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Bioremoval of Cadmium(II), Nickel(II), and Zinc(II) from Synthetic Wastewater by the Purple Nonsulfur Bacteria, Three Rhodobacter Species

  • Jin Yoo (Indoor Environment Division, Incheon Research Institute of Public Health and Environment) ;
  • Eun-Ji Oh (Water and Land Research Group/Division for Natural Environment, Korea Environment Institute) ;
  • Ji-Su Park (EHS Part, Doosan Corporation Electro-Materials) ;
  • Deok-Won Kim (Department of Earth Resources and Environmental Engineering, Hanyang University) ;
  • Jin-Hyeok Moon (Department of Environmental and Biological Chemistry, Chungbuk National University) ;
  • Deok-Hyun Kim (Chemical Accident Investigation Team, National Institute of Chemical Safety) ;
  • Daniel Obrist (Department of Environmental, Earth, and Atmospheric Sciences, University of Massachusetts Lowell) ;
  • Keun-Yook Chung (Department of Environmental and Biological Chemistry, Chungbuk National University)
  • Received : 2023.07.25
  • Accepted : 2023.10.31
  • Published : 2023.12.10

Abstract

The purpose of this study was to determine the inhibitory effect of heavy metals [Cd(II), Ni(II), and Zn(II)] on the growth of Rhodobacter species (Rhodobacter blasticus, Rhodobacter sphaeroides, and Rhodobacter capsulatus) and their potential use for Cd(II), Ni(II), and Zn(II) bioremoval from liquid media. The presence of toxic heavy metals prolonged the lag phase in growth and reduced biomass growth for all three Rhodobacter species at concentrations of Cd, Ni, and Zn above 10 mg/L. However, all three Rhodobacter species also had a relatively high specific growth rate against each toxic heavy metal stress test for concentrations below 20 mg/L and possessed a potential bioaccumulation ability. The removal efficiency by all strains was highest for Cd(II), followed by Ni(II), and lowest for Zn(II), with the removal efficiency of Cd(II) by Rhodobacter species being 66% or more. Among the three strains, R. blasticus showed a higher removal efficiency of Cd(II) and Ni(II) than R. capsulatus and R. sphaeroides. Results also suggest that the bio-removal processes of toxic heavy metal ions by Rhodobacter species involve both bioaccumulation (intracellular uptake) and biosorption (surface binding).

Keywords

Acknowledgement

This study was conducted with the support of the Research Cooperating Program for the National Research Foundation of Korea (Project No. 2019R1F1A 106325212), NRF, Republic of Korea.

References

  1. N. Green, B. Bjerkeng, K. Hylland, A. Ruus, and B. Rygg, Hazardous substances in the European marine environment: Trends in metals and persistent organic pollutants, European Environment Agency (2003). 
  2. P. B. Tchounwou, C. G. Yedjou, A. K. Patlolla, and D. J. Sutton, Heavy metal toxicity and the environment, Molecular, Clinical and Environmental Toxicology, 133-164, Springer, Berlin, Germany (2012). 
  3. M. Aryal and M. Liakopoulou-Kyriakides, Bioremoval of heavy metals by bacterial biomass, Environ. Monit. Assess., 187, 4173 (2015). 
  4. J. H. Duffus, "Heavy metals" - A meaningless term?, Pure Appl. Chem., 74, 793-807 (2002).  https://doi.org/10.1351/pac200274050793
  5. K. S. Kumar, H. U. Dahms, E. J. Won, J. S. Lee, and K. H. Shin, Microalgae-A promising tool for heavy metal remediation, Ecotoxicol. Environ. Saf., 113, 329-352 (2015).  https://doi.org/10.1016/j.ecoenv.2014.12.019
  6. Ihsanullah, A. Abbas, A. M. Al-Amer, T. Laoui, M. J. Al-Marri, M. S. Nasser, M. Khraisheh, and M. A. Atieh, Heavy metal removal from aqueous solution by advanced carbon nanotubes: Critical review of adsorption applications, Sep. Purif. Technol., 157, 141-161 (2016).  https://doi.org/10.1016/j.seppur.2015.11.039
  7. J. O. Duruibe, M. O. C. Ogwuegbu, and J. N. Egwurugwu, Heavy metal pollution and human biotoxic effects, Int. J. Phys. Sci., 2, 112-118 (2007). 
  8. L. R. Herrera-Estrella, A. A. Guevara-Garcia, and J. Lo'pez-Bucio, Heavy metal adaptation, Encyclopedia of Life Science, 1-5, Macmillan Publishers, London, United Kingdom (1999). 
  9. U. Forstner and G. T. Wittmann, Metal Pollution in the Aquatic Environment, 2nd ed., 7-11, Springer Science & Business Media, Berlin, Germany (2012). 
  10. A. Gaur and A. Adholeya, Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils, Curr. Sci., 86, 528-534 (2004). 
  11. L. Jarup, M. Berglund,, C. G. Elinder, G. Nordberg, and M. Vanter, Health effects of cadmium exposure-A review of the literature and a risk estimate, Scand. J. Work Environ. Health, 24, 1-51 (1998).  https://doi.org/10.5271/sjweh.270
  12. C. E. Borba, R. Guirardello, E. A. Silva, M. T. Veit, and C. R. G. Tavares, Removal of nickel (II) ions from aqueous solution by biosorption in a fixed bed column: Experimental and theoretical breakthrough curves, Biochem. Eng. J., 30, 184-191 (2006).  https://doi.org/10.1016/j.bej.2006.04.001
  13. N. Oyaro, J. Ogendi, E. N. Murago, and E. Gitonga, The contents of Pb, Cu, Zn and Cd in meat in nairobi, Kenya, J. Food Agric. Environ., 5, 119-121 (2007). 
  14. S. S. Ahluwalia and D. Goyal, Microbial and plant derived biomass for removal of heavy metals from wastewater, Bioresour. Technol., 98, 2243-2257 (2007).  https://doi.org/10.1016/j.biortech.2005.12.006
  15. A. M. Y. Chong, Y. S. Wong, and N. F. Y. Tam, Performance of different microalgal species in removing nickel and zinc from industrial wastewater, Chemosphere, 41, 251-257 (2007). 
  16. A. Khosmanesh, F. Lawson, and I. G. Prince, Cadmium uptake by unicellular green microalgae, Chem. Eng. J. Biochem. Eng. J., 62, 81-88 (1996).  https://doi.org/10.1016/0923-0467(95)03060-3
  17. M. Farhadian, C. Vachelard, D. Duchez, and C. Larroche, In situ bioremediation of monoaromatic pollutants in groundwater: A review, Bioresour. Technol., 99, 5296-5308 (2008).  https://doi.org/10.1016/j.biortech.2007.10.025
  18. V. Radhika, S. Subramanian, and K. A. Natarajan, Bioremediation of zinc using Desulfotomaculum nigrificans: Bioprecipitation and characterization studies, Water Res., 40, 3628-3636 (2006).  https://doi.org/10.1016/j.watres.2006.06.013
  19. A. Malik, Metal bioremediation through growing cells, Environ. Int., 30, 261-278 (2004).  https://doi.org/10.1016/j.envint.2003.08.001
  20. G. M. Gadd, Bioremedial potential of microbial mechanisms of metal mobilization and immobilization, Curr. Opin. Biotechnol., 11, 271-279 (2000).  https://doi.org/10.1016/S0958-1669(00)00095-1
  21. H. J. Bai, Z. M. Zhang, G. E. Yang, and B. Z. Li, Bioremediation of cadmium by growing Rhodobacter sphaeroides: Kinetic characteristic and mechanism studies, Bioresour. Technol., 99, 7716-7722 (2008).  https://doi.org/10.1016/j.biortech.2008.01.071
  22. A. Idi, M. H. M. Nor, M. F. A. Wahab, and Z. Ibrahim, Photosynthetic bacteria: An eco-friendly and cheap tool for bioremediation, Rev. Environ. Sci. Biotechnol., 14, 271 (2015). 
  23. P. K. Sarkar and A. K. Banerjee, The effect of nickel on growth, morphology and photopigments of Rhodospirillum photometricum, Folia Microbiol. (Praha), 32, 48-54 (1987).  https://doi.org/10.1007/BF02877258
  24. B. B. Nepple, I. Flynn, and R. Bachofen, Morphological changes in phototrophic bacteria induced by metalloid oxyanions, Microbiol. Res., 154, 191-198 (1999).  https://doi.org/10.1016/S0944-5013(99)80014-7
  25. S. Mohamed Fahmy Gad El-Rab, A. Abdel-Fattah Shoreit, and Y. Fukumori, Effects of cadmium stress on growth, morphology, and protein expression in Rhodobacter capsulatus B10, Biosci. Biotechnol. Biochem., 70, 2394-2402 (2006).  https://doi.org/10.1271/bbb.60122
  26. A. Iyer, K. Mody, and B. Jha, Biosorption of heavy metals by a marine bacterium, Mar. Pollut. Bull., 50, 340-343 (2005). https://doi.org/10.1016/j.marpolbul.2004.11.012
  27. A. Pal and A. K. Paul, Microbial extracellular polymeric substances: central elements in heavy metal bioremediation, Indian J. Microbiol., 48, 49 (2008). 
  28. M. Pandi, V. Shashirekha, and M. Swamy, Bioabsorption of chromium from retan chrome liquor by cyanobacteria, Microbiol. Res., 164, 420-428 (2009).  https://doi.org/10.1016/j.micres.2007.02.009
  29. A. Smiejan, K. J. Wilkinson, and C. Rossier, Cd bioaccumulation by a freshwater bacterium, Rhodospirillum rubrum, Environ. Sci. Technol., 37, 701-706 (2003).  https://doi.org/10.1021/es025901h
  30. M. Watanabe, K. Kawahara, K. Sasaki, and N. Noparatnaraporn, Biosorption of cadmium ions using a photosynthetic bacterium, Rhodobacter sphaeroides S and a marine photosynthetic bacterium, Rhodovulum sp., and their biosorption kinetics, J. Biosci. Bioeng., 95, 374-378 (2003).  https://doi.org/10.1016/S1389-1723(03)80070-1
  31. L. Giotta, A. Agostiano, F. Italiano, F. Milano, and M. Trotta, Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides, Chemosphere, 62, 1490-1499 (2006).  https://doi.org/10.1016/j.chemosphere.2005.06.014
  32. Y. Feng, Y. Yu, Y. Wang, and X. Lin, Biosorption and bioreduction of trivalent aurum by photosynthetic bacteria Rhodobacter capsulatus, Curr. Microbiol., 55, 402-408 (2007).  https://doi.org/10.1007/s00284-007-9007-6
  33. S. Panwichian, D. Kantachote, B. Wittayaweerasak, and M. Mallavarapu, Isolation of purple nonsulfur bacteria for the removal of heavy metals and sodium from contaminated shrimp ponds, Electron. J. Biotechnol., 13, 3-4 (2010). 
  34. J. F. Imhoff and H. G. Truper, Purple nonsulfur bacteria, Bergey's Manual of Systematic Bacteriology, 3rd ed., 1658-1661, Williams & Wilkins, Philadelphia, United States (1989). 
  35. K. R. Girija, C. Sasikala, C. V. Ramana, C. Sproer, S. Takaichi, V. Thiel, and J. F. Imhoff, Rhodobacter johrii sp. nov., an endosporeproducing cryptic species isolated from semi-arid tropical soils, Int. J. Syst. Evol. Microbiol., 60, 2099-2107 (2010).  https://doi.org/10.1099/ijs.0.011718-0
  36. L. I. Crouch and M. R. Jones, Cross-species investigation of the functions of the Rhodobacter PufX polypeptide and the composition of the RC-LH1 core complex, Biochim. Biophys. Acta Bioenerg., 1817, 336-352 (2012).  https://doi.org/10.1016/j.bbabio.2011.10.009
  37. R. Gourdon, E. Rus, and S. Bhende, Sofer SS Mechanism of cadmium uptake by activated sludge, Appl. Microbiol. Biotechnol., 34, 274-278 (1990).  https://doi.org/10.1007/BF00166795
  38. L. Huang, Y. Xuan, Y. Koide, T. Zhiyentayev, M. Tanaka, and M. R. Hamblin, Type I and Type II mechanisms of antimicrobial photodynamic therapy: An in vitro study on gram-negative and gram-positive bacteria, Lasers Surg. Med., 44, 490-499 (2012).  https://doi.org/10.1002/lsm.22045
  39. E. Barbot, I. Seyssiecq, N. Roche, and B. Marrot, Inhibition of activated sludge respiration by sodium azide addition: Effect on rheology and oxygen transfer, Chem. Eng. J., 230-235 (2010). 
  40. X. Yang and X. Cui, Adsorption characteristics of Pb(II) on alkali-treated tea residue, Water Resour. Ind., 3, 1-10 (2013).  https://doi.org/10.1016/j.wri.2013.05.003
  41. R. Mopoung and N. Kengkhetkit, Lead and cadmium removal efficiency from aqueous solution by NaOH treated pineapple waste, Int. J. Appl. Chem., 12, 23-35 (2016). 
  42. A. Y. Dursun, G. Uslu, O. Tepe, Y. Cuci, and H. I. Ekiz, A comparative investigation on the bioaccumulation of heavy metal ions by growing Rhizopus arrhizus and Aspergillus niger, Biochem. Eng. J., 15, 87-92 (2003).  https://doi.org/10.1016/S1369-703X(02)00187-0
  43. C. Bar, R. Patil, J. Doshi, M. J. Kulkarni, and W. N. Gade, Characterization of the proteins of a bacterial strain isolated from contaminated site involved in heavy metal resistance-A proteomic approach, J. Biotechnol., 128, 444-451 (2007).  https://doi.org/10.1016/j.jbiotec.2006.11.010
  44. u. Acikel and M. Ersan, Acid phosphatase production by Rhizopus delemar: A role played in the Ni (II) bioaccumulation process, J. Hazard. Mater., 184, 632-639 (2010).  https://doi.org/10.1016/j.jhazmat.2010.08.083
  45. A. Mishra and A. Malik, Recent advances in microbial metal bioaccumulation, Crit. Rev. Environ. Sci. Technol., 43, 1162-1222 (2013).  https://doi.org/10.1080/10934529.2011.627044
  46. G. Wei, L Fan, W. Zhu, Y. Fu, J. Yu, and M. Tang, Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China, J. Hazard. Mater., 162, 50-56 (2009).  https://doi.org/10.1016/j.jhazmat.2008.05.040
  47. K. Takeno, K. Sasaki, M. Watanabe, T. Kaneyasu, and N. Nishio, Removal of phosphorus from oyster farm mud sediment using a photosynthetic bacterium, Rhodobacter sphaeroides IL106, J. Biosci. Bioeng., 88, 410-415 (1999).  https://doi.org/10.1016/S1389-1723(99)80218-7
  48. F. Italiano, A. Buccolieri, L. Giotta, A. Agostiano, L. Valli, F. Milano, and M. Trotta, Response of the carotenoids mutant Rhodobacter sphaeroides growing cells to cobalt and nickel exposure, Int. Biodeterior. Biodegradation, 63, 948-957 (2009).  https://doi.org/10.1016/j.ibiod.2009.05.001
  49. N. W. Woodbury, J. P. Allen, R. E. Blankenship, M. T. Madigan, and C. E. Bauer, The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant reaction centers of purple nonsulfur bacteria, Anoxygenic Photosynthetic Bacteria, 527-557, Springer, Berlin, Germany (1995). 
  50. C. L. Wang, P. C. Michels, S. C. Dawson, S. Kitisakkul, J. A. Baross, J. D. Keasling, and D. S. Clark, Cadmium removal by a new strain of Pseudomonas aeruginosa in aerobic culture, Appl. Environ. Microbiol., 63, 4075-4078 (1997).  https://doi.org/10.1128/aem.63.10.4075-4078.1997
  51. C. L. Wang, P. D. Maratukulam, A. M. Lum, D. S. Clark, and J. D. Keasling, Metabolic engineering of an aerobic sulfate reduction pathway and its application to precipitation of cadmium on the cell surface, Appl. Environ. Microbiol., 66, 4497-4502 (2000).  https://doi.org/10.1128/AEM.66.10.4497-4502.2000
  52. C. L. Wang, A. M. Lum, S. C. Ozuna, D. S. Clark, and J. D. Keasling, Aerobic sulfide production and cadmium precipitation by Escherichia coli expressing the Treponema denticola cysteine desulfhydrase gene, Appl. Microbiol. Biotechnol., 56, 425-430 (2001).  https://doi.org/10.1007/s002530100660
  53. S. Panwichian, D. Kantachote, B. Wittayaweerasak, and M. Mallavarapu, Removal of heavy metals by exopolymeric substances produced by resistant purple nonsulfur bacteria isolated from contaminated shrimp ponds, Electron. J. Biotechnol., 14, 2 (2011). 
  54. L. E., Macaskie and A. C. R. Dean, Microbial metabolism, desolubilization, and deposition of heavy metals: Metal uptake by immobilized cells and application to the detoxification of liquid wastes, Advances in Biotechnological Processes, 159-201, lan R. Liss, Inc., New York, United States (1989). 
  55. F. Veglio, F. Beolchini, and A. Gasbarro, Biosorption of toxic metals: an equilibrium study using free cells of Arthrobacter sp, Process Biochem., 32, 99-105 (1997).  https://doi.org/10.1016/S0032-9592(96)00047-7
  56. E. I. Yilmaz, Metal tolerance and biosorption capacity of Bacillus circulans strain EB1, Res. Microbiol., 154, 409-415 (2003).  https://doi.org/10.1016/S0923-2508(03)00116-5
  57. J. E. Sloof, A. Viragh, and B. Veer, Kinetics of cadmium uptake by green algae, Water Air Soil Pollut., 83, 105-122 (1995).  https://doi.org/10.1007/BF00482598
  58. J. S. Chang, R. Law, C. C. Chang, Biosorption of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21, Water Res., 31, 1651-1658 (1997). 
  59. I. Bakkaloglu, T. J. Butter, L. M. Evison, F. S. Holland, and I. C. Hancock, Screening of various types biomass for removal and recovery of heavy metals (Zn, Cu, Ni) by biosorption, sedimentation, and desorption, Water Sci. Technol., 38, 269-277 (1998). 
  60. M. Torres, J. Goldberg, and T. E. Jensen, Heavy metal uptake by polyphosphate bodies in living and killed cells of Plectonema boryanum (cyanophycae), Microbios, 96, 141-147 (1998). 
  61. R. Munoz and B. Guieysse, Algal-bacterial processes for the treatment of hazardous contaminants: A review, Water Res., 40, 2799-2815 (2006).  https://doi.org/10.1016/j.watres.2006.06.011
  62. F. A. Al-Momani, A. M. Massadeh, and Y. A. Hadad, Uptake of zinc and copper by halophilic bacteria isolated from the Dead Sea shore, Jordan, Biol. Trace Elem. Res., 115, 291-300 (2007).  https://doi.org/10.1007/BF02686003
  63. M. Gavrilescu, Removal of heavy metals from the environment by biosorption, Eng. Life Sci., 4, 219-232 (2004).  https://doi.org/10.1002/elsc.200420026
  64. M. Prado Acosta, E. Valdman, S. G. Leite, F. Battaglini, and S. M. Ruzal, Biosorption of copper by Paenibacillus polymyxa cells and their exopolysaccharide, World J. Microbiol. Biotechnol., 21, 1157 (2005).