Skip to main content
Log in

Hexavalent Chromium Removal by Candida sp. in a Concentric Draft-Tube Airlift Bioreactor

  • Published:
Water, Air, and Soil Pollution Aims and scope Submit manuscript

Abstract

The main purpose of this work was to conduct a kinetic study on cell growth and hexavalent chromium [Cr(VI)] removal by Candida sp. FGSFEP in a concentric draft-tube airlift bioreactor. The yeast was batch-cultivated in a 5.2-l airlift bioreactor containing culture medium with an initial Cr(VI) concentration of 1.5 mM. The maximum specific growth rate of Candida sp. FGSFEP in the airlift bioreactor was 0.0244 h−1, which was 71.83% higher than that obtained in flasks. The yeast strain was capable of reducing 1.5 mM Cr(VI) completely and exhibited a high volumetric rate [1.64 mg Cr(VI) l−1 h−1], specific rate [0.95 mg Cr(VI) g−1 biomass h−1] and capacity [44.38 mg Cr(VI) g−1 biomass] of Cr(VI) reduction in the airlift bioreactor, with values higher than those obtained in flasks. Therefore, culture of Candida sp. FGSFEP in a concentric draft-tube airlift bioreactor could be a promising technological alternative for the aerobic treatment of Cr(VI)-contaminated industrial effluents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acevedo-Aguilar, F. J., Espino-Saldaña, A. E., León-Rodríguez, I. L., Rivera-Cano, M. E., Ávila-Rodríguez, M., et al. (2006). Hexavalent chromium removal in vitro and from industrial wastes, using chromate-resistant strains of filamentous fungi indigenous to contaminated wastes. Canadian Journal of Microbiology, 52, 809–815. doi:10.1139/W06-037.

    Article  CAS  Google Scholar 

  • Arica, M. Y., & Bayramoğlu, G. (2005). Cr(VI) biosorption from aqueous solutions using free and immobilized biomass of Lentinus sajor-caju: Preparation and kinetic characterization. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 253, 203–211. doi:10.1016/j.colsurfa.2004.11.012.

    Article  CAS  Google Scholar 

  • Arslan, G., & Pehlivan, E. (2007). Batch removal of chromium(VI) from aqueous solution by Turkish brown coals. Bioresource Technology, 98, 2836–2845. doi:10.1016/j.biortech.2006.09.041.

    Article  CAS  Google Scholar 

  • Atkinson, B., & Mavituna, F. (1983). Biochemical engineering and biotechnology handbook. London: Nature Press.

    Google Scholar 

  • Bae, W. C., Kang, T. G., Kang, I. K., Won, Y. J., & Jeong, B. C. (2000). Reduction of hexavalent chromium by Escherichia coli ATCC 33456 in batch and continuous cultures. Journal of Microbiology (Seoul, Korea), 38, 36–39.

    CAS  Google Scholar 

  • Branco, R., Alpoim, M. C., & Morais, P. V. (2004). Ochrobactrum tritici strain 5bvI1—characterization of a Cr(VI)-resistant and Cr(VI)-reducing strain. Canadian Journal of Microbiology, 50, 697–703. doi:10.1139/w04-048.

    Article  CAS  Google Scholar 

  • Cheung, K. H., & Gu, J. D. (2003). Reduction of chromate (CrO4 2−) by an enrichment consortium and an isolate of marine sulfate-reducing bacteria. Chemosphere, 52, 1523–1529. doi:10.1016/S0045-6535(03)00491-0.

    Article  CAS  Google Scholar 

  • Cheung, K. H., & Gu, J. D. (2007). Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: A review. International Biodeterioration & Biodegradation, 59, 8–15. doi:10.1016/j.ibiod.2006.05.002.

    Article  CAS  Google Scholar 

  • Chisti, M. Y. (1989). Airlift bioreactors. London: Elsevier Applied Science.

    Google Scholar 

  • Chisti, Y. (1998). Pneumatically agitated bioreactors in industrial and environmental bioprocessing: Hydrodynamics, hydraulics, and transport phenomena. Applied Mechanics Reviews, 51, 33–112.

    Article  Google Scholar 

  • Clesceri, L. S., Greenberg, A. E., & Eaton, A. D. (1998). Standard methods for the examination of water and wastewater (20th ed.). Washington: American Public Health Association.

    Google Scholar 

  • DeLeo, P. C., & Ehrlich, H. L. (1994). Reduction of hexavalent chromium by Pseudomonas fluorescens LB300 in batch and continuous cultures. Applied Microbiology and Biotechnology, 40, 756–759. doi:10.1007/BF00173341.

    Article  CAS  Google Scholar 

  • Francisco, R., Alpoim, M. C., & Morais, P. V. (2002). Diversity of chromium-resistant and -reducing bacteria in a chromium-contaminated activated sludge. Journal of Applied Microbiology, 92, 837–843. doi:10.1046/j.1365-2672.2002.01591.x.

    Article  CAS  Google Scholar 

  • Ganguli, A., & Tripathi, A. K. (2002). Bioremediation of toxic chromium from electroplating effluent by chromate-reducing Pseudomonas aeruginosa A2Chr in two bioreactors. Applied Microbiology and Biotechnology, 58, 416–420. doi:10.1007/s00253-001-0871-x.

    Article  CAS  Google Scholar 

  • Gouda, M. K. (2000). Studies on chromate reduction by three Aspergillus species. Fresenius Environmental Bulletin, 9, 799–808.

    CAS  Google Scholar 

  • Guillén-Jiménez, F. M., Morales-Barrera, L., Morales-Jiménez, J., Hernández-Rodríguez, C. H., & Cristiani-Urbina, E. (2008). Modulation of tolerance to Cr(VI) and Cr(VI) reduction by sulfate ion in a Candida yeast strain isolated from tannery wastewater. Journal of Industrial Microbiology & Biotechnology, 35, 1277–1287. doi:10.1007/s10295-008-0425-7.

    Article  CAS  Google Scholar 

  • Hach Company (2008). Hach water analysis handbook. Loveland: Hach Company.

    Google Scholar 

  • Han, X., Wong, Y. S., Wong, M. H., & Tam, N. F. Y. (2007). Biosorption and bioreduction of Cr(VI) by a microalgal isolate, Chlorella miniata. Journal of Hazardous Materials, 146, 65–72. doi:10.1016/j.jhazmat.2006.11.053.

    Article  CAS  Google Scholar 

  • Ishibashi, Y., Cervantes, C., & Silver, S. (1990). Chromium reduction in Pseudomonas putida. Applied and Environmental Microbiology, 56, 2268–2270.

    CAS  Google Scholar 

  • Jianlong, W., Zeyu, M., & Xuan, Z. (2004). Response of Saccharomyces cerevisiae to chromium stress. Process Biochemistry, 39, 1231–1235. doi:10.1016/S0032-9592(03)00255-3.

    Article  CAS  Google Scholar 

  • Juvera-Espinosa, J., Morales-Barrera, L., & Cristiani-Urbina, E. (2006). Isolation and characterization of a yeast strain capable of removing Cr(VI). Enzyme and Microbial Technology, 40, 114–121. doi:10.1016/j.enzmictec.2005.10.045.

    Article  CAS  Google Scholar 

  • Konovalova, V. V., Dmytrenko, G. M., Nigmatullin, R. R., Bryk, M. T., & Gvozdyak, P. I. (2003). Chromium(VI) reduction in a membrane bioreactor with immobilized Pseudomonas cells. Enzyme and Microbial Technology, 33, 899–907. doi:10.1016/S0141-0229(03)00204-7.

    Article  CAS  Google Scholar 

  • Liu, Y. G., Xu, W. H., Zeng, G. M., Li, X., & Gao, H. (2006). Cr(VI) reduction by Bacillus sp. isolated from chromium landfill. Process Biochemistry, 41, 1981–1986. doi:10.1016/j.procbio.2006.04.020.

    Article  CAS  Google Scholar 

  • Lloyd, J. R. (2003). Microbial reduction of metals and radionuclides. FEMS Microbiology Reviews, 27, 411–425. doi:10.1016/S0168-6445(03)00044-5.

    Article  CAS  Google Scholar 

  • Lovley, D. R., & Phillips, E. J. P. (1994). Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Applied and Environmental Microbiology, 60, 726–728.

    CAS  Google Scholar 

  • McGrath, S. P., & Smith, S. (1990). Chromium and nickel. In B. J. Alloway (Ed.), Heavy metals in soils (pp. 125–150). New York: Wiley.

    Google Scholar 

  • Mergeay, M. (1995). Heavy metal resistances in microbial ecosystems. In A. D. L. Akkermans, J. D. van Elsas, & F. J. De Bruijn (Eds.), Molecular microbial ecology manual (pp. 1–17). Dordrecht: Kluwer Academic.

    Google Scholar 

  • Middleton, S. S., Latmani, R. B., Mackey, M. R., Ellisman, M. H., Tebo, B. M., & Criddle, C. S. (2003). Cometabolism of Cr(VI) by Shewanella oneidensis MR-1 produces cell-associated reduced chromium and inhibits growth. Biotechnology and Bioengineering, 83, 627–637. doi:10.1002/bit.10725.

    Article  CAS  Google Scholar 

  • Morales-Barrera, L., & Cristiani-Urbina, E. (2006). Removal of hexavalent chromium by Trichoderma viride in an airlift bioreactor. Enzyme and Microbial Technology, 40, 107–113. doi:10.1016/j.enzmictec.2005.10.044.

    Article  CAS  Google Scholar 

  • Morales-Barrera, L., & Cristiani-Urbina, E. (2008). Hexavalent chromium removal by a Trichoderma inhamatum fungal strain isolated from tannery effluent. Water, Air, and Soil Pollution, 187, 327–336. doi:10.1007/s11270-007-9520-z.

    Article  CAS  Google Scholar 

  • Morales-Barrera, L., Guillén-Jiménez, F. M., Ortiz-Moreno, A., Villegas-Garrido, T. L., Sandoval-Cabrera, A., Hernández-Rodríguez, C. H., et al. (2008). Isolation, identification and characterization of a Hypocrea tawa strain with high Cr(VI) reduction potential. Biochemical Engineering Journal, 40, 284–292. doi:10.1016/j.bej.2007.12.014.

    Article  CAS  Google Scholar 

  • Muter, O., Patmalnieks, A., & Rapoport, A. (2001). Interrelations of the yeast Candida utilis and Cr(VI): Metal reduction and its distribution in the cell and medium. Process Biochemistry, 36, 963–970. doi:10.1016/S0032-9592(01)00136-4.

    Article  CAS  Google Scholar 

  • Pal, N. (1997). Reduction of hexavalent chromium to trivalent chromium by Phanerochaete chrysosporium. In B. C. Alleman, & A. Leeson (Eds.), In situ and on-site bioremediation, vol. 2 (pp. 511–517). Ohio: Batelle.

    Google Scholar 

  • Park, D., Yun, Y. S., Cho, H. Y., & Park, J. M. (2004). Chromium biosorption by thermally treated biomass of the brown seaweed, Ecklonia sp. Industrial & Engineering Chemistry Research, 43, 8226–8232. doi:10.1021/ie049323k.

    Article  CAS  Google Scholar 

  • Park, D., Yun, Y. S., Jo, J. H., & Park, J. M. (2005). Mechanism of hexavalent chromium removal by dead fungal biomass of Aspergillus niger. Water Research, 39, 533–540. doi:10.1016/j.watres.2004.11.002.

    Article  CAS  Google Scholar 

  • Pattanapipitpaisal, P., Brown, N. L., & Macaskie, L. E. (2001a). Chromate reduction and 16S rRNA identification of bacteria isolated from Cr(VI)-contaminated site. Applied Microbiology and Biotechnology, 57, 257–261. doi:10.1007/s002530100758.

    Article  CAS  Google Scholar 

  • Pattanapipitpaisal, P., Brown, N. L., & Macaskie, L. E. (2001b). Chromate reduction by Microbacterium liquefaciens immobilised in polyvinyl alcohol. Biotechnology Letters, 23, 61–65. doi:10.1023/A:1026750810580.

    Article  CAS  Google Scholar 

  • Pazouki, M., Keyanpour-Rad, M., Shafie, S., & Shahhoseini, S. (2007). Efficiency of Penicillium chrysogenum PTCC 5037 in reducing low concentration of chromium hexavalent in a chromium electroplating plant wastewater. Bioresource Technology, 98, 2116–2122. doi:10.1016/j.biortech.2006.08.005.

    Article  CAS  Google Scholar 

  • QuiIntana, M., Curutchet, G., & Donati, E. (2001). Factors affecting chromium(VI) reduction by Thiobacillus ferrooxidans. Biochemical Engineering Journal, 9, 11–15. doi:10.1016/S1369-703X(01)00116-4.

    Article  CAS  Google Scholar 

  • Ramírez-Ramírez, R., Calvo-Méndez, C., Ávila-Rodríguez, M., Lappe, P., Ulloa, M., Vázquez-Juárez, R., & Gutiérrez-Corona, J. F. (2004). Cr(VI) reduction in a chromate-resistant strain of Candida maltosa isolated from the leather industry. Antonie Van Leeuwenhoek, 85, 63–68. doi:10.1023/B:ANTO.0000020151.22858.7f.

    Article  Google Scholar 

  • Şahin, Y., & Öztürk, A. (2005). Biosorption of Cr(VI) ions from aqueous solution by the bacterium Bacillus thuringiensis. Process Biochemistry, 40, 1895–1901. doi:10.1016/j.procbio.2004.07.002.

    Article  CAS  Google Scholar 

  • Shen, H., & Wang, Y. T. (1994). Biological reduction of chromium by E. coli. Journal of Environmental Engineering, 120, 560–572. doi:10.1061/(ASCE)0733-9372(1994)120:3(560).

    Article  CAS  Google Scholar 

  • Shen, H., & Wang, Y. T. (1995). Simultaneous chromium reduction and phenol degradation in a coculture of Escherichia coli ATCC 33456 and Pseudomonas putida DMP-1. Applied and Environmental Microbiology, 61, 2754–2758.

    CAS  Google Scholar 

  • Smith, W. A., Apel, W. A., Petersen, J. N., & Peyton, B. M. (2002). Effect of carbon and energy source on bacterial chromate reduction. Bioremediation Journal, 6, 205–215. doi:10.1080/10889860290777567.

    Article  CAS  Google Scholar 

  • Snape, J. B., & Thomas, N. H. (1992). Modeling particle transport by bubbles for performance guidelines in airlift bioreactors. Biotechnology and Bioengineering, 40, 337–345. doi:10.1002/bit.260400302.

    Article  CAS  Google Scholar 

  • Stanin, F. T. (2005). The transport and fate of chromium(VI) in the environment. In J. Guertin, J. A. Jacobs, & C. P. Avakian (Eds.), Chromium(VI) handbook (pp. 165–214). Boca Raton: CRC Press.

    Google Scholar 

  • Stasinakis, A. S., Thomaidis, N. S., Mamais, D., & Lekkas, T. D. (2004). Investigation of Cr(VI) reduction in continuous-flow activated sludge systems. Chemosphere, 57, 1069–1077. doi:10.1016/j.chemosphere.2004.08.020.

    Article  CAS  Google Scholar 

  • Stearns, D. M., Belbruno, J. J., & Wetterhahn, K. E. A. (1995). A prediction of chromium(III) accumulation in humans from chromium dietary supplements. The FASEB Journal, 9, 1650–1657.

    CAS  Google Scholar 

  • Sumathi, K. M. S., Mahimairaja, S., & Naidu, R. (2005). Use of low-cost biological wastes and vermiculite for removal of chromium from tannery effluent. Bioresource Technology, 96, 309–316. doi:10.1016/j.biortech.2004.04.015.

    Article  CAS  Google Scholar 

  • Thacker, U., Parikh, R., Shouche, Y., & Madamwar, D. (2007). Reduction of chromate by cell-free extract of Brucella sp. isolated from Cr(VI) contaminated sites. Bioresource Technology, 98, 1541–1547. doi:10.1016/j.biortech.2006.06.011.

    Article  CAS  Google Scholar 

  • Viamajala, S., Peyton, B. M., Sani, R. K., Apel, W. A., & Petersen, J. N. (2004). Toxic effects of chromium(VI) on anaerobic and aerobic growth of Shewanella oneidensis MR-1. Biotechnology Progress, 20, 87–95. doi:10.1021/bp034131q.

    Article  CAS  Google Scholar 

  • Viamajala, S., Smith, W. A., Sani, R. K., Apel, W. A., Petersen, J. N., Neal, A. L., et al. (2007). Isolation and characterization of Cr(VI) reducing Cellulomonas spp. from subsurface soils: Implications for long-term chromate reduction. Bioresource Technology, 98, 612–622. doi:10.1016/j.biortech.2006.02.023.

    Article  CAS  Google Scholar 

  • Wang, Y. T. (2000). Microbial reduction of chromate. In D. R. Lovley (Ed.), Environmental microbe–metal interactions (pp. 225–235). Washington: American Society for Microbiology Press.

    Google Scholar 

  • Wang, Y. T., & Shen, H. (1997). Modelling Cr(VI) reduction by pure bacterial cultures. Water Research, 31, 727–732. doi:10.1016/S0043-1354(96)00309-0.

    Article  CAS  Google Scholar 

  • Xu, W., Liu, Y., Zeng, G., Li, X., Tang, C., & Yuan, X. (2005). Enhancing effect of iron on chromate reduction by Cellulomonas flavigena. Journal of Hazardous Materials, 126, 17–22. doi:10.1016/j.jhazmat.2005.03.056.

    Article  CAS  Google Scholar 

  • Zakaria, Z. A., Zakaria, Z., Surif, S., & Ahmad, W. A. (2007). Hexavalent chromium reduction by Acinetobacter haemolyticus isolated from heavy-metal contaminated wastewater. Journal of Hazardous Materials, 146, 30–38. doi:10.1016/j.jhazmat.2006.11.052.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

E. C.-U. is a fellow holder of a grant from the Comisión de Operación y Fomento de Actividades Académicas, Instituto Politécnico Nacional, Mexico City, Mexico. The authors gratefully acknowledge the financial support provided by the Secretaría de Investigación y Posgrado, IPN. The CONACyT awarded a graduate scholarship to one of the co-authors (F.M.G.-J.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eliseo Cristiani-Urbina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guillén-Jiménez, F.d.M., Netzahuatl-Muñoz, A.R., Morales-Barrera, L. et al. Hexavalent Chromium Removal by Candida sp. in a Concentric Draft-Tube Airlift Bioreactor. Water Air Soil Pollut 204, 43–51 (2009). https://doi.org/10.1007/s11270-009-0024-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-009-0024-x

Keywords

Navigation