Removal of heterocyclic compound carbazole using cell immobilization of Thalassospira profundimaris strain M02

  • I.M. Maliki
  • N.H. Abdul-Manas
  • S.A. Ahmad
  • H. Fuse
  • N. Ramírez-Moreno
  • A. Zulkharnain
Keywords: Bioremediation, Calcium alginate, Carbazole, Cell immobilization, Gellan gum


Cell immobilization offers promising potential to maximize microbial biodegradation activity and overcome limitations involved in bioremediation. Thalassospira profundimaris strain M02 was used to determine the effectiveness of cell immobilization for carbazole biodegradation. Effects of different matrices, effective diffusivity, mechanical strength, matrix concentration, cell mass load and reusability were investigated in this study. Results revealed that calcium alginate (Ca-Al) was better compared to gellan gum as higher carbazole biodegradation rate was observed. Diffusion analysis and mechanical strength analyses also revealed that Ca-Al possessed superior characteristics as immobilization matrix for carbazole biodegradation compared to gellan gum. Ca-Al works best at 4% (w/v) with 1.25 g of cell mass loading. In addition, immobilized strain M02 retained carbazole biodegradation activity after 6 cycles of usage.


Abarian, M., Hassanshahian, M. and Esbah, A. (2019). Degradation of phenol at high concentrations using immobilization of Pseudomonas putida P53 into sawdust entrapped in sodium-alginate beads. Water Science and Technology 79(7), 1387-1396.

Abdulrasheed, M., Zakaria, N.N., Ahmad Roslee, A.F., Shukor, M.Y., Zulkharnain, A., Napis, S., Alias, S.A., Gonzalez-Rocha, G. and Ahmad S.A. (2020). Biodegradation of diesel oil by cold-adapted bacterial strains of Arthrobacter spp. from Antarctica. Antarctic Science 32, 1-13.

Ahmad, S.A., Shamaan, N.A., Syed, M.A., Dahalan, F.A., Khalil, K.A., 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.

Azri, M.F.D.B., Zulkharnain, A.B., Husaini, A.A.S.A. and Ahmad, S.A.B. (2015). The degradation of carbazole and the production of ligninolytic enzyme by isolated marine fungi. Journal of Chemical and Pharmaceutical Sciences 8, 330-335.

Cisneros-de la Cueva, S. Mart´ınez-Prado, M.A., López-Miranda, J., Rojas-Contreras, J.A., and Medrano-Roldan, H. (2016). Aerobic degradation of diesel by Aspergillus terreus KP862582. Revista Mexicana de Ingeniería Química 15, 347-360.

Darham, S., Gomez-Fuentes, C., Zulkharnain, A., Sabri, S., Calisto-Ulloa, N., Ramírez-Moreno, N. and Ahmad, S.A. (2019). Isolation and identification of molybdenum-reducing cold-adapted marine bacteria isolated from Bernardo O’higgins Riquelme base station, Antarctica. Malaysian Journal of Biochemistry and Molecular Biology 22, 8-15.

Fang, L., Xu, Y., Xu, L., Shi, T., Ma, X., Wu, X. and Hua, R. (2020). Enhanced biodegradation of organophosphorus insecticides in industrial wastewater via immobilized Cupriavidus nantongensis X1T. Science of The Total Environment 755, doi: 10.1016/j.scitotenv.2020.142505.

Ferreira, L., Rosales, E., Sanromán, M.A. and Pazos, M. (2015). Preliminary testing and design of permeable bioreactive barrier for phenanthrene degradation by Pseudomonas stutzeri CECT 930 immobilized in hydrogel matrices. Journal of Chemical Technology and Biotechnology 90, 500-506.

Ibrahim, S., Zulkharnain, A., Zahri, K.N.M., Lee, G.L.Y., Convey, P., Gomez-Fuentes, C., Sabri, S., Abdul Khalil, K., Alias, S.A., Gonzalez-Rocha, G. and Ahmad, S.A. (2020). 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 19,1041-1052.

Jorfi, S., Ghafari, S., Ramavandi, B., Soltani, R.D.C. and Ahmadi, M. (2019). Biodegradation of high saline petrochemical wastewater by novel isolated halotolerant bacterial strains using integrated powder activated carbon/activated sludge bioreactor. Environmental Progress and Sustainable Energy 38, doi:10.1002/ep.13088.

Karamba, K.I., Ahmad, S.A., Zulkharnain, A., Yasid, N.A., Khalid, A. and Shukor, M.Y. (2017). Biodegradation of cyanide and evaluation of kinetic models by immobilized cells of Serratia marcescens strain AQ07. International Journal of Environmental Science and Technology 14, 1945-1958.

Karamba, K.I., Sabullah, M.K., Zulkharnain, A., Gomez-Fuentes, C. and Ahmad, S.A. (2020). Enzymatic cyanide detoxification by partially purified cyanide dihydratase obtained from Serratia marcescens strain AQ07. Revista Mexicana de Ingeniería Química 19, 493-506.

Lee, G.L.Y., Ahmad, S.A., Yasid, N.A., Zulkharnain, A., Convey, P., Wan Johari, W.L., Alias, S.A., Gonzalez-Rocha, G. and Shukor, M.Y. (2018). Biodegradation of phenol by cold-adapted bacteria from Antarctic soils. Polar Biology 41, 553-562.

Louvado, A., Gomes, N.C.M., Simões, M.M.Q., Almeida, A., Cleary, D. F. R. and Cunha, A. (2015). Polycyclic aromatic hydrocarbons in deep sea sediments: microbe–pollutant interactions in a remote environment. Science of the Total Environment 526, 312-328.

Huang, R.Y., Tian, W.J., Liu, Q., Yu, H.B., Jin, X., Zhao, Y.G. and Feng, G. (2016). Enhanced biodegradation of pyrene and indeno (1, 2, 3-cd) pyrene using bacteria immobilized in cinder beads in estuarine wetlands. Marine pollution bulletin 102, 128-133.

Hui, J.L.C., Baini, R., Manas, N.H.A., and Zulkharnain, A. (2020). Optimization of immobilization media of Thalassospira profundimaris: diffusion and strength applications. International Journal of Recent Technology and Engineering 8, 311-316.

Jin, X., Tian, W., Liu, Q., Qiao, K., Zhao, J., and Gong, X. (2017). Biodegradation of the benzo [a] pyrene-contaminated sediment of the Jiaozhou Bay wetland using Pseudomonas sp. immobilization. Marine Pollution Bulletin 117, 283-290.

Maniyam, M.N., Ibrahim, A.L. and Cass, A.E. (2019). Enhanced cyanide biodegradation by immobilized crude extract of Rhodococcus UKMP-5M. Environmental Technology 40, 386-398.

Martínez-Prado, M. and Soto-Álvarez, C. (2019). Removal of petroleum hydrocarbons from a low permeability soil: bioremediation and electroremediation. Revista Mexicana de Ingeniería Química 16, 955-970.

Mendoza-Madrigal, A.G., Dura ́n-Pa ́ramo, E., Valencia del Toro, G., Chanona-Pe ́rez, J.J., Martínez-Ramírez, O.C. and Arzate-Va ́zquez, I. (2017). Viability kinetics of free and immobilized Bifidobacterium bifidum in presence of food samples under gastrointestinal in vitro. Revista Mexicana de Ingeniería Química 16, 159-168.

Mikolajczyk, S., Warenik-Bany, M., Maszewski, S., and Pajurek, M. (2020). Dioxins and PCBs – environment impact on freshwater fish contamination and risk to consumers. Environmental Pollution 263, 114611.

Roslee, A.F.A., Zakaria, N.N., Convey, P., Zulkharnain, A., Lee, G.L.Y., Gomez-Fuentes, C. and Ahmad, S.A. (2020). Statistical optimisation of growth conditions and diesel degradation by the Antarctic bacterium, Rhodococcus sp. strain AQ5‒07. Extremophiles 24, 277-291.

Rajendran, R., Prabhavathi, P., Karthiksundaram, S., Pattabi, S., Kumar, S. D. and Santhanam, P. (2015). Biodecolorization and bioremediation of denim industrial wastewater by adapted bacterial consortium immobilized on inert polyurethane foam (PUF) matrix: a first approach with biobarrier model. Polish Journal of Microbiology 64, 329-338.

Salam, L.B., Ilori, M.O. and Amund, O.O. (2015). Carbazole degradation in the soil microcosm by tropical bacterial strains. Brazilian Journal of Microbiology 46, 1037-1044.

Upendar, G., Dutta, S., Bhattacharya, P. and Dutta, A. (2017). Bioremediation of methylene blue dye using Bacillus subtilis MTCC 441. Water Science and Technology 75, 1572-1583.

Vikrant, K., Giri, B.S., Raza, N., Roy, K., Kim, K.H., Rai, B.N. and Singh, R. S. (2018). Recent advancements in bioremediation of dye: current status and challenges. Bioresource Technology 253, 355-367.

Wang, B., Xu, X., Yao, X., Tang, H. and Ji, F. (2019). Degradation of phenanthrene and fluoranthene in a slurry bioreactor using free and ca-alginate-immobilized Sphingomonas pseudosanguinis and Pseudomonas stutzeri bacteria. Journal of Environmental Management 249, doi: 10.1016/j.jenvman.2019.109388.

Xu, X., Zhou, H., Chen, X., Wang, B., Jin, Z. and Ji, F. (2019). Biodegradation potential of polycyclic aromatic hydrocarbons by immobilized Klebsiella sp. in soil washing effluent. Chemosphere 223, 140-147.

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, doi: 10.1007/s13205-018-1555-x.

Zakaria, N.N., Roslee, A.F.A., Gomez-Fuentes, C., Zulkharnain, A., Abdulrasheed, M., Sabri, S., Ramírez-Moreno, N., Calisto-Ulloa, N. and Ahmad, S.A. (2020) Kinetic studies of marine psychrotolerant microorganisms capable of degrading diesel in the presence of heavy metals. Revista Mexicana de Ingeniería Química 19, 1375-1388.

How to Cite
Maliki, I., Abdul-Manas, N., Ahmad, S., Fuse, H., Ramírez-Moreno, N., & Zulkharnain, A. (2020). Removal of heterocyclic compound carbazole using cell immobilization of Thalassospira profundimaris strain M02. Revista Mexicana De Ingeniería Química, 20(1), 413-422.

Most read articles by the same author(s)