Effect of heavy metals and other xenobiotics on biodegradation of waste canola oil by cold-adapted Rhodococcus sp. strain AQ5-07

  • S. Ibrahim Universiti Putra Malaysia
  • A. Zulkharnain
  • K. N. M. Zahri
  • G. L.Y. Lee
  • P. Convey
  • C. Gomez-Fuentes
  • S. Sabri
  • K. A.K. Khalil
  • S. A. Alias
  • G. Gonzalez-Rocha
  • S. A. Ahmad
Keywords: Antarctica, biodegradation, canola oil, heavy metals, Rhodococcus, xenobiotics


The Antarctic is generally considered to be one of the most pristine areas in the world. However, both long and short-range pollutants are now known to be present in the Antarctic environment. Canola oil is an example of a polluting hydrocarbon that can be accidentally released into the Antarctic environment in oil wastewater treatment plants. The Antarctic soil bacterial strain Rhodococcus sp. AQ5-07, known to be capable of using waste canola oil (WCO) as its sole source of carbon, was tested for its ability to degrade canola oil in the presence of different heavy metals and xenobiotics. Rhodococcus sp. AQ5-07 was grown on minimum salt media containing different heavy metals (Zn, Co, Ni, Ag, Pb, Cu, Cr, Hg, Cd and As), xenobiotics (acrylamide and phenol) supplemented with 3% WCO. Three out of the 10 heavy metals tested (Hg, Cd and Ag) led a significant reduction in canola oil degradation at a concentration of 1 ppm. The IC50 values of Hg, Cd and Ag were 0.38, 0.45 and 0.32 ppm, respectively. The strain could also withstand 10 mg/L acrylamide, 50 mg/L phenol and 0.5% (v/v) diesel. This study confirmed the ability of Rhodococcus sp. AQ5-07 to degrade canola oil in the presence of various heavy metals and other xenobiotics, supporting its potential use in bioremediation of vegetable oil and wastewater treatments in low temperature environments.


Abdel-Salam, A.M., Al-Dekheil, A., Babkr, A., Farahna, M. and Mousa, H.M. (2010). High fiber probiotic fermented mares milk reduces the toxic effects of mercury in rats. North American Journal of Medical Sciences 2, 569-575.

Abdelali F., El-Hassani, F.Z., Aissam, H., Merzouki, M. and Benlemlih, M. (2011). Aerobic treatment of lipid-rich wastewater by a bacterial consortium. African Journal of Microbiology Research 5, 5333-5342.

Abou-Shanab, R.A.I., Van Berkum, P. and Angle, J.S. (2007). Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68, 360-367.

Abubakar, M., Abdul Habib, N.M.S., Manogaran, M., Yasid, N.A., Alias, S.A., Ahmad, S.A., Smykla J., Hassan M.A., and Abd Shukor M.Y. (2019). Response surface-based optimization of the biodegradation of a simulated vegetable oily ballast wastewater under temperate conditions using the Antarctic bacterium Rhodococcus erythropolis ADL36. Desalination and Water Treatment 144, 129-137.

Ahmad, S.A., Shamaan, N.A., Syed, M.A., Dahalan, F.A., Abdul Khalil, K., Ab Rahman, N.A. and Shukor, M.Y. (2017). Phenol degradation by Acinetobacter sp. in the presence of heavy metals. Journal of the National Science Foundation of Sri Lanka 45, 247-253.

Ahmad, S.A., Asokan, G., Yasid, N.A., Nawawi, N.M., Subramaniam, K., Zakaria, N.N. and Shukor, M.Y. (2018). Effect of heavy metals on biodegradation of phenol by Antarctic: Arthrobacter bambusae strain AQ5-003. Malaysian Journal of Biochemistry and Molecular Biology 21, 47-51.

Aktas, E., Yigit, N. and Ayyildiz, A. (2002). Esterase activity in various Candida species. Journal of International Medical Research 30, 322-324.

Alcázar-Medina, F., Núñez-Núñez, C., Rodríguez-Rosales, M., Valle-Cervantes, S., Alarcón-Herrera, M. and Proal-Nájera, J. (2019). Lead removal from aqueous solution by spherical agglomeration using an extract of Agave lechuguilla Torr. as biosurfactant. Revista Mexicana De Ingeniería Química 19, 71-84.

Bargagli, R. (2005) Antarctic ecosystems: environmental contamination, climate change, and human impact. Berlin: Springer.

Bharathi, P., Elavarasi, N. and Mohanasundaram, S. (2012) Studies on rate of biodegradation of vegetable (coconut) oil by using Pseudomonas aureginosa. International Journal of Environmental Biology 2, 12–19.

Buendía-González, L., Cruz-Sosa, F., Rodríguez-Huezo, M., Barrera-Díaz, C., Hernández-Jaimes, C. and Orozco-Villafuerte, J. (2019). In vitro simultaneous accumulation of multiple heavy metals by Prosopis laevigata seedlings cultures. Revista Mexicana De Ingeniería Química 18, 1167-1177.

Buranasilp, K. and Charoenpanich. J. (2011) Biodegradation of acrylamide by Enterobacter aerogenes isolated from wastewater in Thailand. Journal of Environmental Sciences 23, 396-403.

Chan, Y.J., Chong, M.F., Law, C.L. and Hassell, D.G. (2009) A review on anaerobic-aerobic treatment of industrial and municipal wastewater. Chemical Engineering Journal 155, 1-18.

Chudobova, D., Maskova, D., Nejdl, L., Kopel, P., Merlos-Rodrigo, M.A., Adam, V. and Kizek, R. (2013). The effect of silver ions and silver nanoparticles on Staphylococcus aureus. In: Microbial pathogens and strategies for combating them: science, technology and education (A. Méndez-Vilas, ed.), 728-735.

Čipinytė, V., Grigiškis, S. and Baškys, E. (2009) Selection of fat-degrading microorganisms for the treatment of lipid-contaminated environment. Biologija 55, 84-92.

Council of Managers of National Antarctic Programs (COMNAP) (2012). Main Antarctic facilities operated by national Antarctic programs in the Antarctic Treaty Area (south of 60' latitude south). https://www.comnap. aq/Information/SitePages/Home.aspx.

Convey, P., Hughes K.A. and Tin, T. (2012). Continental governance and environmental management mechanisms under the Antarctic Treaty System: Sufficient for the biodiversity challenges of this century?. Biodiversity 13, 234-248.

Corral-Escárcega, M.C., Ruíz-Gutiérrez, M.G., Quintero-Ramos, A., Meléndez-Pizarro, C.O., Landizabal-Gutiérrez, D. and Campos-Venegas, K. (2017). Use of biomass-derivedfrom pecan nut husks (Carya illinoinensis) forchromium removal from aqueous solutions. Column modeling and adsorption kinetic studies. Revista Mexicana de Ingeniería Química 13, 939-953.

Danikuu F.M. and Sowley E.N.K. (2014) Biodegradation of shea nut cake by indigenous soil bacteria. Journal of Medical and Biomedical Sciences 3, 9-15.

Dors, G., Mendes, A.A., Pereira, E.B., de Castro, H.F. and Furigo, A. (2013) Simultaneous enzymatic hydrolysis and anaerobic biodegradation of lipid-rich wastewater from poultry industry. Applied Water Science 3, 343-349.

El-Deeb, B. and Altalhi, A.D. (2009) Degradative plasmid and heavy metal resistance plasmid naturally coexist in phenol and cyanide assimilating bacteria. American Journal of Biochemistry and Biotechnology 5, 84-93.

Hernández-Martínez, R., Valdivia-Rivera, S., Betto-Sagahon, J., Coreño-Alonso, A., Tzintzun-Camacho, O. and Lizardi-Jiménez, M. (2018). Solubilization and removal of petroleum hydrocarbons by a native microbial biomass in a bubble column reactor. Revista Mexicana De Ingeniería Química 18, 181-189.

Hoffman, D.R., Okon J.L. and Sandrin T.R. (2005) Medium composition affects the degree and pattern of cadmium inhibition of naphthalene biodegradation. Chemosphere 59, 919-927.

Hong, S., Soyol-Erdene, T.O., Hwang, H.J., Hong, S.B., Hur, S.D. and Motoyama, H. (2012). Evidence of global-scale As, Mo, Sb, and Tl atmospheric pollution in the Antarctic Snow. Environmental Science and Technolnolgy, 46, 11550-11557.

IAATO (2017) Tourism Statistics. Available at:. https://iaato.org/en_GB/tourism- statistics.

Ibrahim, S., Zahri, K.N.M., Convey, P., Khalil, K.A., Gomez-Fuentez, C., Zulkarnain, A., Alias, S.A., Gonzalez-Rocha, G. and Ahmad, S.A. (2019). Optimisation of biodegradation conditions for waste canola oil by cold-adapted Rhodococcus sp. AQ5-07 from Antarctica. Electronic Journal of Biotechnology (Under Review).

Ibrahim, S., Muhammad, A., Tanko, A.S., Abubakar, A., Ibrahim, H., Shukor, M.Y. and Ahmad, S.A. (2016). Studies of action of heavy metals on caffeine degradation by immobilised Leifsonia sp. strain SIU. Bayero Journal of Pure and Applied Sciences 8, 138-144.

Ibrahim, S., Shukor, M.Y.A., Yazid N.A. and Ahmad S.A. (2018) Microbial degradation of vegetable oils: A review. Malaysian Journal of Biochemistry and Molecular Biology 28, 45-55.

Interiano-López, M., Ramírez-Coutiño, V., Godinez-Tovar, L., Zamudio-Pérez, E. and Rodríguez-Valadez, F. (2019). Bioremediation methods assisted with humic acid for the treatment of oil-contaminated drill cuttings. Revista Mexicana De Ingeniería Química 18, 929-937.

Karamba, K.I., Ahmad, S.A., Zulkharnain, A., Syed, M.A., Khalil, K.A., Shamaan, N.A., Dahalan, F.A. and Shukor, M.Y. (2016). Optimisation of biodegradation conditions for cyanide removal by Serratia marcescens strain AQ07 using one-factor-at-a-time technique and response surface methodology. Rendiconti Lincei 27, 533-545.

Kumar, S., Mathur, A., Singh, V., Nandy, S., Khare, S.K. and Negi, S. (2012). Bioremediation of waste cooking oil using a novel lipase produced by Penicillium chrysogenum SNP5 grown in solid medium containing waste grease. Bioresource Technology 120, 300-304.

Kwapisz, E., Wszelaka, J., Marchut, O. and Bielecki, S. (2008). The effect of nitrate and ammonium ions on kinetics of diesel oil degradation by Gordonia alkanivorans S7. International Biodeterioration and Biodegradation 61, 214-222.

Lee, G.L.Y., Ahmad, S.A., Yasid, N.A., Zulkharnain, A., Convey, P., Johari, W.L.W., Alias, S.A., Gonzalez-Rocha, G. and Shukor, M.Y. (2018). Biodegradation of phenol by cold-adapted bacteria from Antarctic soils. Polar Biology 3, 553-562.

Matsumiya, Y., Wakita, D., Kimura, A., Sanpa, S. and Kubo, M. (2007). Isolation and characterization of a lipid-degrading bacterium and its application to lipid-containing wastewater treatment. Journal of Bioscience and Bioengineering 103, 325-330.

Nagarajan, J., Nawawi, N.M. and Ibrahim, A.L. (2014). Rhodococcus UKMP-5M, an endogenous lipase producing actinomycete from Peninsular Malaysia. Biologia 69, 123-132.

Nawaz, M.S., Billedeau, S.M. and Cerniglia, C.E. (1998) Influence of selected physical parameters on the biodegradation of acrylamide by immobilized cells of Rhodococcus sp. Biodegradation 9, 381-387.
Nies, D.H. (1999) Microbial heavy-metal resistance. Applied Microbiology and Biotechnology 51, 730-750.

Pereira, M.G., Mudge, S.M. and Latchford, J. (2003) Vegetable oil spills on salt marsh sediments; comparison between sun- flower and linseed oils. Marine Environmental Research 56, 367-385.

Phong, N.T., Duyan, N.T. and Diep, C.N. (2014) Isolation and characterization of lipid-degrading bacteria in wastewater of food processing plants and restaurants in Can Tho City, Vietnam. American Journal of Life Sciences 2, 382-388.

Rack, U. (2015). Polar expeditions. In: Exploring the Last Continent, (Liggett, D., Storey, B., Cook, Y. and Meduna, V. eds), Cham: Springer.

Rajasekar, A., Babu, T.G., Pandian, S.T., Maruthamuthu, S., Palaniswamy, N. and Rajendran, A. (2007). Role of Serratia marcescens ACE2 on diesel degradation and its influence on corrosion. Indian Journal of Microbiology and Biotechnology 34, 589-598.

Rajendran, P., Muthukrishnan, J. and Gunasekaran, P. (2003). Microbes in heavy metal remediation. Indian Journal Experimental Biology 41, 935-944.

Robinson, J.B. and Tuovinen, O.H. (1984). Mechanisms of microbial resistance and detoxification of mercury and organomercury compounds: physiological, biochemical, and genetic analyses. Microbiological Reviews 48, 95-124.

Ross, D.A. (2004). The toxicology of mercury. New England Journal of Medicine 350, 945-947.

Ruiz-Marín, A., Zavala-Loria, J.C., Canedo-López, Y. and Cordova-Quiroz, A.V (2013). Tropical bacteria isolated from oil-contaminated mangrove soil: bioremediation by natural attenuation and bioaugmentation. Revista Mexicana de Ingeniería Química 12, 553-560.

Sadler, W.R. and Trudinger, P.A. (1967). The inhibition of microorganisms by heavy metals. Mineralium Deposita 2, 158-168.

Sandrin, T.R. and Maier, R.M. (2003) Impact of metals on the biodegradation of organic pollutants. Environmental Health Perspectives 111, 1093-1101.

Serikovna, S.Z., Serikovich, K.S., Sakenovna, A.S., Murzakhmetovich, S.S. and Khamitovich, A.K. (2013). Screening of lipid degrading microorganisms for wastewater treatment. Malaysian Journal of Microbiology 9, 219-226.

Sharma, B., Singh S. and Siddiqi N.J. (2014). Biomedical implications of heavy metals induced imbalances in redox systems. Biomed Research Intnational 2014, doi:10.1155/2014/640754.

Shon, H.K., Tian, D., Kwon, D.Y., Jin, C.S., Lee, T.J. and Chung, W.J. (2002). Degradation of fat, oil, and grease (FOGs) by lipase-producing bacterium Pseudomonas sp. strain D2D3. Journal of Microbiology and Biotechnology 12, 583-591.

Shukor, M.Y., Gusmanizar, N., Ramli, J., Shamaan, N.A., MacCormack, W.P. and Syed, M.A. (2009a). Isolation and characterization of an acrylamide-degrading Antarctic bacterium. Journal of Environmental Biology 30, 107–112.

Shukor, M.Y., Dahalan, F.A., Jusoh, A.Z., Muse, R., Shamaan, N.A. and Syed, M.A. (2009b). Characterization of diesel-degrading strain isolated from hydrocarbon-contaminated site. Journal of Environmental Biology 30, 145–150.

Sihag, S. and Pathak, H. (2016). Biodegradation of 2T engine oil using soil microbe and gravimetric analysis. International Journal of Scientific Engineering Research 7, 1286-1295.

Soyol-Erdene, T.O., Huh, Y., Hong, S. and Hur, S.D. (2011). A 50-year record of platinum, iridium, and rhodium in Antarctic Snow: volcanic and anthropogenic sources. Environmental Science and Technology 45, 5929-5935.

Stebbing, A.R.D (2002). Tolerance and hormesis - increased resistance to copper in hydroids linked to hormesis. Marine Environmental Research 54, 805-809.

Suárez-García, L., Cuervo-López, F., & Texier, A.-C. (2019). Biological removal of mixtures of ammonium, phenol, cresol isomers, and sulfide in a sequencing batch reactor. Revista Mexicana De Ingeniería Química 18, 1189-1202.

Subramaniam, K.,, Mazuki, T.A.T.,, Shukor, M.Y., and Ahmad, S.A. (2019). Isolation and optimisation of phenol degradation by Antarctic isolate using one factor at time. Malaysian Journal of Biochemistry and Molecular Biology 22, 79-86.

Tiwari, A.K. (2017). Environmental monitoring around Indian Antarctic Stations. Proceedings of Indian National Science Academy 83, 399-413.

Vodopivez, C., Curtosi, A., Villaamil, E., Smichowski, P., Pelletier, E. and Mac Cormack, W.P. (2015) Heavy metals in sediments and soft tissues of the Antarctic clam Laternula elliptica: More evidence as a? Possible biomonitor of coastal marine pollution at high latitudes?. Science of Total Environment 502, 375-384.

Williams, L., Borchhardt, N., Colesie, C., Baum, C., Komsic-Buchmann, K., Rippin, M., Becker, B., Karsten, U. and Büdel, B. (2017) Biological soil crusts of Arctic Svalbard and of Livingston Island, Antarctica. Polar Biology 40, 399-411.

Wang, Y., Tian, Y., Han, B., Zhao, H., Bi, J. and Cai, B. (2007). Biodegradation of phenol by free and immobilized Acinetobacter sp. strain PD12. Journal of Environmental Sciences 19, 222-225.

Xie, Z. and Sun, L. (2008). A 1,800-year record of arsenic concentration in the penguin dropping sediment, Antarctic. Environmental Geology 55, 1055-1059.

Yusuf, I., Ahmad, S.A., Phang, L.Y., Yasid, N.A. and Shukor, M.Y. (2019). Effective production of keratinase by gellan gum-immobilised Alcaligenes sp. AQ05-001 using heavy metal-free and polluted feather wastes as substrates. 3 Biotech 9, 32. Doi:org/10.1007/s13205-018-1555-x.

Zakaria, N.N., Ahmad, S.A., Yasid, N.A., Yin, G.L.L., Manogaran, M., Subramaniam, K., Mazuki, T.T.A., Nawawi, N.M. and Shukor, M.Y. (2018). Biodegradation of phenol by Antarctic bacterium Rhodococcus baikonurensis strain AQ5-001 in the presence of heavy metals. Malaysian Journal Biochemistry and Molecular Biology 21, 29-36.
How to Cite
Ibrahim, S., Zulkharnain, A., Zahri, K., Lee, G., Convey, P., Gomez-Fuentes, C., Sabri, S., Khalil, K., Alias, S., Gonzalez-Rocha, G., & Ahmad, S. (2019). Effect of heavy metals and other xenobiotics on biodegradation of waste canola oil by cold-adapted Rhodococcus sp. strain AQ5-07. Revista Mexicana De Ingeniería Química, 19(3), 1041-1052. https://doi.org/10.24275/rmiq/Bio917