Immobilization of Bacillus sp. Strain Neni-8 in Dialysis Tubing Reduced Copper Toxicity to the Molybdenum Reduction Process

Authors

  • Garba Uba Department of Science Laboratory Technology, College of Science and Technology, Jigawa State Polytechnic, Dutse, PMB 7040, Nigeria.
  • Aisami Abubakar Department of Biochemistry, Faculty of Science, Gombe State University, P.M.B 127, Tudun Wada, Gombe, Gombe State, Nigeria.
  • Hafeez Muhammad Yakasai Department of Biochemistry, Faculty of Basic Medical Sciences, College of Health Sciences, Bayero University Kano, Nigeria.

DOI:

https://doi.org/10.54987/bstr.v10i2.781

Keywords:

Bioremediation, Molybdenum, Molybdenum blue, Copper, Dialysis tubing

Abstract

In ruminants, even trace amounts of molybdenum can be lethal. In areas with high pollution, molybdenum levels in soil and mine tailings can exceed 20,000 ppm. Bioremediation of molybdenum can be challenging when toxic copper is also present. This research presents a novel approach using dialysis tubing and the molybdenum-reducing activity of Bacillus sp. strain Neni-8 for molybdenum removal from aqueous solutions. Molybdenum blue (Mo-blue), produced during enzymatic reduction, is insoluble in dialysis tubing and this can be a twofold advantage as a method of removal and as a method to protect bacterial cells from heavy metal inhibition, especially copper. In this experiment, we assess the toxicity-shielding effect of dialysis tubing for molybdenum reduction to Mo-blue by this bacterium in the presence of copper. As the concentrations of copper were increased, both free and immobilized cells were strongly inhibited. Modelling using the dissociationone-phase exponential decay model gave an IC50 value for the immobilized form of 0.1107 mg/L (95% confidence interval from 0.073 to 0.217 while the IC50 value for the free cell system was 0.023 mg/L (95% C.I. from 0.019 to 0.028). Since the confidence interval for the IC50 values did not overlap, the immobilized system gave better protection from copper than the free cell system. Toxicity to free cells was higher than toxicity to cells trapped in dialysis tubes, suggesting that trapping Mo-reducing cells may be an effective strategy for the bioremediation of water or wastewater contaminated with multiple heavy metals.

References

Padrilah SN, Ahmad SA, Yasid NA, Sabullah MK, Daud HM, Khalid A, et al. Toxic Effects of Copper on Liver and Cholinesterase of Clarias gariepinus. Environ Sci Pollut Res. 2017;24(28):22510-23.

Holan JR, King CK, Sfiligoj BJ, Davis AR. Toxicity of copper to three common subantarctic marine gastropods. Ecotoxicol Environ Saf. 2017 Feb;136:70-7.

Mashifane TB, Moyo NAG. Acute toxicity of selected heavy metals to Oreochromis mossambicus fry and fingerlings. Afr J Aquat Sci. 2014 Jul 3;39(3):279-85.

Kousar S, Javed M. Evaluation of acute toxicity of copper to four fresh water fish species. Int J Agric Biol. 2012;14(5):801-4.

Bone PA. Copper deficiency, molybdenum toxicity and copper toxicity: Where are we now? Cattle Pract. 2010;18(2):73-5.

Rusnam, Gusmanizar N, Shukor MY, Dan-Iya BI. Modelling the Effect of Copper on the Growth Rate of Enterobacter sp. strain Neni-13 on SDS. J Environ Microbiol Toxicol. 2021 Jul 31;9(1):10-5.

Espinosa CD, Stein HH. Digestibility and metabolism of copper in diets for pigs and influence of dietary copper on growth performance, intestinal health, and overall immune status: a review. J Anim Sci Biotechnol. 2021 Jan 11;12(1):13.

Rajput V, Minkina T, Sushkova S, Behal A, Maksimov A, Blicharska E, et al. ZnO and CuO nanoparticles: a threat to soil organisms, plants, and human health. Environ Geochem Health. 2019 May 20;

Shukor MY, Bakar NA, Othman AR, Yunus I, Shamaan NA, Syed MA. Development of an inhibitive enzyme assay for copper. J Environ Biol. 2009;30(1):39-44.

Shaw BJ, Handy RD. Dietary copper exposure and recovery in Nile tilapia, Oreochromis niloticus. Aquat Toxicol Amst Neth. 2006 Feb 10;76(2):111-21.

Pitt MA. Molybdenum toxicity: interactions between copper, molybdenum and sulphate. Agents Actions. 1976;6(6):758-69.

O'Doherty C, Keenan J, Horgan K, Murphy R, O'Sullivan F, Clynes M. Copper-induced non-monotonic dose response in Caco-2 cells. Vitro Cell Dev Biol - Anim. 2019 Apr 1;55(4):221-5.

Husain N, Mahmood R. Copper(II) generates ROS and RNS, impairs antioxidant system and damages membrane and DNA in human blood cells. Environ Sci Pollut Res. 2019 Jul 1;26(20):20654-68.

Yakasai HM, Rahman MF, Yasid NA, Ahmad SA, Halmi MIE, Shukor MY. Elevated Molybdenum Concentrations in Soils Contaminated with Spent Oil Lubricant. J Environ Microbiol Toxicol. 2017;5(2):1-3.

Smedley PL, Kinniburgh DG. Molybdenum in natural waters: A review of occurrence, distributions and controls. Appl Geochem. 2017 Sep 1;84:387-432.

Perrault JR, Buchweitz JP, Lehner AF. Essential, trace and toxic element concentrations in the liver of the world's largest bony fish, the ocean sunfish (Mola mola). Mar Pollut Bull. 2014;79(1-2):348-53.

McGrath SP, Micó C, Zhao FJ, Stroud JL, Zhang H, Fozard S. Predicting molybdenum toxicity to higher plants: Estimation of toxicity threshold values. Environ Pollut. 2010;158(10):3095-102.

Geelani R, Amin S, Balkhi M, Masood A. Role of molybdenum in the biological function of sulfite oxidase and sulfur dioxide toxicity. J Ind Pollut Control. 2007;23(2):299-306.

Battogtokh B, Lee JM, Woo N. Contamination of water and soil by the Erdenet copper-molybdenum mine in Mongolia. Environ Earth Sci. 2014;71(8):3363-74.

Lahann RW. Molybdenum hazard in land disposal of sewage sludge. Water Air Soil Pollut. 1976;6(1):3-8.

Yu C, Xu S, Gang M, Chen G, Zhou L. Molybdenum pollution and speciation in Nver river sediments impacted with Mo mining activities in Western Liaoning, northeast China. Int J Environ Res. 2011;5(1):205-12.

Kargar M, Khorasani N, Karami M, Rafiee GR, Naseh R. Study of aluminum, copper and molybdenum pollution in groundwater sources surrounding (Miduk) Shahr-e- Babak copper complex tailings dam. World Acad Sci Eng Technol. 2011;76:412-6.

Rusnam, Gusmanizar N. Isolation and Characterization of a Molybdenum-reducing and Coumaphos-degrading Bacillus sp. strain Neni-12 in soils from West Sumatera, Indonesia. J Environ Microbiol Toxicol. 2019 Dec 31;7(2):20-5.

Adnan M, Abu Zeid I, Ahmad SA, Effendi Halmi M, Abdullah S, Shukor M. A Molybdenum-reducing Bacillus sp. Strain Zeid 14 in Soils from Sudan that Could Grow on Amides and Acetonitrile. Malays J Soil Sci. 2016 Jan 1;20:111-34.

Yakasai MH, Ibrahim KK, Yasid NA, Halmi MIE, Rahman MFA, Shukor MY. Mathematical modelling of molybdenum reduction to mo-blue by a cyanide-degrading bacterium. Bioremediation Sci Technol Res. 2016 Dec 31;4(2):1-5.

Yakasai HM, Rahman MF, Manogaran M, Yasid NA, Syed MA, Shamaan NA, et al. Microbiological reduction of molybdenum to molybdenum blue as a sustainable remediation tool for molybdenum: A comprehensive review. Int J Environ Res Public Health. 2021;18(11).

Yakasai HM, Rahman MF, Manogaran M, Yasid NA, Syed MA, Shamaan NA, et al. Microbiological Reduction of Molybdenum to Molybdenum Blue as a Sustainable Remediation Tool for Molybdenum: A Comprehensive Review. Int J Environ Res Public Health. 2021 Jan;18(11):5731.

Sabullah MK, Rahman MF, Ahmad SA, Sulaiman MR, Shukor MS, Gansau AJ, et al. Isolation and characterization of a molybdenum-reducing and phenolic- and catechol-degrading Enterobacter sp. strain saw-2. BIOTROPIA - Southeast Asian J Trop Biol. 2017 May 22;24(1):47-58.

AbdEl-Mongy MA, Rahman MF, Shukor MY. Isolation and Characterization of a Molybdenum-reducing and Carbamate-degrading Serratia sp. strain Amr-4 in soils from Egypt. Asian J Plant Biol. 2021 Dec 31;3(2):25-32.

Rusnam, Rahman MF, Gusmanizar N, Yakasai HM, Shukor MY. Molybdate Reduction to Molybdenum Blue and Growth on Polyethylene Glycol by Bacillus sp. strain Neni-8. Bull Environ Sci Sustain Manag E-ISSN 2716-5353. 2021 Jul 31;5(1):12-9.

Rusnam, Rahman MF, Gusmanizar N, Yakasai HM, Shukor MY. Molybdate Reduction to Molybdenum Blue and Growth on Polyethylene Glycol by Bacillus sp. strain Neni-8. Bull Environ Sci Sustain Manag. 2021 Jul 31;5(1):12-9.

Sabo IA, Yahuza S, Shukor MY. Molybdenum Blue Production from Serratia sp. strain DRY5: Secondary Modeling. Bioremediation Sci Technol Res. 2021 Dec 31;9(2):21-4.

Zeid IMA, Rahman MF, Shukor MY. Isolation of A Molybdenum-reducing Bacillus sp. strain Zeid 15 and Modeling of its Growth on Amides. Bull Environ Sci Sustain Manag. 2021 Dec 31;5(2):19-27.

Manogaran M, Manogaran B, Othman AR, Gunasekaran B, Shukor MYA. Decolourisation of Reactive Red 120 by a Heavy Metal-tolerant Bacterium Isolated from Juru River, Malaysia. Bioremediation Sci Technol Res. 2020 Jul 31;8(1):23-6.

Wang M, Yin H, Peng H, Feng M, Lu G, Dang Z. Degradation of 2,2?,4,4?-tetrabromodiphenyl ether by Pycnoporus sanguineus in the presence of copper ions. J Environ Sci China. 2019;83:133-43.

El Deeb B, Altalhi AD. Degradative plasmid and heavy metal resistance plasmid naturally coexist in phenol and cyanide assimilating bacteria. Am J Biochem Biotechnol. 2009;5(2):84-93.

Shukor MS, Shukor MY. Bioremoval of toxic molybdenum using dialysis tubing. Chem Eng Res Bull. 2015;18(1):6-11.

Rahman MA, Ahmad SA, Salvam S, Halmi MIE, Yusof MT, Shukor MY, et al. Dialysis tubing experiment showed that molybdenum reduction in S. marcescens strain DrY6 is mediated by enzymatic action. J Environ Bioremediation Toxicol. 2013;1(1):25-7.

Halmi MIE, Ahmad SA, Yusof MT, Shukor MY, Syed MA. Entrapment of Mo-reducing bacterium increase its resistance towards heavy metals. Bull Environ Sci Manag. 2013;1(1):11-3.

Halmi MIE, Wasoh H, Sukor S, Ahmad SA, Yusof MT, Shukor MY. Bioremoval of molybdenum from aqueous solution. Int J Agric Biol. 2014;16(4):848-50.

Komori K, Rivas A, Toda K, Ohtake H. A method for removal of toxic chromium using dialysis-sac cultures of a chromate-reducing strain of Enterobacter cloacae. Appl Microbiol Biotechnol. 1990;33(1):117-9.

Shukor MY, Rahman MF, Shamaan NA, Syed MS. Reduction of molybdate to molybdenum blue by Enterobacter sp. strain Dr.Y13. J Basic Microbiol. 2009;49(SUPPL. 1):S43-54.

Sau GB, Chatterjee S, Mukherjee SK. Chromate reduction by cell-free extract of Bacillus firmus KUCr1. Pol J Microbiol. 2010;59(3):185-90.

Chee HS, Manogaran M, Suhaili Z, Yakasai MH, Rahman MFA, Shamaan NA, et al. Isolation and characterisation of a Mo-reducing bacterium from Malaysian soil. Bioremediation Sci Technol Res. 2017 Dec 31;5(2):17-24.

Roane TM, Josephson KL, Pepper IL. Dual-Bioaugmentation Strategy To Enhance Remediation of Cocontaminated Soil. Appl Environ Microbiol. 2001 Jul;67(7):3208-15.

Hettiarachchi GM, Pierzynski GM, Ransom MD. In situ stabilization of soil lead using phosphorus and manganese oxide. Environ Sci Technol. 2000;34(21):4614-9.

Babich H, Stotzky G. Effect of Cadmium on Fungi and on Interactions Between Fungi and Bacteria in Soil: Influence of Clay Minerals and pH. Appl Environ Microbiol. 1977 May;33(5):1059-66.

Kamel Z. Toxicity of cadmium to twoStreptomyces species as affected by clay minerals. Plant Soil. 1986 Jun 1;93(2):195-203.

Yoon KP. Construction and characterization of multiple heavy metal-resistant phenol-degrading pseudomonads strains. J Microbiol Biotechnol. 2003;13(6):1001-7.

Chun JW, Ho EM. Effect of Several Physicochemical Factors on the Biodegradation of Acrylamide by Pseudomonas sp. JK-7 Isolated from Paddy Soil. Korean J Microbiol. 2004;40(1):29-36.

Xie Q, Yang G, He G. Isolation and characterization of a phenol degrading bacterium PN6-15. Huazhong Keji Daxue Xuebao Ziran Kexue BanJournal Huazhong Univ Sci Technol Nat Sci Ed. 2009;37(8):129-32.

Bakhshi Z, Najafpour G, Kariminezhad E, Pishgar R, Mousavi N, Taghizade T. Growth kinetic models for phenol biodegradation in a batch culture of Pseudomonas putida. Environ Technol. 2011;32(16):1835-41.

Yusuf I, Shukor MY, Syed MA, Yee PL, Shamaan NA, Ahmad SA. Investigation of keratinase activity and feather degradation ability of immobilised Bacillus sp. Khayat in the presence of heavy metals in a semi continuous fermentation. J Chem Pharm Sci. 2015;8(2):342-7.

Mohanty SS, Jena HM. Biodegradation of phenol by free and immobilized cells of a novel Pseudomonas sp. nbm11. Braz J Chem Eng. 2017 Mar;34:75-84.

Babalola M, Ayodeji A, Bamidele O, Ajele J. Biochemical characterization of a surfactant-stable keratinase purified from Proteus vulgaris EMB-14 grown on low-cost feather meal. Biotechnol Lett. 2020 Dec 1;

Kai EX, Johari WLW, Habib S, Yasid NA, Ahmad SA, Shukor MY. The growth of the Rhodococcus sp. on diesel fuel under the effect of heavy metals and different concentrations of zinc. Adv Polar Sci. 2020 May 12;132-6.

Downloads

Published

2022-12-31

How to Cite

Uba, G., Abubakar, A., & Yakasai, H. M. (2022). Immobilization of Bacillus sp. Strain Neni-8 in Dialysis Tubing Reduced Copper Toxicity to the Molybdenum Reduction Process. Bioremediation Science and Technology Research (e-ISSN 2289-5892), 10(2), 45–49. https://doi.org/10.54987/bstr.v10i2.781

Issue

Section

Articles