(3):351–357. https://doi.org/10.1111/j.1574-6941.2007.00332.x
Potter TL, Simmons KE (1998) Composition of petroleum mixtures. Total petroleum hydrocarbon criteria working group series, vol 2. Amherst Scientific Publishers, Amherst, pp 75–80. https://doi.org/10.1111/j.1462-2920.2007.01425.x
Powell SM, Ferguson SH, Bowman JP, Snape I (2006) Using real-time PCR to assess changes in the hydrocarbon-degrading microbial community in Antarctic soil during bioremediation. Microb Ecol 52:523–532. https://doi.org/10.1007/s00248-006-9131-z
Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248. https://doi.org/10.1016/S0167-7799(02)01943-1
Severin T, Bacosa HP, Sato A, Erdner DL (2016) Dynamics of Heterocapsa sp. and the associated attached and free-living bacteria under the influence of dispersed and undispersed crude oil. Lett Appl Microbiol 63:419–425. https://doi.org/10.1111/lam.12661
Steichen JL, Labonté JM, Windham R, Hala D, Kaiser K, Setta S, Faulkner PC, Bacosa HP, Yan G, Kamalanathan M, Quigg A (2020) Microbial, physical, and chemical changes in Galveston Bay following an extreme flooding event, Hurricane Harvey. Front Mar Sci 7:186. https://doi.org/10.3389/fmars.2020.00186
Singh P, Singh VP, Singh R, Borthakur A, Madhav S, Ahamad A, Kumar A, Pal DB, Tiwary D, Mishra PK (2020) Bioremediation: a sustainable approach for management of environmental contaminants. In: Singh P, Kumar A, Borthakur A (eds) Abatement of environmental pollutants. Elsevier, Amsterdam, pp 1–23. https://doi.org/10.1016/B978-0-12-818095-2.00001-1
Sun L, Chiu M, Xu C, Lin P, Schwehr K, Bacosa HP, Kamalanathan M, Quigg A, Chin W, Santschi P (2018) The effects of sunlight on the composition of exopolymeric substances and subsequent aggregate formation during oil spills. Mar Chem 203:49–54. https://doi.org/10.1016/j.marchem.2018.04.006
Tao Y, Fishman A, Bentley WE, Wood TK (2004) Altering toluene 4-monooxygenase by active-site engineering for thesynthesis of 3-methoxycatechol, methoxyhydroquinone, andmethylhydroquinone. J Bacteriol 186:4705–5471. https://doi.org/10.1128/JB.186.14.4705-4713.2004
Takami H, Kobata K, Nagahama T, Kobayashi H, Inoue A, Horikoshi K (1999) Biodiversity in deep-sea sites located near the south part of Japan. Extremophiles 3:97–102. https://doi.org/10.1007/s007920050104
Vaillancourt FH, Bolin JT, Eltis LH (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41:241–267. https://doi.org/10.1080/10409230600817422
Vogt C, Kleinsteuber S, Richnow HH (2011) Anaerobic benzene degradation by bacteria. Microb Biotechnol 4(6):710–724. https://doi.org/10.1111/j.1751-7915.2011.00260.x
Williams K, Bacosa HP, Quigg A (2017) The impact of dissolved inorganic nitrogen and phosphorous on responses of microbial plankton to the Texas City “Y” oil spill in Galveston Bay, Texas (USA). Mar Pollut Bull 121:32–44. https://doi.org/10.1016/j.marpolbul.2017.05.033
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Hernando Bacosa is grateful to the support from the Japanese Government Monbukagakusho Scholarship program to pursue graduate studies in Tohoku University.
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Bacosa, H.P., Mabuhay-Omar, J.A., Balisco, R.A.T. et al. Biodegradation of binary mixtures of octane with benzene, toluene, ethylbenzene or xylene (BTEX): insights on the potential of Burkholderia, Pseudomonas and Cupriavidus isolates. World J Microbiol Biotechnol 37, 122 (2021). https://doi.org/10.1007/s11274-021-03093-4
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DOI: https://doi.org/10.1007/s11274-021-03093-4